Annals of the Missouri Botanical Garden ; contains papers, primarily in systematic botany tanical Garden, St. Louis. Papers originating outside . All manuscripts are peer-reviewed by qualified, in- to ations x are ni in the back of the last issue “Roy E. Deut Latin Edi B Missouri Botanical Garden | — — Tham A AbShebbaz: Missouri Botanical Garden .— Gerrit Davidse Missouri Botanical Garden Peter Goldblatt | Missouri i Botanical Garden S Gordon McPherson RaT Missouri i Botanical Garden ` I Fadoua Taylor Missouri Botanical Garden Henk van der Werff a issouri Botanical Garden ce niea MO 631 10. Pentel) sR : 7 : additional mail- 0 EE ppp aaa n r eee ss A A AAA SA E ESS Volume 97 Annals Number 1 of the 2010 wissour:sotanicAl Missouri npr 19200 Botanical GARDEN LIBRARY (arden Y OBSERVATIONS ON THE FLORAL Kuo-Fang Chung,? Henk van der Werff, and MORPHOLOGY OF SASSAFRAS RANDAIENSE (LAURACEAE) Ching-I Peng* ABSTRACT The floral morphology been well documented. Consequently much confusi bs the spring of 2007. 7 e inflo of Sassafras randaiense (Hayata) Rehder — a rare spec on exists in taxonom ies endemic to Taiwan, has never c literature regarding its flower structure and orescences of S. randaiense are highly reduced panicles to botryoid cymes, with up to 10 such inflorescences shukan6q ipai mappe to form an umbel ne miu gs ymes. Its flowers uraceae. Our observations also revealed that its — are protogynous and eet ina reproductive shoot alternate their d phase of Cae dichogamy. The temporal dioecy imposed by T described as a a ndrodioecious, or polyga this sexual system n ex poa suggesting the sexual syste ain why S. randaiense has d ous species in the gue “Floral morphology, Lauraceae, plant br: y system, Sassafras, Taiwan, taxonomy. Sassafras J. Presl pey comprising S. albidum (Nutt.) Nees in eastern North America, S. tzumu (Hemsl.) Hemsl. in oiled China, and S. randaiense (Hayata) Rehder in Taiwan (Rehder, 1920), is a classic example of eastern North American and East Asian disjunct distribution (Wen, 1999; Nie et al., 2007). This small genus is well circumscribed by a combination of features: deeply fissured bark, deciduous habit, late winter to early spring blossom before the unfolding of young leaves, and leaves that are often trilobed when young (Rehder, 1920; Keng, 1953). Anatomically, Sassafras is the only genus in Lauraceae with typical — s wood (van der Werff & Richter, 1996). The flower structure and sexuality of the three species, however, exhibit considerable variation that in the past was exagger- ated as of generic importance, causing much taxo- nomic controversy (Rehder, 1920; Keng, 1953). We thank Peter Raven for encouraging us to pursue this study and for helpful discussions; Arnold Arboretum (Harvard fm and Taiwan Forestry Research Institute for the high-resolution digital images of Sassa fras Ju ript; and Chieh-I Huang and Chieh-Hua Liu for field assistance. randaiense collections; Helpful comments a. mt by V. pia : Rohwer, and s. n are greatly appreciated. This work was rted i EC. School of dun mal kuofangchung@ntu. edu.tw > Missou uri Botanical Ga des compede bopeng@sinica.edu.tw doi: 10.3417/2008029 O. Box 299, St. Louis, Missouri Herbarium (HAST), Bie | Research Cines. Academia Sinica, Nangang, Taipei 1 e Conserv en National Taiwan s Daan, Taipei 10617, Taiwan. i 63166-0299, U.S.A. henk.vanderwerff@mobot.o 1529, Taiwan. ino for Ann. Missourt Bor. Garb. 97: 1-10. PUBLISHED ON 31 MancH 2010. Annals of the Missouri Botanical Garden Nevertheless, the monophyly of the three Sassafras species has been confirmed by a recent molecular phylogenetic study (Nie et al., 2007). Results from Nie et al. (2007) = ener un kipa thit its sami the Tertiary boreotropical flora (Wolfe, 1975; "me et " ). Compared to its North American and mainland Chinese congeners that are commonly found in their native o (Rehder, 1920), Sassafras randaiense is only sparsely found in the mid clean pagues m) of the island and was ranked le (VU) according to IUCN Red List criteria iu & MR 1996; IUCN, E i Taiwan, this making high-value furniture (Lu et al., 1982; Wang et al., 1991; Yang et al., 2000) and is well known by the public as "e "t wa plant of 5 JOEY sepe Nan Sonan) whose ibeqüls feed exclusively on the foliage eS S. ra ege pue et a ATMA Saniter of of this rare Lad valuable tree in the past — decades (e.g., Hu, 1979; Lu et al., 1982; Chen €: pa 1985; Wang et al., 1991; Lin, 1992; Yang et al., 2000 Lin et al., 2003; Cuin et al., 2006). However, faced by its low and variable annual seed production, deep seed dormancy, and low rate of successful asexual propagation, cultivation of S. randaiense remains one of the biggest challenges for forestry in Taiwan During the course of pre paring the treatment of Sota for Flora of China, the second author oticed that, in recent taxonomic literature, Sassafras ien was almost unanimously described as a polygamous species by local taxonomists (e.g., Liu, 1960; Liu, 1970; Chang, 1976; Liu & Liao, 1980; Ying, 1985; ls 19%, = omre Rohwer e ls functionally unisexual "Boden. À survey ra taxonomic literature also revealed that the inflores- cences of S. randaiense had been dese ribed variousl as either racemose (e.g., Hayata, 1911; Rehder, 1920. Kamikoti, 1933; Kanehira, 1936; Liu, 1960; Liu, 1970; Chang, 1976; Li et al., 1982; Lu et al., 1982) or paniculate (e.g., Liu & Liao, 1980; Ying, 1985; Liao, . 1996). Another discrepancy appeared when Kamikoti (1933) described pollen sacs of the third- whorl i of S. e as open at the ns majority of the taxonomists (e.g, Ha a i. “1911: Kanehira, 1936; Keng, 1953; Liu, 1960; Li, 1963 Chang, 1976; Ying, 1985; Liao, 1988, 1996; Rohwer, 1993). Because inflorescence types and flower struc- ture are I > Su CIS for La we were praed m lo carefully review relevant taxonomic literature and conduct field observations to clarify the floral morphology of S. randaiense. TAXONOMY OF SASSAFRAS Characterized by distinct staminate and pistillate als he. enh. American Sassafras albidum is (van der Werff, 1997). Its pistillate flowers Mo six staminodia surrounding the long-styled gynoecium (van der Werff, 1997). The staminate flowers of S. albidum have nine normal stamens in three whorls with a pair of stalked glands attached to the base of each of the third-whorl filaments. All anthers are apparently introrse. The fourth-whorl staminodia and the central gynoecium commonly observed in a typical laurel flower may be lacking in the staminate flowers of the D For a long time, S. albidum was thought to be the only s of the genus Sassafras with an isolated diebns in eastern North America (Rehder, 1920). In 1891, Hemsley described two species, Litsea laxiflora Hemsl. and Lindera tzumu Hemsl., based on flowering and fruiting materials collected by Augus- tine Henry from Hubei, China. In 1906, E. H. Wilson, prior to his departure for the third botanical exploration to China, suggested to Hemsley that Litsea laxiflora and Lindera tzumu, together with materials collected by Wilson himself from China, were conspecific with the North American Sassafras bidum (Hemsley, 1907a). Inspired by Wilson’s proposition, Hemsley reexamined the materials and published an article in which he transferred Lindera tzumu to Sassafras (as S. tzumu (Hemsl.) Hemsl.) and synonymized Litsea laxiflora under S. tzumu (Hems- ley, 1907a). In this and the companion papers, Hemsley described S. tzumu as a dioecious species with very similar male and female flowers (Hemsley, 1907a, b), differing from S. albidum by the presence of the staminodia and pistillode in both male and female flowers. The flowers of S. Am however, were interpreted as being hermaphroditic by Lecomte (1911, 1913). Emphasizing n difference between dioecy and hermaphrodite, Lecomte (1911) estab- lished Pseudosassafras Lecomte for the plant occur- = in China. A few years later, Wilson’s D the flower sexuality of S. tzumu in China did in Plantae Wilsonianae (Gamble, m! h this account, Wilson (in Gamble, 1916: 74) suggested that flowers of S. tzumu "though apparently hermaph- rodite are functionally unisexual and my observations lead me to believe that they are polygamo-dioecious." The endemic Sassafras randaiense, uniquely characterized E 2-celled anthers, was first scri as Lindera randaiensis Hayata ue 1911). The type specimen (S. Kusano s.n., 1908, Taiwan A E Volume 97, Number 1 Chung et al. Floral Morphology of Sassafras randaiense M, N) was interpreted as a staminate individual a du alleged Lindera Thunb. species by Hayata (1911). In the fall of 1918, accompanied Kanehira and S. Sasaki, E. H. Wil species in Alishan (Arishan) i According to Kanehira’s notes (1920, 1936), Wilson collected both fruiting and male flower materials and immediately recognized the close affinity of L. randaiensis with Sassafras. Wilson’s observation and intuition, however, were not accepted by Hayata, whose taxonomy emphasized the importance of anther the classification of Lauraceae differing mainly in the 2- versus 4-loculed anthers and the lesser tendency of the lateral lobing in the former species. In this article, L. randaiensis was transferred to Sassafras and was described as an androdioecious species (Rehder, 1920). In the same article, Rehder (1920) also synonymized Pseudosassafras under Sassafras and suggested that flowers of S. tzumu were hermaphroditic but functionally unisexual. Despite Rehder’s treatment, the recognition of Pseudosassafras as a separate genus endemic to East Asia was followed number of taxonomists (e.g., Handel-Mazzetti, 1931; Liou, 1934; Nakai, 1940). Emphasizing the m ce of 2- versus 4-celled anthers, Kamikoti (1933) created Yushunia Kamik. to accommodate the 2-celled Y. randaiensis (Hayata) Kamik. Although Kamikoti (1933) did not comment on the sexuality of . randaiensis, he described Yushunia as dioecious. Yushunia was later criticized as unnatural by im (1940), who instead treated Y. randaiensis as a vari of Chinese sassafras (as P. laxiflorum (Hemsl.) e var. randaiensis (Hayata) Nakai). In December 1920, Kanehira published an article n Japanese, in which he recorded Wilson's field observations of Lindera randaiensis in Alishan and accepted Rehder’s (1920) new treatment of Taiwan sassafras. In 1936, the second edition of Kanehira’s Formosan Trees Indigenous to the Islands, a taxonomic masterpiece in Taiwan, was published. In this work, however, Kanehira did not comment directly on the sexuality of Sassafras randaiense. Instead, he briefly escribed the morphology of male flowers and mentioned that the female flowers were often inter- mixed with them (Kanehira, 1936). Interestingly, in the illustration, S. randaiense was depicted as an androdioecious species, and a male flower lacking the fourth-whorl staminodia (Kanehira, 1936), resembling that of S. albidum In 1953, Keng published a taxonomic revision of Sassafras in which he basically followed the generic with a hermaphroditic flower concept of Rehder (1920) except for further dividing Sassafras into two subgenera. Keng (1953) placed S. albidum in subgenus Sassafras and the two East Asian species in subgenus Pseudosassafras (Lecomte) H. Keng. Keng’s (1953) interpretation on the sexuality of the Asian species, however, was somewhat confusing. Although Keng referred to Wilson’s comment (Gam- ble, 1916; see above) on the sexuality of the two Asian species as “the pistillate flowers of the two eastern Asiatic species are apparently hermaphrodite” (Keng, 1953), he concluded his investigations with a series of comparisons between staminate and pistillate flowers of the three Sassafras species in the taxonomic key, floral diagrams, and table appended to the paper (Keng, 1953). The differences between the staminate and pistillate flowers of the two Asian species, however, are minor, with staminate flowers character- ized by relatively larger androecium and smaller gynoecium in comparison to those of the pistillate flowers (Keng, 1953). In a monumental dendrology textbook titled Mustra- tions of Native and Introduced Ligneous Plants of Taiwan by T. S. Liu (1960), Sassafras randaiense was ane as a S aus species. In that book, the was basically a Chine bandade of Kanehira’s Japanese text (1936). In is illustration of the ipee, — are two figures each le flower (Fig. 2L), respectiv: buds, that are very similar to the line drawings in Kanehira (1936). Subsequent to Liu's treatment (1960), nearly all taxonomic and floristic works of Lauraceae in Taiwan described S. randaiense as a polygamous E (Liu, 1970; Ei 1976; Liu & Liao, 1980; Ying, 1985; Liao, 1988, 1 wever, Chang (1976) en Liao (1988, 1996) did not follow E description of the male flowers in Kanehira (1936) and Liu (1960); instead, their description of the male > EAS a L l A | LECT TT 1 depicting a 2 depicted in Hayata (1911). In their article titled “Studies on the propagation of Taiwan sassafras,” Lu et al. (1982) studied embryol- ogy and seed physiology of Sassafras randaiense. After examining a considerable numbers of flower buds, Lu et al. (1982) concluded that flowers of Taiwan sassafras are bisexual. Lu et al. (1982) also commen- ted that, although flowers of the type specimen of S. randaiense were interpreted as staminate (ovary nonfunctional) bs Hayata (1911), they were appar- ently bisexual. However, the work of Lu et al. (1982) has been rarely cited by recent taxonomic works To facilitate the understanding of the complicated taxonomic history of Sassafras randaiense, the nomen- clature of the species is listed below. Full lists of synonyms of S. albidum and 5. tzumu are av: 'ailable in van der Werff (1997) and Li et al. (2008), respectively. 4 Annals of the Missouri Botanical Garden 25°N 249N O 20 40 22N 120°E 121E 122€ Figure 1. Distribution Sassa wate gay on 1 D of ras randaiense ho ma mei ša Tawm based on trace at HAST, TAI, and = li Fans in the herbarium. The number i delimits mountainous re m id " he numbers of enin studied at each locality. The shaded are i yuan (1600 m), 16 Jan. 2007. Hz, i stay localities (voucher specimens are all deposited at HAST) include A, (2025 m), 9 Feb. 3000. D, E :B. k unachibkusa (2100 m), 8 Feb. 2007, Huang 2993; e ` , Kuanwu Lodg (1550 m), 9 Feb. ature Reserve (1950 m), 9 Feb. Talu Forest Rd. ET Mere pue TM IL MET i 2007, Huang 3016; H, Taipingihan Rd. (1600 m), 13 Feb. 2007, Huang 30 Chung et al. 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Arnold Arbor. 1: 244. 1920. Basionym: Lindera (Hayata) Kamik., Annual Rep. Taihoku Bot. 3: 78. 1933 [1934]. Pseudosassafras laxiflorum var. randaiensis (Hayata) Nakai, J. Jap. Bot. 16: 126. 1940. TYPE: Taiwan. Mt. Randaizan, 1908, S. Kusano s.n. (holotype, TI!). METHODS In January and February 2007, we conducted field trips to eight localities in Taiwan (Fig. 1) to collect and observe flowers of Sassafras randaiense in their natural habitats. Because Taiwan sassafras trees are tall and often grow on steep mountain slopes, tagging was essentially impossible for the trees we observed. A total of 20 trees were observed. For each of the 20 plants, three to five flowering branches were collected by an extensible (to 40 ft.) pole pruner. One to three flowering shootings were pickled. Pickled flowers and voucher specimens are deposited in the Herbarium of cademia Sinica, m (HAST). floral morphology Measurements of re based on one to three pickled flowering buds. in of flowers and flowering branches were taken in the field. Collecting sites in northern Taiwan (sites A, C-H, Fig. 1) were revisited in June and July 2007. Site B (Fig. 1) was not revisited because of its poor accessibility. RESULTS Measurements and observations of floral morphol- ogy of the 28 reproductive shoots of 20 Sassafras randaiense trees, including the number of inflores- cences per reproductive shoot, number of flowers per orescence, infloresce ype, inflorescence CE sexual D es uis cell number, are summarized in Table INFLORESCENCE MORPHOLOGY Young inflorescences of Sassafras randaiense are enclosed in a vegetative winter bud (Weberling, 1988, 1989) by four to six decussate bracts (cataphylls, Weberling, 1988, 1989; Fig. 2A), as described by Rohwer (1993). These bracts have been often misinterpreted as involucre (e.g., Liao, 1996). The inflorescence of S. randaiense is determinate, ending with a terminal flower (Fig. 2A—C). On average, about 13 flowers (7-23 [12.68 + 3.19, N = 147]; Table 1) of Taiwan sassafras are arranged in a highly reduced panicle (62.8%) or raceme-like cyme (37.2%) (Fig. 2A). The determinate racemes are better termed botryoid cymes (e.g., Rohwer, 1993; Li & Christophel, 2000) to distinguish from true racemes, which are indeterminate inflorescences (sensu Weberling, 1988, 1989). In S. randaiense, the average length of the inflorescence is 4.18 cm (2.58 cm [4.18 — 1.22, N — 145], much longer than previously reported (i.e., 3 cm; Hayata, 1911; Keng, 1953; Liao, 1996). Up to 10 (3-10 [5.54 + 1.56], N = 28) id cymes are then tightly clustered around the panicles and/or vegetative terminal bud (pseudoterminal), giving the appearance of an umbel of panicles and/or botryoid cymes (Fig. 2C). After the early spring flowering stage, the vegetative terminal buds turn into a normal leafing branch and elongate (van der Werff, 2001), as shown in Figure 2D. The overall appearance of the inflorescences of S. randaiense described above conforms well to the group 1 inflorescence type that is characteristic of the tribe Laureae (sensu van der Werff & Richter, 1996). FLOWER MORPHOLOGY All observed flowers of Sassafras randaiense ix tepals in two whorls, and three sagittate staminodia as the fourth whorl, with a central gynoecium (Figs. 2E-K). The third-whorl stamens possess a pair of globose glands at the base of each filament (g in Fig. 2E). A majority of the anthers are 2-locular (Fig. 2E, G, I, J); however, flowers with 3- celled (Fig. 2F) and 4-celled (Figs. 2H, K) anthers were also observed (Table 1). Specifically, three observed trees in Litaishenmuyuan, Chilanshan area P 2977), have 4-celled or a mixture of 2-celled d 4-celled anthers. While anthers of the first and idi stamen whorl are introrse (Fig. 2F, C), those of the third whorl are apparently extrorse or latrorse (Fig. 2F, G, J) but never introrse. When flowers are in the male phase (see below), those of the third whorl are apparently extrorse (Figs. 2G, I, J). The flower comprise (from the outside inward) si whorls, nine stamens in three < phase, arrowhead points to an iiri third- -whorl anther Uang 3008, 1: 56 pm). —J. Flower in male phase (Huang 3008, 235 PM). —K. Flower i elled er (Huang 2978, 16 Jan. 2007). —L. Illustration of a male flower in Liu (1960). —M. — of pd diia Pis (S. Kusano s.n., TI). —N. Flowering branch of the holotype. Scale bars: A-D, N = 1 cm; E-K = Annals of the Missouri Botanical Garden structure of S. randaiense thus fits perfectly with the typical hermaphroditic flowers of Lauraceae (Rohwer, 1993; van der Werff, 2001). In no case have we observed any flower that showed the characteristics of the male flower (Fig. 2L) as depicted in Kanehira (1936) and Liu (1960). The distinction between introrse and extrorse anthers of the third-whorl stamens of a hermaphroditic laurel flower was considered crucial in the taxonomy of Lauraceae (van der Werff & Richter, 1996) and has been used frequently in taxonomic keys at the generic level (e.g., van der Werff, 1991; Rohwer, 1993). In the taxonomic literature in Taiwan, this character is widely used, and Sassafras randaiense has routinely keyed out by the introrse anthers of its third-whorl stamens (e.g., Li, 1963; Liu & Liao, 1980; Ying, 1985; Liao, 1988, 1996; Liu et al., 1994; Yang et al., 1997). However, because filaments of many laurel species are long and become twisted after desiccation, this character is difficult to observe correctly and its application in taxonomic identification is problematic (van der Werff, 2001). Our differing observations on this subject therefore necessitate a revision of such taxonomic keys for the Lauraceae. FLOWER BEHAVIOR AND POSSIBLE SEXUAL SYSTEM OF SASSAFRAS RANDAIENSE In addition to being apparently hermaphroditic, flowers of Sassafras randaiense are clearly protogy- way from the stigma and stamens bend further toward the first- (Fig. 2E). In Figure 2F and H, the stigma is wilted and the third-whorl stamens are no longer in close contact with the first-whorl stamens. In Figure 2G and J, the three third-whorl stamens bend further inward. exposing the extrorse anthers and enclosing the gynoecium. If the third-whorl anthers of S. randaiense were introrse as described by a majority of previous authors, pollen of these innermost anthers would not be dispersed away from the flower. whorl stamens onou y comprise two flower morphs that differ in the timing of flower opening. It is called synchronous because all flowers within an individual plant alter their sexual phases synchronously. In P. : americana, for example, flowers of the first morph enter the female phase in the morning, wilt and close at noon _ to emerge as male phase in the afternoon, and close again in the evening. The second-morph individuals, on the contrary, start the same cycle in the afternoon, resulting in a temporal dioecy for the species (Stout, 1927; Kubitzki & Kurz, 1984). However, to confirm the ; existence of synchronous dichogamy in S. randaiense, it. would be necessary to tag and to follow a population of individuals in the field (McDade, 1986; Renner, 2001; Utteridge & Saunders, 2001). Although we were unable to perform such investigations in 2007 due to the difficulty of accessing the tall Taiwan sassafras trees in their natural habitats, we have recently located other populations that are suitable for pursuing more sophisticated studies on the reproductive biology of S. randaiense in the next flowering season. The protogynous and possibly synchronous dicho- gamy of Sassafras randaiense also explains why this species had been associated with several kinds of sexual systems (e.g. androdioecy, Rehder, 1920; dioecy, Kamikoti, 1933; polygamy, Liu, 1960). When flowers of Taiwan sassafras are found in their female phase (e.g., Fig. 2E, K), the flowers are usually described as hermaphroditic. However, when flowers on the plant are found in the male stage, the wilted gynoecia are likely to be interpreted as nonfunctional and the plant likely to be interpreted as a staminate individual. Although the condition of the holotype (Fig. 2M, N) did not allow us to closely examine its flowering stage, the type cimen is likely to represent a male-phased individual of S. randaiense. QUESTIONS OF MALE FLOWERS The apparent hermaphroditic condition of Sassafras randaiense led us to question the identity and authenticity of the particular male flower (Fig. 2L) depicted in Kanehira (1936) and Liu (1960). Similar to the line drawing (e.g., Fig. 2L), Kanehira's description on the male flower did not include staminodia (Kanehira, 1936), nor did the description in Liu (1960). Although Hayata (1911) probably misinterpreted the male-phased bisexual flowers as male flowers, the fourth-whorl staminodia are clearly present in the type specimen and precisely described by Hayata (1911). According to the notes in Kanehira (1920, 1936) that Wilson collected fruiting and male flower materials in Arishan in October 1918, the line drawings of Kanehira (1936) and Liu (1960) were likely based on specimens collected during that trip. However, Kanehira's notes on the phenology of w ras are problematic because S. ran- Volume 97, Number 1 2010 Chung et al. Floral Morphology of Sassafras randaiense daiense normally blooms in the late winter to early spring (mid December to late March). To trace the source of the male flower depicted in Kanehira (1936) and Liu (1960) and validate the accuracy of these two illustrations, we examined the specimens collected by Wilson and Kanehira currently housed in A and TAIF, respectively. Interestingly, we found no qe material among Wilson's collections (E. H. on 0800 and E. H. Wilson 10800a at A) that had E examined by Rehder (1920) as well as specimens collected by R. Kanehira and S. Sasaki on the same trip with E. H. Wilson (R. K. Kanehira & S. Sasaki 10682-10688 a t TAIF; d E ee a credible mates s en, it asonable question the nl of i line peat in Kanehira (1936) and Liu (1960) as well as Wilson's observation recorded by Kanehira (1920, 1936). SUMMARY Our field observations on Sassafras randaiense clarify its inflorescence and flower morphology and suggest that its sexual system is likely synchronous dichogamy. Given the significant publicity economic interest of S. randaiense rather unusual that, except for Lu et al. (1982) and possibly Kamikoti (1933), very few botanists had critically examined the flowers an uctive biology of this species. One possible ime; is that, because this easily recognized species poses no difficulty in the taxonomy of Lauraceae in Taiwan, there is no demanding need for a critical study of its flower morphology. Our findings on protogyny and possibly synchronous dichogamy of S. randaiense can also explain, at least in part, why its seed production is low and variable. As is well documented in Persea whose sexual system is synchronous B ben in the absence of the two morphs o avocados growing in close proximity, the crop yield of avocado is extremely low (Stout, 1927). Our subse- in populations of S. randaiense where the distribution of trees was scattered, with the closest 1). By contrast, in localities where individual t = are less than 100 m apart - H in Fig. E abundant seed production was observed (e.g., Fig. 2D). However, further field studies are iind to confirm the existence of synchronous dichogamy in S. randaiense and its influence on its seed production. Literature Cited — C.-E. 1976. Lauraceae. Pp. 406—468 in H. L. Li, T.-S Liu, T.-C. Huang, T. Koyama & C. E. DeVol (editum) Flora of Taiwan, Vol. 2. Epoch Publishing Co., Taipei. Chen, M.-H. & P.-J. Wang. 1985. Somatic embryogenesis and plant regeneration on Sassafras randaiense (Hay.) Redh. e . Bull. Acad. Sin. 26: 1-12. Denk, T., F. Grimsson & Z. Kvaéek. 2005. The Miocene floras M: Icelim d and their significance for late Cainozoic fene — biogeography. Bot. J. Linn. 49: iudi. T G. 1916. Lauraceae. Pp. 66—86 in C. S. Sargent (editor), I Wilsonianae, Vol. 2. The University Press, Cambridg Guan, B. T., W. Pa “Kuo, S.-T. Lin & C.-F. Yu. 2006. Short- distance dient of intact Taiwan sassafras fruits in a te I p rain forest of northeastern Taiwan. Bot. i andel- en i. H. 1931. Symbolae Sinicae, Vol. 7. Julius x nger, Vienna. Hayata, B. 1911. Materials E the flora of Formosa. J. Coll. Sci. Imp. x4 ae ga qi. Hemsley, ee J. Linn. Soc., Bot. 26: 0-393. . 1907a. Sassafras in China. Bull. Misc. Inform. Kew E 1907b. Sassafras tzumu. Hooker’s Icon. Pl. 29: tab. Hsu, Y.-F., C.-C. Chen & P.-S. Yang. 1986. The orm review on the endemic butterflies in Taiwan. Mem. Col . Natl. Taiwan Univ. 26: 55-69 (In Chinese, on English summary). Hu, C.-Y. 1979. Introduction to the research project on Sassafras propagation. Taiwan Forest. 5: 30-31 (In Chinese). IUCN. 2001. IUCN Red List Categories and Criteria, Version 3.1. Prepared by the IUCN Species Survival Commission. IUCN, Gland, Switzerland, and Cambridge, United King- om. — : 1933. Neue und kritische Lauraceeen aus aiwan. I. Ann. Rep. Taihoku Bot. Gard. 3: 77-80. oia, R 1920. On sassafras in — Trans. Nat. Hist. Soc. Formosa 10: 270-272 (In Japane . 1936. Formosan Trees In a to the Islands, 2nd ed. Department of Forestry, Government Research Institute, Taihoku (In Japanese, with pi e ry s H. 1953. A taxonomic —— of S as (Laur- ae). Quart. J. Taiwan Mus. 6: 78-85. Rubio, K. & H. Kurz. 1984. Sen :hronized dichogamy and oecy in Neotropical Lauraceae. Pl. Syst. Evol. 147: 253 ; Lecomte, H. 1911. Sur un Pseudosassafras de Chine. Notul. Syst. eon 2: 266-210. —. a. Eee H. Lee. Nouv. Arch. Mus. Hist. - ser. 9, 5 Li, H.-L. 1 963. Woody Flora of Taiwan. Livingston Publish- ing Co., Narberth esiti N i, S.-K. nm Yang, P.-H. E T Z.-D. Shia & 1982. Laura ED H.W y. Li (editor), Flora rai ae — Sinicae, Vol. 31. Science Press, Beijing (In Chine Li, J. & "D.C Christophel. 2000. Systematic > onships within qa Lese mplex (Lauraceae): A cladistic analysis on the basis of morphological and leaf cuticle data. Austral. S=. Bot. 13: 1-13. Li, X. W., J. Li & H. van der — 2008. — m Pp. 159- M l in Z. Y. Wu, P. H. Rav Hung (editors), Flora of China, aa 7 (Menispermaceae el Capparaceae). Science Press, Beijing, and Missouri Botanical Garden, St. Louis Annals of the Missouri Botanical Garden Liao, b e The Taxonomic Revisions of the Family n Taiwan. Department of Forestry, National Taiwan. Docs Taipei. . 1996. Lauraceae. Pp. 433-499 in Editorial Committee of the Flora of Taiwan (editor), Flora of Taiwan, 2nd ed., Vol. 2. Editorial Committee of the Flora of Taiwan, Taipei. Lin, J.-H., B. T. Cuan, S.-T. Lin & C.-F. Yu. 2003. Attributes of leaves on reproductive shoots of Taiwan sassafras leid randaiense (Hay.) Rehder) at Chilan Shan, ern Taiwan. J. Exp. Forest Natl. Taiwan Univ. 17: 2532 (h (In E with English abs tract). Lin, T.-P. 1992 od of Mu. the deep dormancy of e ae ie S E ehd. seed. Pp. 365-368 in S.-C. Huang, S.-C. Hsieh & D.-J. Liu (editors), The Impact of Biological Research on Agricultu E i Breeding R. Asian and Oceania VR Symposium. Society for the ipic of Breedin Research in Asian and Oceania, Ch Ns H. 1934. Lauracées de Chine et d'Indochine. Hermann & Cie, Paris. Liu, T.-S, 1960. Illustrations of Native and In troduced Ligneous Plants of Taiwan, Vol. 1 1. College Z Agriculture, National Taiwan University, Taipei (In Chi ese). & C.-J. Liao. T Dend rology, "Vol. 1. The Com ss, Lid., i (In Chin - Liu, Y. "C 1970. Colored lu of Important Trees in Taiwan. National Chung-Hsing University, Taichung (In T Chin F.-Y. Lu € C.H. Ou. 1994. Trees of Taiwan Ge ol poen. National Chung-Shing University, "EY (In Chinese). Lu, C.-H 1982. Studies on the i el. d da and iential phenotypic unisexuality in pical Penta- gonia yap ime (Rubiaceae). Oecologi 68: 218-223. ai, T. 1940. Notulae Em plantas M Micah (XIV). ^ l y ld be z Sun. 2007. Phyl ylogeny and A hence (Lauraceae) disjunct between eastern Asia and eastern North America. Pl. Syst. Evol. 267: 19 L —203. Rehder, A. 1920. The Ameri can q a ies of Sassafras. J. Arnold PP k: 242: NT Renner, S. S. 2001. How common is heterodichogamy? Trends Ecol. Evol. 15: 595—597. Rohwer, J. G. 1993. i in K. Kubitzki, J. G. Rohwer & V. Bittrich ied he Families and Genera of Vascular Plants, Vol. Flowering Plants. Dicotyledons—Magnoliid, Hamamelid, and Caryophyllid Families. Fig gE aha Berlin. Sasaki, S. 1930. A Catalogue of the Government Herbari Department of Forestry, Government Research eiit ail e A. B. 1927. The n: behavior of avocados. Mem. New York Bot. Gar. Te E Utteridge, T. M. & R. M. K. I 2001. Sexual dimorphism di n BE. dide oecy i sa perlarius and M. japonica era ac Biotropica 33: 368-374. van der Werff, H 7. Lauraceae. Pp. 26-36 in ~~ - North Aaea md Committee (editor), Flora North America North of Mexico, Vol. 3. Oxford Beset Press, = York. l. An an — aw to the genera of Lauraceae in the flora Malesiana region. a 46: 125-140. & H. Richter 1996. Toward an pa classification dl Lauraceae. Ann. S Bot. Gard. 409-41 m Wang, P. J., C. Y. Hu & M. H. Chen. 1991. Taiwan sassafras [Sassafras n (Hay.) Rehd.] > E mY Ie S. Bajaj (editor), Biotech Ey ulture and Forestry, Vol. 16, ge TI. Springer Verlag erlin Weberling, F - 1988. Inflorescence structure in primilive angios ET Taxon 37: ed — ———. 1989. Morphology owers and Inflorescences. Conable | University ed oe ridge. Wen, J. 1999. Evolution of eastern Asian and eastern North American disjunct pattern in flowering plants. Annual Rev. Ecol. Syst. 30: 421-455, Wolfe, J. A. 1975. Some nspects of P aue of the ixi jr cei during the late Cre us and Tert Ann. Missouri Bot. = 62: 2 264 279. Yang, 1 d. Chung & Z.-Z. Chen Multiple dix — A and ds establishment i in shoot tip and nodal culture of Taiwan Sassafras (Sassafras randaiense (Hay.) Rehd.) Taiwan J. Forest. Sci. 15 31-39 ang, Y.-P., H.-Y. Liu & S.-Y. Lu. 1997. Manual of Taiwan x Plants, Vol 2. poen of Agriculture, The Executive Yuan, Taipei (In Chinese). Ying, S.-S. 1985. A revision of the family Lauraceae in Taiwan. Mem Agric. Natl. Taiwan Univ. 25: 83-117 (In Chinese, sib English summary). NT a ee TER en aN Oe TEMS VALE ESTUDIOS EN EL GENERO PASPALUM (POACEAE, PANICOIDEAE, PANICEAE): PASPALUM DENTICULATUM Y ESPECIES AFINES! Silvia S. Denham,? Osvaldo Morrone,” y Fernando O. Zuloaga? RESUMEN Se realiza un estudio sistemático de las especies afines a Paspalum denticulatum Trin., V la totalidad de las especies que han sido usualmente tratadas en el grupo informal Livida de Paspalum L. El análisis efectuado muestra que Livida es un grupo € = no — caracteres que permitan delimitar estudiadas nsideran como no agrupa por lo que las especies aq rtwegianum E. Fourn., P. trinii Swallen son tratados aqui bajo la sinonimia de P. las especies no ilustradas anteriormente, microfotografías (MEB) de los antecios y una clave Sw distribución, láminas de taxonómica para diferenciar las especies aceptadas. ABSTRACT Species Lr to Paspalum denticulatum Trin. i up Li palum of Pas L. The analysis ua Liv o de los restantes grupos 2 género Pani padas dentro del subgénero Paspa lum. Se desc a trichophyllum Henrard. Se presentan mapas de tudied n including taxa traditionally placed in the an artificial group, without characters that inform delimit it from remaining groups dea Paspalum; for this reason, its sine es are treated as un — uped within subgenus aspalu Henrard. Distribution maps, plat included, as well as a taxonomic a to diffensiniute the acc words: Livida, Paniceae, Paspalum, Poaceae. m p w Swallen and P. trinii Swallen onymii Hack., P. ir are here treated under the synonym s of species not previously illustrated, and SEM microphotographs of the upper anthecia are epted species El género Paspalum L. comprende cerca de 330 especies distribuidas en regiones tropicales y sub- le ap a templadas principalmente del Nuevo Mundo, con unas pocas especies que habitan en el Viejo Mundo (Clayton & Renvoize, 1986; Watson & Dallwitz, 1992; Zuloaga & Morrone, 2005). Son a menudo edem en misses NEA, como e eer nos, sabanas y p ; en ambientes ertum o boscosos y en dunas idem y hábitats halófitos o anegados. Diversas especies se comportan como ruderales o malezas, hallándose en bordes de caminos, vías férreas y suelos modificados. Se han propuesto um as e la nericas para el = morfologia de las inflorescencias y de las espiguillas (Chase, 1927, 1929, ined.; Clayton & Renvoize, 1986; Zuloaga & Morrone, 2005). Las clasificaciones infra- genéricas mas destacables y que han sido utilizadas como referencia para estudios sistematicos posteriores son Chase (1929, ined.). En ellos la autora reconoce dos subgéneros en Paspalum: Ceresia (Pers.) Rehb. y Paspalum; dentro del subgénero Paspalum reune a las especies por su afinidad morfológica en s informales. Denham (2005) establece el subgénero Harpostachys (Trin.) S. Denham, donde incluye a las especies del grupo informal Decumbentes de Paspalum y las del género Thrasya Kunth. Zuloaga et al. (2004) aceptan cuatro subgéneros en Paspalum: Anachyris ! Este estudio fue financiado por la Agencia Nacional de 13374, 32640 y colecciones de V pm Dudás * Instituto de Botánica Darwinion, Labardén MEN sdenham@darwin.edu.ar. 008092 doi: 10.3417/2 e campo focis realizadas con un su sidio de la Cientifi Téenica (ANPCyT; PIC 739, T 117 y por el Consejo Nacional de En net Científicas y Técnicas (CONICET. “PIP 5453). Las idio National G por la realización de las biie de este trabajo. 200, CC 22 (B1642HYD), San Isidro, Buenos Aires, Argentina. Autor para la eographic Society ($47792-05). Agradecemos al Sr. ANN. Missouni Bor. Ganp. 97: 11-33. PubLisHeED ON 31 March 2010. Annals of the Missouri Botanical Garden Tabla 1. Clasificaciones subgenéricas de Paspalum y de las especies del grupo informal Livida. Chase (1929) para Chase (ined.) para Zuloaga y Morrone (2005) América del Norte América del Sur para América del Sur austral Subgen. Ceresia Subgen. Ceresia Subgen. Ceresia Subgen. Paspalum Subgen. Paspalum Grupo Malacophylla Grupo Malacophylla Subgen. Anachyris Grupo Decumbentes Grupo Decumbentes Subgen. Harpostachys (grupo Decumbentes + Thrasya) Subgen. Paspalum Grupo Livida Grupo Livida (Denticulata) Grupo Livida P. num P. alcalinum P. alcalinum P. arsenei P. arsenei P. crinitum P. crinitum P. hartwegianum hartwegianum P. lividum P. lividum = P. denticulatum P. mutabile P. mutabile P. pubiflorum P. pubiflorum P. pubiflorum var. glabrum P. pubiflorum var. glabrum P. tinctum P. tinctum P. denticulatum P. denticulatum P. hieronymii = P. denticulatum P. proliferum = P. denticulatum P. remotum P. trichophyllum Grupo Linearia P. trichophyllum P. jesuiticum P. telmatum P. planum P. planum + 9 especies más (Nees) Chase, con seis especies; Ceresia, con 2] especies; Harpostachys, con 39 especies y Paspalum, que incluye las restantes especies del género. Zuloaga y Morrone (2005) en su tratamiento de las especies de Paspalum para América del Sur austral reconocen 28 grupos informales en el subgénero Paspalum. En este estudio se sigue la clasificación infragenérica aceptada por Zuloaga et al. (2004) y Zuloaga y Morrone (2005; Tabla 1). Entre los grupos informales del subgénero Paspa- lum, Chase (1929) establece el grupo Livida, donde E. Foum., P. pubiflorum var. glabrum Vasey y P. tinctum Chase, y también indica que este probable- mente no sea un grupo natural. Posteriormente, Chase (ined.), en un tratamiento inédito del género para América del Sur, considera en Livida a P. alcalinum, , P. crinitum. P. denticulatum Trin, P. hartwegianum, P. hieronymii Hack., P. lividum, P. mutabile, P. proliferum Arechav., P. pubiflorum, P. pubiflorum var. glabrum, P. remotum J. Rémy, P. tinctum y P. trichophyllum Henrard; caracteriza al grupo por incluir plantas perennes, mayormente glabras, con cañas comprimidas pauci- a multinodes, láminas planas o plegadas en la base, varios racimos de eje grueso o relativamente delgado, raquis de 0.5— 2 mm de ancho, espiguillas en pares de 1.1-3.4 mm de largo y fruto pálido, papiloso a liso. Zuloaga y Morrone (2005) reconocen, también informalmente, al grupo Livida por presentar plantas perennes, con cañas comprimidas, erectas a decum- bentes, de varios nudos, inflorescencias con pocos a numerosos racimos, espiguillas en pares, lisas a escabrosas, y por el antecio superior pajizo y papiloso; consid L ¿Lal Xa les V rr E z siete en América del Sur austral: Paspalum alcalinum, Chase (ined.) trata a Paspalum planum bajo el grupo informal Linearia del subgénero Paspalum (a pesar de no incluirlo en la clave, lo describe entre las especies de Linearia). Reconoce a este grupo por presentar plantas foliosas en la base y las vainas dion unt eiiis s ti Volume 97, Number 1 2010 Denham et al. 13 Estudios en el Género Paspalum superiores elongadas y sin lámina, inflorescencias con 2—3 racimos conjugados, y espiguillas principalmente solitarias. Zuloaga y Morrone (2005) tratan a P. planum en el grupo Livida y las especies previamente tratadas en Linearia por Chase (ined.) bajo los grupos informales Notata i El presente trabajo busca, como parte de una revisión del género Paspalum en ejecución, establecer si ae caracteres para definir taxonómicamente al po Livida y analizar, desde un punto de vista sistemático, las especies que tradicionalmente han sido incluidas en el mismo. MATERIALES Y MÉTODOS Se espec los siguientes aaas i B. "BAA. BM, "COL. ina F, FCQ, C, IBGE, JUA, K, LIL, LPB, MA, MBM, MEXU, MO, NY, P, R, SI, US, VEN, W (Holmgren et al., 1990). Se siguieron los procedimientos , clásicos para estudios de Aires, Argentina, siguiendo el procedimiento descrito por Soderstrom y Zuloaga a TRATAMIENTO TAXONOMICO El análisis del grupo Livida (Chase, 1929; Zuloaga & Morrone, 2005) permitió comprobar que los carac- teres. utilizados por diferentes autores para definirlo informalmente, no permiten asignar al grupo una categoría taxonómica definida. En efecto, el hecho de ser las especies plantas perennes, con cafias comprimi- das, inflorescencias con pocos a numerosos racimos espiguillas en pares con antecio superior papiloso no representan caracteres ünicos del grupo; estos caracteres. combinados están presentes en diversas especies de Paspalum, por ejemplo de los subgéneros Anachyris, Paspalum y Harpostachys. Además, estudios filogenéticos basados e en GbE parecia = rone et al.. en prep.) fil dif [is ntes clados no relacionados entre sí. En consecuencia, en el presente tratamiento se delimitan taxonómicamente las especies previamente incluidas en el grupo Livida, sin agrupar a las mismas en una categoría definida, y considerándolas dentro del breuis Paspalum CLAVE PARA DIFERENCIAR LAS ESPECIES DE PASPALUM DENTICULATUM Y ESPECIES ÁFFINES La Dia r ea aa 2 lb. F I ig sil gl R 1 "M à mas 2a. i — iid hasta de 50(—65) de alto. as basales nte — nius ans sedosos P. mutabile 2b. Espiguillas elipsoides o anchamente endis a qe se no orbiculares, plantas (30-)40-150 cm de alto, vainas basales glabras o papiloso-pilosas, pelos no in 3a. Espiguillas elipsoides, dos veces más largas q anchas, con pelos u rice disribuidos sobre la gluma superior y la lema inferi L P alos 3b. Espiguillas anchamente elipsoides a Ei hasta 1.5 veces más largas que anchas, con pelos más abundantes hacia los márgenes o uniforme- awaq distribuidos —— e 4 erguidas d espiguillas apiculadas, no tárgidas . A A Ode Visa 4. P. kariwa — 4b. Plantas decumbentes, arraigadas y s sres en los nudos inferiores a estoloníferas, con cañas ramificadas; espiguillas no apiculadas, túrgidas sse 5 NO: obi ense x Pea epi qa Antecio superior pálido a la madurez; inilmenchh- cias axilares presentes. Bolivia y — de la Argentina 9. P. remotum 6a. Espiguillas y raquis marcadamente esca s. en ambas — y en Men don 6b. idis glabras o ua n no abroso en ambas superficies o sólo los E 1 márgenes ía. Innovaciones intravaginales ................. 8 Tb. Innovaciones extravaginales ................. 8a. Espiguillas de 34,5 X 1.8-2.2 mm, elipsoides HEAR A 7. P. planum Bb. Espiguillas de 2.5-2.8 X 1.2-1.5 mm, anchamente élipsoldes 6G ine 6G be ee ape sis 5. P. jesuiticum 9a. Plantas de bases Mabeladas ........ 10. P. telmatum 9b. Plantas de bases no flabeladas 10a. — elipsoides, de 1.2-1 m de ancho, pedicelos oscuros largos E = 1.2 mm), . P. crinitum 10b. Espiguillas anchamente elipsoides, de 1.2-1.8 mm de ancho, sobre pedicelos cortos (0. 2 ro P. dent i asa 1. Paspalum alcalinum Mez, Repert. Spec. Nov. Regni Veg. 15: 75. 1917, nom. cons. prop. 1803, Taxon 57(1): 304. 2008. TIPO: México. San Luis Potosí: Hac. Angostura, C. G. Pringle 3764 (holotipo, B no visto; isotipos, F 105515! foto SI!, M! MA!, MEXU 3419!, MO 2354872!, foto SI!, P!, US-2941970!, W!). Figuras 1, 2, 3B, ¢ — — ME Bull. Torrey a m 13: . VU. Texas: s. loc LLE Buckley s.n. ete US 2854140). Plantas perennes, cespitosas, con rizomas cortos, hojosos, cubiertos de catáfilos glabros; cafias erectas o decumbentes a estoloníferas, con estolones viajeros, arraigadas y ramificadas en los nudos, porción erecta Missouri Botanical Garden Annals of the 14 pálea superior. lado de la lema inferior. —F. la. —C. Porción del raquis de los racimos, r, vista ventral mostrando la ntana 2909-3, SL igu z de la | —E. Espiguilla, vista del ntecio superio Eskuche & Fo z. —A. Habito. —B. Detalle D. Espiguilla, vista del lado de la gluma superior. mostrando la lema superior. —G. A as y filamentos estaminales. A-H de Paspalum alcalinum Mez. sal superior. vista —H. Pálea superior, lodícul Figura 1. pedicelos. — Antecio Denham et al. 15 Volume 97, Number 1 2010 Estudios en el Género Paspalum W P crinitum * P alcalinum e P jesuiticum O P mutabile 4 P. remotum H P hartwegianum s... — t EN het e Figura 2. Distribución de Paspalum crinitum — in Hitch., P. alcalinum Mez, P. jesuiticum Parodi, P. mutabile Chase, Fou P. remotum J. Rémy y P. hartwegianum E. em 2 I 0.3—0.4 cm de diámetro; cm, comprimidos, macizos, de 45-120 entrenudos de esponjosos, ek ses pi ¡ Gap a pilosos. Vainas usualmente mayores entrenudos, superpuestas, flojas, de dorso ds glabras a pilosas o papiloso-pilosas junto a la porción distal, los márgenes membranáceos, glabros; cuello glabro o piloso; lígulas de 3-6 mm, membranáceas, enteras 0 laciniadas; pseudolígula presente, con pelos hasta de 6 mm de largo; láminas lineares, de 10-35 X 0.5 em, ascendentes, planas a convolutas o enrolladas, angostada y ápice setáceo, con ambas caras "m a esparcidamente pilosas, papiloso-pilosas junto a la unión con la vaina, los márgenes escabrosos, glabros, las superiores de menor desarrollo. Pediíncu- los subexertos a exertos, hasta de 50 cm, cilíndricos, estriados; inflorescencias terminales, de 7-20 X l- 4 em; eje principal de 3-16 cm, triquetro, glabro, escabroso; pulvínulos pilosos, con largos pelos blan- =, hasta de 5 mm; racimos 4-12, alternos, ascendentes, adpresos o poco divergentes del eje pri inea distantes, x na en una espiguilla desarrollada; raquis de los racimos de 2-8 cm, los apicales más cortos, 1-1.6 mm de ancho, reducido hacia la porción distal, aplanado, cortamente alado liso a hispídulo, verdoso, con los márgenes escabrosos, glabros o con largos pelos papilosos aislados; pedice- los en pares, desiguales, hasta de 1.2 mm, triquetros, escabrosos; espiguillas en pares, imbricadas, distri- buidas en 4 series. Espiguillas elipsoides, de 2 1.2-1.4 mm, agudas, pubescentes, pajizas o con tintes purpúreos; gluma superior y lema inferior subiguales, membranáceas, de dorso finamente papiloso, homo- géneamente pilosas, con pelos cortos hasta de 0.5 mm; Annals of the Missouri Botanical Garden Figura 3. lema superior (de rn 4799. SI.B junto al ápice de la pálea. —C. Cuerpos ide sílice en la lema s lado de la = (de ean 3805. SD. (de Arséne 269 3, US . Pa: ABE spalum eS SI). Barra: = um; D y E = 100 um; € — = E gluma inferior ausente; gluma superior tan larga como a espiguilla, 5-nervia, con un nervio central, los restantes submarginales; lema inferior tan larga como la espiguilla, pilosidad como en la gluma o glabres- cente, 3-nervia, nervios laterales submarginales, levemente carinados; pálea inferior y Pe PS ausentes, Antecio superior elipsoide, de 2.2— 1.2 mm, crustáceo, fuertemente Neil pajizo, glabro, 0.2-0.6 mm más corto que la gluma superior y lema inferior; lema con papilas simples regularmente distribuidas en toda su superficie y micropelos bi- y y tricelulares junto al ápice, con abundantes e uerpos de sílice, los márgenes enrollados sobre la pálea, 5- con papilas en toda su superficie y micropelos junto a los márgenes apicales; s nervia: pálea de textura similar que la lema. lodículas 2, ca. 0.3 mm: re 3, anteras de 1.6 mm. Cariopsis elipsoide, de 1.7 1.1 mm; hilo elíptico; embrión 1/3 del largo de : cariopsis. Distribución geográfica y hábitat. Paspalum alca- linum se distribuye de manera disyunta en Estados Unidos de América (Texas) en México, ha sido ocasionalmente coleccionada : en Colombia, y luego está presente en la Argentina y Paraguay. Se halla en C. Papam alcala mea —E. Paspalum pubiflora rum d ex E. J A. Paspalum planum Hack., papilas simples en la superficie de la - Micropelos bi- y tricelulares ápice del antecio del de la pálea e Morrone 5322. SD. — —D. Tow denticulatum Trin., áp ourn., ápice del antecio del lado 2 Rémy, mic e bi- y tricelulares en la lema superior (de Zuloaga 5826, 1 suelos húmedos, bordes de selvas, pastizales y márgenes de caminos o vegetación secundaria, desde el nivel del mar hasta los 200 m.s.m 2n = 40 (Dandin & Chen- Número cromosómico. naveeraiah, 1977, 1983) Observaciones. Paspalum buckleyanum ha sido comünmente tratado bajo la sinonimia de P. hartwe- gianum (Chase, 1929; Hitchcock, 1951; McVaugh, 1983; Zuloaga et al., 1994), pero el análisis de los materiales tipo puso en evidencia que, por la morfología de sus espiguillas, es conespecífico con P. alcalinum, especie que también crece en México. Zuloaga y Morrone (2003) citan a P. buckleyanum como sinónimo de P. alcalinum. Luego, Paspalum buckleyanum tiene prioridad sobre P. alcalinum. Debido a que el nombre P. buckleyanum ha sido escasamente usado y mantener la estabilidad nomenclatural se ha puesto la conservación del nombre P. alcalinum sobre P. buckleyanum (Denham, 2008 Pohl y Davidse (1994, 2001) y — et al. (1999) tratan a Paspalum alcalinum como sinónimo de P. hartwegianum. Sin embargo, ambas especies se diferencian porque en P. hartwegianum las espigui- para p )ro- di Volume 97, Number 1 2010 Denham et al. 17 Estudios en el Género Paspalum llas son anchamente elipsoides a obovoides y la pilosidad en la gluma superior y lema inferior no es homogénea, siendo más densa hacia los márgenes, con pelos más largos que en el resto de la superficie; también los nervios submarginales de la lema superior son más delicados que en P. Chase (1929, ined.) distingue a — alcali- num de P. hartwegianum, entre otros caracteres, por las cafias simples y erectas en P. alcalinum y cañas ramificadas y decumbentes en P. hartwegianum. No obstante, este carácter es variable en P. alcalinum, especie en la que se =" ejemplares que tienen rgos estolones (Quart . Rojas 5597) o ejemplares con cañas cil (Garcia Barriga 10009, Morrone et al. 5356) y otros con cañas todas Paspalum alcalinum se aparta de P. denticulatum por tener esta última especie espiguillas anchamente o con escasos dientes sobre alcalinum se distingue por sus espiguillas homogé- neamente pilosas, con pelos cortos hasta de 0.5 mm. ARGENTINA. (BAA). n. Dun Luis del Palmar, 20 km SE de San * del Palmar. (uri D: CTES, SI); Saladas, Ruta Nac. 12, 60 km Bella Vista camino a Empedrado, eee etal, MAR Entre Ríos: La Paz. 5 km de La Paz camino a Paraná, Ruta Nac. 12, Morrone et al. 5356 (SI). F - LE de s Ca sas, Insfrán s.n. (SI). Jujuy: d a a Tiraxi. Zuloaga 4557 (SI). Salta: Dpto. Anta, Pozo hes 10 Km SSE de J. V. González, Saravia Toledo 1235 (8D). Santa Fe: Dpto. s 2 Amores, Bissio & Batista 1100 (SD). Santiago del E 5 km al S de Pampa de los Guanacos, Eskuche & Pusak 2909-3 (SI). COLOMBIA. Cundinamarca: Mpio. La Esperanza, García Berge 10009 (U S. MÉ XICO. México: AU 55, Km 28, 4 2 Atlacamuco, Morrone et al. : (SD. licen nae Villarrica, a . 110. de wap camino a Zamora, salida a Villarrica, Morrone et al. 36.39 (SI). Morelos: Carretera de cuota Tepoztlán-Oaxtepec, Zuloaga ee a Swallen 2964 (MEXU). PARAGUAY. Alto Paraguay: Pun o Casado, Cerro Galván, Rojas 2778 (BAA. G. US); Rojas . 5597 = 5863 (BAA. K. MA. P. US). aguna Porá, Vanni et al. 2601 HS o. ayes: Estero Patiño, Km 164 de la v1 Transchaco, Schinini & Palacios 25921 (CTES, FCQ, G. MO); Chaco Paraguayo, Ruta Transchaco Km 295, esta 1049 (CTES) 2. Paspalum crinitum Chase in Hitchc.. Contr. U.S. Natl. Herb. 17: 237. 1913. TIPO: México. San Luis Potosí: Hac MET š jul. 1891, C. G. Pringle 3755 (holotipo, US 824361*; isotipos, B no visto, F 105506!, foto ST, n no visto, MEXU!, MO 2977056!, MO 51146531, P!, W no visto). Figuras 2, 4. Plantas perennes, cespitosas, cafias erectas, de 50— 100 cm, simples; entrenudos de 5-25 cm, comprimi- dos, estriados, huecos, glabros, pajizos o con tíntes violáceos; nudos 2 a 3, glabros. Vainas de 3-20 cm, las inferiores superpuestas, numerosas, esparcida a dens- amente papiloso-pilosas, las superiores más cortas que los entrenudos, glabras; cuello glabro, castaño; lígulas —5 mm, membranáceas, decurrentes con la vaina; pseudolígula con escasos pelos de 4—5 mm; láminas lineares, de (4-)10-20 X 0.2-0.8 cm, numerosas en la base, planas, esparcidamente papiloso-pilosas en ambas vá y los márgenes, de base redondeada a angostada y ápice agudo, no setáceo, los márgenes escabrosos, don. Pedánculos largamente exertos, hasta de 30 cm, glabros; inflorescencias largamente exertas, de 7-17 X 3-7 cm, terminales; eje principal de 5-15 cm, glabro, violáceo; pulvínulos glabros o pilosos; racimos 4 a — alternos, divergentes del eje principal, espiguilla desarrollada; is le E oM de 1.2- 7 X 0.6-1 mm, ligeramente aplanado, violáceo, los en una márgenes escabrosos y con pelos papilosos aislados o sin los mismos; pedicelos en pares, filiformes, de más de 1.2 mm, oscuros, violáceos, escabriúsculos; espi- guillas imbricadas, dispuestas en 4 series irregulares Espiguillas elipsoides, de 2.5-2.8 X 1.2-1.3 mm, plano-convexas, obtusas a subagudas, glabras, menos frecuentemente con espiguillas corta y esparcidamente pilosas en los márgenes de la gluma — +" o con tíntes violáceos; gluma inferior au uma superior tan larga como la espiguilla, hialina, delic cada, Ma 5)-nervia, con un nervio medio, los restantes submarginales; lema inferior glumiforme, tan larga como la espiguilla, 3-nervia; pálea inferior y flor inferior ausentes. Antecio superior elipsoide, de 2.4-2.7 X ca. 1.2 mm, crustáceo, pajizo, papiloso, con papilas simples regularmente « istribuidas, y pelos bicelulares hacia el ápice de la pálea; estambres 3, anteras de .9 mm. Cariopsis no vista. Distribución geográfica y hábitat. Esta especie es endémica de México, crece en los estados de Durango, Jalisco, San Luis Beetle et al., 1999) eb en suelos húmedos. alc ni los 2000 m.s.m. Número cromosómico. 2n = 40 (Gould, 1966). Observaciones. Se caracteriza por sus láminas mayormente basales, espiguillas elipsoides sobre largos pedicelos oscuros, glabras, ocasionalmente con pelos en los márgenes de la gluma superior; la gluma superior y la lema inferior son delicadas y pajizas o con tintes violáceos. Paspalum crinitum es morfológicamente afín a P. denticulatum. distingién dose esta última por tener las láminas dispersas en las 18 Annals of the Missouri Botanical Garden ra 4 Paspalum crinitum Chase in Hitehe. — racimos, pedicelos. —D. Espjoy; A. Hábito. — B. Detalle de la lí > diz š : š A E : gula. —C. Porc >] raquis de los —F. Antecio superior, vista dorsal — Ma la gluma superior. —E. Espiguilla, vista del ps n raquis de | superior. —H. Pálea superior. Bah. 3 ma superior. —G. Antecio s ior, vi "m Pringle 3755, isotipo P : Pálea superior, lodículas y estambres. A-B ie a M M. Mu no. Antonio s.n., MEXU-213533; C-1 de Ea ana ek aah Leach np mes «ad ue Sd ad air CONTIENE NIE NIENTE O NIU I SUS NOT O O E O NIRE EUN re E e A RI Me EUR TE LC RR A NM DERE PPS Pr" í E i : Volume 97, Number 1 2010 Denham et al. 19 Estudios en el Género Paspalum cañas (vs. más numerosas en la base en P. crinitum) y las espiguillas denticuladas (vs. espiguillas glabras o menos frecuentemente corta y esparcidamente pilosas en los márgenes de la gluma superior en P. crinitum), hallándose sobre pedicelos triquetros, cortos de 0. 1.2 mm y pajizos (vs. pedicelos filiformes, de más de 2 mm, oscuros, violáceos, escabriüsculos). Material examinado. MÉXICO. Coahuila: Chojo Grande, 27 mi. SE of Saltillo, Palmer 338 (MEXU). Puebla: Rancho Posadas, Arséne 1604 (M d Rancho de las Posadas, Hno. Antonio s.n. (MEXU 213533). 3. Paspalum denticulatum on Gram. Pani, [Trinius]: 111. 1826. TIPO: “Amer. equinoxi s.d., J. Lindley s.n. — PIN 0441 e isotipo, US ! [fragm. ex LE]. Figuras 3D, 7 Paspalum — Trin. ex Schltdl., Linnaea 26: 383. 1854. TIPO: México. Hac. La A julio, C. J. W. Schiede s.n. nici designado por Chase, 1929: 57, LE- TRIN 0441.03!; dcus! B no visto, BM!, foto SI!, G!, P!, US 928992! [fragm. ex LEJ). PES poiria D zx 2 m Montevi- feb., J. 894. TIPO: allas 202 a MVM. no vidio isotipo, CTES!). Paspalum hieronymii Hack., Oesterr. Bot. Z. 51: I 1901. TIPO. Argentina. To mán: s. loc., 7 ene. 3, P. €. Lorentz H. E. W. Hieronymus 1084 ie W!; sotipos, B!, G!, K!, US 2855296! [fragm. ex WJ). Paspalum jujuyense Zuloaga, Bol. Soc. Argent. Bot. 16: 65. 974. TI rgen ntina. Jujuy: Dpto. Dr. Manuel nm rano: Sierra de fapla, Mina 9 de Octubre. 25 feb. 1971, A. L. p "ra 21626 (holotipo, LP!). Plantas perennes, cespitosas, cortamente rizomatosas; cafias erectas, decumbentes a estoloníferas, simples o ramificadas en los nudos basales y medios, arraigadas, porción erecta de 10-180 cm, 0.7-5 mm diám. con 3 a 15 nudos; — de 2—24 cm, estriados, comprimi- dos, macizos o cos, glabros; nudos — castaño claros, Prim Vainas usualmente más largas que los entrenudos, comprimidas, aquilladas, super- puestas, flojas, glabras o menos frecuentemente pilosas con los márgenes membranáceos, glabros, raro p Dos cuello glabro a cortamente iE lígulas de 0.6— 4 mm, membranáceas; pseudolígula ausente o presente; láminas lineares, de (1.8—)7-28(-35) X 0.1-0.8 cm, ascendentes, planas, glabras a esparcidamente pilosas o hispídulas en ambas caras, de base atenuada a redondeada y ápice agudo, los már esc planos o involutos. Pedúnc P exertos, hast de 2010 cm, ilíndricos glabros; un] Je 3- 22 X 1-7 em; eje principal aplanado, liso a escabriúsculo; pulvínulos con un mechón blanquecinos; racimos 3 a 20(a 27), ascendentes, divergentes del eje principal, alternos, terminando en una espiguilla desarrollada; raquis de los racimos de 1.5-5.9 cm X 0.7-2 mm, los apicales menores, aplanados, verdes a purpúreos, hispídulos, glabros o con - papilosos aislados, hasta de 5 mm; pedicelos en s, desiguales, de 0.5-1.2 mm, triquetros, beds espiguillas imbricadas, en 4 series, en ocasiones la inferior abortada. Espiguillas anchamente elipsoides, de 1928 X 1.2-18 mm, agudas a cortamente aep glabras, verde pálidas o con es purpüreos; gluma superior y lema inferior subiguales, wata 'kup'iaaqq con el dorso finamente papiloso; gluma inferior ausente; gluma superior tan larga como la espiguilla, 3-nervia, con un nervio central, los restantes submarginales, finamente denticulada bre los nervios junto al ápice a lisa; lema inferior glumiforme, tan larga como la espiguilla, 3-nervia; pálea inferior y flor inferior ausentes. Antecio superior dd elipsoide, de 1.8-2.2 X 1-1.5 mm, crus- táceo, fuertemente papiloso, pajizo, glabro; lema con papilas simples regularmente distribuidas en toda su superficie, los márgenes enrollados sobre la pálea, 5- nervia; pálea de textura similar que la lema, con papilas en toda su superficie y micropelos bicelulares hacia el ápice; lodículas 2, ca. 0.4 mm; estambres 3, anteras de mm. Cariopsis elipsoide, de 1.4—1.8 X ca. 0.8 mm; hilo elíptico; embrión 1/3 del largo de la cariopsis. Iconografía. Burkart, 1969: 397 (bajo Paspalum lividum) Distribución geográfica y hábitat. Paspalum denti- culatum se distribuye desde el sur de Estados Unidos de América hasta la Argentina y Uruguay. Crece en terrenos bajos y húmedos, es frecuente en bordes de caminos, desde el nivel del mar hasta los 3000 m.s.m. Números cromosómicos. = 20, 2n = 40 (Saura, 1943; Gould, 1958; Reeder, 1967; Quin, 1977; Quarin et al., 1982; Quarin & Burson, 1991; Norrmann et al., bn Hunziker et al., 1998; Morrone et al., 2006). Observaciones. | Chase (ined.) considera a Paspalum lividum, P. Mou P. — y E an li para aida utiliza cities del tamaño y textura de las espiguillas y ancho y color del raquis; además destaca el rango de distribución de cada especie, restringiendo a P. denticulatum al norte de Brasil, a P. hieronymii a Uruguay y norte de Argentina, a P. lividum desde el sur de Estados Unidos de América hasta la Argentina y a P. proliferum del sur de Brasil a Uruguay y Argentina Al ser considerada por Chase como la especie de más amplia distribución, Paspalum lividum es tratada en distintas Floras regionales (Me Vaugh, 1983; Pohl & Davidse, 1994; Renvoize, 1998; Allen & Hall, 2003) aunque sin discutir las diferencias con las restantes EET I UE EE ENTRE EET IN mL ST — X x * i < T z Y ” š : Annals of the Missouri Botanical Garden P TrV PI mayor que el establecido por Chase (ined.). Por su parte, P. proliferum ha sido citada para Uruguay por Rosengurtt et al. (1970) y Parodi (1937), quien duda de su identidad por su similitud con P. lividum. La especie has f, Ll ] 1 - juju I I p ia de Jujuy en Argentina (Zuloaga, 1974) y citada posteriormente como válida por Zuloaga et al. (1994). Zuloaga y Morrone (2005) consideran a estos cuatro taxones bajo la sinonimia de P. denticulatum sobre la base de la variación morfológica observada. El análisis del material tipo de los taxones antes mencionados, junto ecu sk. : l po y al 1 terial de herbario, permite concluir que no existen caracter válidos para la separación de más de una especie, por lo que se concuerda con el criterio sustentado por Zuloaga y Morrone (2005). Material. representativo examinado. ARGENTINA. Bue- nos Aires: Ramallo, isla Las Hermanas, Burkart 12809 (SD. Ai ermo, Barreto 54 - Chaco: Resistenc a, A nta Cruz: Cordillera Province, Bañados del Izozog, Cachari, Navarro & Vargas 302 (LPB, MO). BRASIL. ará: Ilha Morena, Huber 2337 (G). Rio G : Ç r Sul: Uruguayana, Barreto 1587 (SD). COLOMBIA. Cundina- e Mpio. Mosquera, Zanjón-Las Cáted Saravia (C Y. JL). Nariño: Pasto, Espinosa 2759 (COL). CUBA. Habana: Habana, Regla, Ekman 1 0894 (GC). Pin orazán: de Tegucigalpa, Muñoz 2] (SI). MÉXICO. Chi Matuda 1604 (MEX U). Hidalgo O de Tecoza — E E gs š. š 5 Tehuantepec, King 393 (MEXU). San Luis Potosí: 13 km NO de Acuña, Dávila et al. 75 (MEXU). Sinaloa: Culiacán etc» Palmer 1552 (SD. Tasanslipes: Has Sens n racia, C 21 (MO). V "cru: ca. ]O mi. SE of Cordoba, Reeder & Reeder 1991 (MEXU). PARAGUAY. Mis Paraguay: Bahia Negra, Chaco Paraguayo, Rojas 13814 i na Porá, à S. entral: Estero del Y á, Puerto Guyratí, Zardini & Tilleria 33920 Sp. * F. €. Casado Km 32, Rosengurtt B-5866 (K, P, US). Presidente Hayes: Rte. Concepción a Pozo Colorado, 15 km del Río Paraguay, Zuloaga & Morrone 7319 ( PERÚ. Cajamarca: Prov. San Miguel, El Limoncito, La Florida, Llatas Quiróz & Palacios 1817 (SI). La Libertad: 1 Trujillo, campos de Manciche, Ridoutt 207 (SI). Lima: San 2 Isidro, Asplund 10922 (G, US). URUGUAY. Canelones: x Santa Lucía, Osten 4601 (G). Colonia: Palmira, Río ` Uruguay, Herter s.n. (G). Montevideo: Atahual | :8 US). VENEZUELA. Distrito Federal: Puerto Escondido : Pittier 13453 (G, VEN). Falcón: Carretera Coro—Mirimire, : ca. del Río Hueque, Wingfield 6223 (MO, VEN). x 4. Paspalum hartwegianum E. Fourn., Mexic. Pl. 2: 12. 1886. TIPO: México. Guanajuato: ad fossas prope León, s.d., K. T. Hartweg 245 (lectotipo, designado por Chase, 1929: 58, Pt: duplicados, B no visto, LE!, US 928960! [fragm. ex Pl, W!). Figuras 2, 5 Paspalum tinctum Chase, Contr. U.S. Natl. Herb. 28(1): 62, fig. 30. 1929, syn. nov. TIPO: México. Guanajuato: Irapuato, 1900 m, 1 oct. 1910, A. S. Hitchcock 7404 (holotipo, US 929014, foto!). Plantas perennes, cespitosas, rizomas cortos; cañas erectas a decumbentes, en ocasiones arrai gadas sólo en los primeros nudos basales, de 50-150 cm, 0.2-0.5 cm diám., simples, menos frecuentemente ramificadas en la porción basal; entrenudos de 5-18(-30) cm, comprimidos, huecos o macizos, estriados, pajizos, abros; nudos comúnmente glabros, oscuros. Vainas de 1-25 em, las basales superpuestas, las superiores más cortas o más largas que los entrenudos, de dorso redondeado, glabras o esparcidamente papiloso-pilosas hacia los márgenes apicales; cuello glabro o piloso; lígulas membranáceas, de 1.5 í lanceoladas 13-25(-40) X 0.4-0.8 cm, las superiores ucidas, conduplicadas a planas, de base angostada y ápice setáceo, glabras o con ambas caras esparcida- mente pilosas hacia la base. Pedúnculos subexertos, hasta de 47 em, glabros; inflorescencias exertas, de 9- 6 X 2-6 em; eje principal glabro, estriado, acanalado, castaño a violáceo; pulvínulos generalmente pilosos, con pelos blanquecinos hasta de 7 mm; racimos 3 a 23, ascendentes, alternos o algunos racimos conjugados, erminando en una espiguilla desarrollada; raquis de los racimos de 4-7 cm X 1.2-1.7 mm, los apicales más Cortos, márgenes glabros o pilosos, lisos o escabrosos; pedicelos en pares, triquetros, 1-1.7 mm, escabriúscu- los; espiguillas distribuidas en 4 series, imbricadas, en ocasiones la superior abortada. Espiguillas anchamente elipsoides a obovoides, de (2.3-)2.6-3.1 x (1.4—)1.6- 1.9 mm, aplanadas, pubescentes, pajizas o con tintes ; gluma inferior ausente; gluma superior tan ga como la espiguilla, con el dorso corta- y Volume 97, Number 1 Denham et al. 21 2010 Estudios en el Género Paspalum KM "—0————9———e"U-(K7———————————Y—^———————————————U——" 5. Paspalum hartwegianum E. Fourn. —A. Habito. —RB. Detalle de la lígula. —C. Porción del raquis de los racimos, No — D. Espiguilla, vista del lado de la I superior. —E. Espiguilla, vista del lado de la lema inferior. —F. Antecio — vista dorsal mostrando la lema. —G. A o superior, vista ventral mostrando la pálea superior. —H. Cariopsis, vista scutelar. —I. Cariopsis, vista hilar. A-I de King < Soderstrom 4603, US. = 2 a esparcidamente piloso más densamente hacia los márgenes, J-nervia, los nervios laterales submargi- nales; lema inferior glumiforme, tan larga como la espiguilla, con pilosidad semejante a la gl perior a glabrescente, 3-nervia; pálea inferior y flor inferior ausentes i ; bicelulares hacia el ápice de la pálea y bordes de la lema; lodículas 2, de 0.47 mm, estambres 3, anteras 1.6-1.7 mm, violáceas. Cariopsis elipsoide, de 1.4—1.8 X ca. 1 mm, hilo elíptico, embrión mayor a 1/3 de la cariopsis. Distribución geográfica y hábitat. Especie endé- mica de México, habita en los estados de Sonora, Sinaloa, Jalisco, Michoacán, Guanajuato, Oaxaca, Morelos y México. Crece desde el nivel del mar hasta y caminos. América, pero estas citas corresponden al tipo de Paspalum buckleyanum, usualmente tratado sinónimo de P. hartwegianum, o a P. Allen & Hall, 2003); no se han observado ejemplares para Estados Unidos de América en este estudio. Números cromosómicos. = 30, 2n = 40, 60 (Gould. 1958: Davidse & Pohl, 1972; Pozzobon et al, 2000; Morrone et al., 2006). Esta especie se caracteriza por sus espiguillas pubescentes y anchamente elipsoides a Es morfológicamente afin a Paspalum alcalinum; las diferencias entre ambas se discuten bajo esta ültima especie. Chase (1929) utiliza caracteres del color de las espiguillas y del raquis y el tamaño de las espiguillas para separar a Paspalum tinctum de otras especies del grupo Livida. A su vez, Pohl y Davidse (1994) separan a P. tinctum y P. hartwegianum por el número de racimos (15 a 28 vs, 4 a 12 às espiguillas 1.8 mm en P. tinctum) y el color de raquis (verde oscuro o pürpura en P. tinctum) para se ar ambos taxones, pero la variabilidad observada en el total de los ejemplares incluye racimos y espiguillas pajizas a violáceas y espiguillas que varían entre 2.4— 3.1 mm de largo y 14-19 mm de ancho. En Consecuencia, no es posible s separar claramente 4 p. Por lo que se reduce a la Sinonimia esta última especie. Annals of the Missouri Botanical Garden Material examinado. MÉXICO. Jalisco: 5 mi. SW of | Santa Cruz de Las Flores, McVaugh 16294 (MEXU); Tala, Cervantes-Castro 202 (MEXU); Unión de Tula, Potrero la Tijera, Santana 476 (MEXU); Chapala, Holwey 3437 (US); near Km 58 rd. from Zapotlanejo, McVaugh 17251 (US); 1 km de San José de Los Andrade, desviación a Tototlán, la brecha Ayutla-Mazcota, Guzmán 41 | Juchitepec, León 9 (MEXU). Michoacán: Valley of Zamora, i (MEXU, US); Cerro Potrerillos, Merril, King & | Soderstrom 4603 (US). Morelos: Tepoztlán, Espino 14 | (MEXU); Cuernavaca, Hitchcock 91 1 (MO, US). Oaxaca: Hac. Aguilera, Conzatti 3600 (MEXU, US). Sinaloa: 19 km I N Mazatán along hwy. 15, Snow 66 i Guaymas, 1.7 mi. SE of Pitahaya, Felger 1257 (MEXU). t 5. Paspalum jesuiticum Parodi, Darwiniana 15: ` 104, fig. 9. 1969. TIPO: Brasil. Rio Grande do - Sul: Porto Alegre, 11 feb. 1953, A. Araujo 179 (holotipo, BAA!). Figura 2. Paspalum perspicinervium Renvoize, Kew Bull. 42: 922. 1987. TIPO: Brasil. Paraná: Curitiba, Barigui, s.d., Ferreira 182 (holotipo, MBM!; isotipos, K!, SI!). Plantas perennes, estoloníferas, rastreras, con innovaciones intravaginales en los nudos arraigados; cañas floríferas erguidas a geniculadas, de 20-60 cm, paucinodes; entrenudos 2 a 3, ligeramente comprimi- dos, estriados, macizos, glabros; nudos castaños, glabros. Vainas usualmente menores que los entrenu- dos, lateralmente comprimidas, aquilladas, las infer- lores papiloso-pilosas, las superiores glabras a esparcidamente papiloso-pilosas, los márgenes mem- branáceos, glabros; cuello glabro; ligulas de 2-3 mm, membranáceas, castañas, glabras; pseudolígula au- sente; láminas linear-lanceoladas, de 5-12 X 0.6- l cm, planas, glabras a esparcidamente papiloso- pilosas en ambas caras, base redondeada y ápice agudo, los márgenes finamente escabriúsculos. Ped- únculos exertos a parcialmente incluidos en las vainas foliares; inflorescencias exertas, de 5-8 X 2-4 em; eje ipal de 2-4 em, aplanado, glabro; pulvínulos pilosos; racimos 4 a 9, ascendentes, alternos, los plano, verdoso, glabro; pedicelos en pares, breves, hasta de 1 mm, glabros, finamente escabrosos; espiguillas dispuestas en 4 series, imbricadas, en mente elipsoides, de 25-28 x 1.2-1.5 mm, plano- convexas, de ápice agudo, glabras, verdosas: gluma inferior ausente; 1 espiguil A S ca alt lal cael on i O ER A E TE E: A AA O O Volume 97, Number 1 2010 Denham et al. 23 Estudios en SS Género Paspalum convexo, pajizo, f lema con papilas simples weer as regularmente en toda su superficie, pelos bicelulares s la porción apical, los márgenes enrollados sobre la pálea, 5-nervia; pálea de textura similar que la lema, con micropelos bicelu- lares junto al apice; lodículas 2, conduplicadas, ca. 3 mm; estambres 3, anteras de 1—1.4 mm, amarillo- anaranjadas. Cariopsis no vista. Iconografia. Parodi, 1969: 105. Distribución geográfica y hábitat. Habita en do Sul y en el nordeste de Argentina, en la provincia de Misiones. n — 30 (Morales Fernandes Número cromosómico. et al., 1974). Observaciones. Se caracteriza por el hábito ras- trero, las innovaciones intravaginales, las vainas basales más cortas que los entrenudos y comprimidas, aquilladas y pilosas. Zuloaga n Morrone (2005) ubican a esta especie en rmal Livida y la relacionan por su boh. con i alcalinum y P. denticula- tum, aunque claramente la distinguen de ambas por el porte marcadamente rastrero de P. jesuiticum. ARGENTINA. Misiones: Bon- 9 (BAA). BRASIL. n Mpio. Kummrow 1695 (MO); Mpio. Lou Rio da Divisa, Hatschbach 28524 (K, MBM, US). Rio own do S . Ex ental pe Centro Agronó- i aiba, Mis 250 5053 3 (SD. Catarina: Joinville, Hans 270 (R); Joinville, ex ra Francisca, Reitz & Klein 5708 (C). Material n t€ —-— Pilào Pr 6. Paspalum mutabile Chase, Contr. U.S. Natl. Herb. 28: 61, fig. 29. 1929. TIPO: México. San Luis Potosí: near Cárdenas, 20 July 1910, A. 5. Hitchcock 5773 cbe. US 9 928949!; isotipo, US 928947!). Figuras 2, 6 Plantas perennes, — cafias de 20—50(—65) ramificadas en los nudos 4-15 cm, comprimidos, estriados, huecos, glabros; nudos gla- basales, cm, erectas, simples inferiores, ais entrenudos de bros a pilosos. Vainas predominantemente superpuestas, más largas que los entrenudos, aquilla- das, comprimidas, densamente papiloso-pilosas, pelos sedosos, las superiores esparcidamente papiloso- pilosas a glabrescentes; cuello piloso; lígulas mem- branáceas de 2-4 mm; pseudolígula con abundantes pelos sedosos de 4-6 mm; láminas lineares a linear- lanceoladas, de 5-15 X 0.5-1 em, planas, ascen- dentes, papiloso-pilosas en ambas superficies, de base redondeada, los márgenes pilosos. Pedúnculos exertos hasta de 30 cm; inflorescencias terminales de 6-10 X cm; eje principal aplanado de 4-6 cm, glabro; pulvinulos pilosos, con pelos hasta de 5 mm; racimos 3 a 6, alternos, divergentes, espiguilla desarrollada; raquis de los racimos de 2— terminando en una 6 cm X 1-1.5 mm, aplanado, — Re pedicelos en pares, breves, hasta mm; espiguillas distribuidas en 2 a 4 series, eds la espiguilla inferior ocasionalmente abortada. Espi- guillas orbiculares, de 2-2.3 X 1.6-1.8 mm, plano- convexas, subagudas, pajizas o en ocasiones con tintes violáceos, cortamente pilosas, raro glabrescentes; gluma inferior ausente; gluma superior tan larga como la espiguilla o levemente más corta, pubescente, con pelitos delicados, ca. mm, inci más densamente hacia los márgenes, 3-nervia; lema inferior glumiforme, tan larga como la espiguilla, glabra o con unos pocos pelitos aislados, 3-nervia; pálea inferior y flor inferior ausentes. Ántecio superior anchamente elipsoide, tan largo como la espiguilla, crustáceo, papiloso, con papilas simples regularmente distribuidas sobre la pálea y lema, micropelos bi-, tri- y tetracelulares en toda la superficie o en el medio superior; lodículas 2, de 0.5 mm; estambres 3, anteras de 1 mm. Cariopsis no vista. Distribución geográfica y hábitat. Paspalum mu- tabile habita en México, en los estados de San Luis Potosí, Hidalgo y Querétaro; Beetle et al. (1999) también la citan para Tamaulipas y para Coahuila. Crece en campos abiertos, arbustivos o pastizales, sobre suelos arcillosos, húmedos o cerca del agua, entre 1000 y 1900 m.s.m. (Beetle et al., 1999). Observaciones. Esta especie ha sido poco colec- cionada y citada pero sus caracteres distintivos la separan claramente de las restantes especies del subgénero; se caracteriza por sus espiguillas orbicu- lares y por las vainas — € — densamente papiloso-pilosas con pe Los fragmentos 'rvados del exea (US 8949) e isotipo (US 928947) presentan espiguillas levemente glabrescentes con respecto al material examinado de Paspalum mutabile. Material examinado. MÉXICO. Hidalgo: Jacala, axes 7100 (SI). Querétaro: bern nn del Río Marta Mari ca. de Tanchanaquito, Zamudio & Carranza 7251 (MEXU. Potosí: 14 mi. by rd. N of Valles toward Nuevo Morelos, Johnson & Graham 40094 (MEXU). 7. Paspalum planum Hack., Bull. Herb. Boissier, 7: 448. 1907. TI in regione fluminis Thu”, nov (holotipo, W!; isotipos, BAA!, 2855825", W!). Figuras 3A, sér. 2, PO: Poetas: “In campis , E. Hassler 9647 BM 61, Ki, Pt, US Annals of the = Missouri Botanical Garden A di Moenia e es Aa irri "igura 6. om mutabile Chase. —A. Hab jina —b. guilla, vista del lado de la y Antecio superior, eeg dorsal mostrando —6. —H. Pálea superior. lodículas y estambres. A-H de Johnson & "m ábito. —B. Detalle y 2 nn —L. Porción del gluma superior. E guilla, vista del lado la lema superior. cio e vista ventral mos 1094, MEXU. raquis de los racimos, de la lema inferior. —F. trando la pálea superior. am 40 Denham et a Volume 97, Number 1 l. 2010 Estudios en el Género Paspalum € P telmatum T P trichophyllum ae ——— _ -— - e 0° 120° 100° BA iis * mmt i eo Lara, y he w. et ^t `, emt oa Figura 7. Distribución de m telmatum Swallen, P. ex E. gcn y P. denticulatum Trin T" ns Mez, Repert. Spec. Nov. Regni Veg. 15: 7. TIPO: Paraguay. Caaguazú: Caaguazú, 9 nov. a yi Balansa 70 (lectotipo, designado por Zuloaga y Morrone, 2003: 494, B!; duplicados. B!, BAA!, G!, K!, L no visto, P!, SI!, US 2 2942532!). Plantas perennes, cespitosas, con innovaciones intravaginales, macollas de base rojiza o pajiza; cañas simples, erectas, de (30—)60-150 cm, 2-4(-5) diám.; entrenudos 3 a 4, comprimidos, estriados, huecos, glabros; nudos oscuros, glabros, raro con pelos cortos. Vainas inferiores menores que las superiores, de 6-16 cm, carinadas, estriadas, glabras a esparcidamente pilosas o hirsutas hacia la región ligular; cuello glabro a papiloso-hirsuto; lígulas decurrentes con las vainas, membranáceas a coriá- ceas, de 2-3 mm; pseudolígula ausente; láminas trichophyllum Henrard, P. planum Hack., P. pubiflorum Rupr. lineares, de (10-30-40 cm, con base angostada, rígida, de 1—1.5 mm de ancho en la porción basal, aplanadas hacia la porción media y superior, hasta de (3-)4-6 mm de anal, glabras a cortamente pu- bescentes, agudo, laminas su e 40 em, cilíndricos, estriados, glabros; inflorescen- cias terminales exertas, de 4-13 X 1-3 cm; eje principal de 5-10 em, aplanado, glabro; pulvínulos glabros a pilosos, con pelos hasta de 5 mm; racimos 4 a 8, ascendentes, alternos, los superiores a veces subconjugados, terminando en una espiguilla desarro- llada; raquis de los racimos de 1.5-5 cm X 0 1.2 mm, violáceo o pajizo, glabro; pedicelos de l- 3 mm, escabriüsculos; espiguillas en pares, distribui- das en 4 series sobre el raquis, imbricadas o no, raro CC I, la espiguilla inferior abortada. Espiguillas elipsoides, de 34,5 X glabras, .8-2.2 mm, ligeramente plano-convexas, pajizas y con tintes pürpureos, de ápice agudo; gluma inferior ausente, rara vez presente, en este caso menor de 1 mm; gluma superior tan larga como la espiguilla, membranácea, delicada, de dorso finamente papiloso y escabritisculo, 3-nervia, de ápice m o brevemente em lema inferior glumi- orme; pálea y flor inferior ausentes. Antecio superior ar 0.4-0.8 mm más corto que la gluma superior y lema inferior, crustáceo, pajizo, lustroso, fuertemente papiloso, con ¿srl — de Lo 2, de E no vista. Iconografía. Zuloaga y Morrone, 2005: 209. Distribución geográfica y hábitat. Hasta el mo- mento era sólo conocida por las colecciones tipo de Paspalum planum y su sinónimo; aquí se amplía su distribución a Paraguay oriental, en el departamento de Canindeyú y Brasil central, en cerrados de Bahia y Minas Gerais. Habita en terrenos bajos y húmedos, sobre suelos arenosos, pudiendo hallarse en suelos de arenas blancas; llega hasta los 1600 m.s.m ápice obtuso; es 3, anteras de Observaciones. Esta especie se distingue por las innovaciones intravaginales, las láminas con base gostad racimos cortos, hasta 5 cm, con espiguillas grandes, de 3—4.5 mm de largo Chase (ined.) trata a esta especie buio el grupo Linearia; incluye en este grupo un total de 10 especies y ] os t 1 4 : š excepcionalmente cuatro o cinco, con espiguillas solitarias, en pares en Paspalum ovale Nees ex Steud. Paspalum ovale y P. planum se distinguen de las restantes especies de Linearia ia (sensu Chase, ined.) Je tener infl y espiguillas en pares sobre las citaciones, Paspalum ovale fue ubicado en el grupo Ovalia (Zuloaga € Morrone, 2005) y P. oo asignado al grupo Livida (Zuloaga & Maroma, 2005). Mez (1917), al describir Paspalum oryzoides, men- ciona bajo el material tipo de la especie los ejemplares Balansa 70 y Hassler 9647; éste último id al material de la colección tipo de P. planu Material examinado. BRASIL. Bahia: Mpio. M entre Andaraí y Mucugé, 5 km N de Mue ugé, i et al 1799 (IBGE, MO, 5D. — do Espinhaço, yw et al. Formosa, Parque Nac. G à à 1918 —— Et Canindeyú: Carpa Cué, Jimenez 1773 (CTES 8. Paspalum pubiflorum Rupr. ex F. Mexic. Pl. 2: 11. 1886. TIPO: México. Pads Tehuacán de las Granadas, 5500 ft., s.d., M. Annals of the Missouri Botanical Garden Galeotti 5747 (holotipo, BR!; isotipos, P!, US 2855739! [fragm. ex P]). Figuras 3E, 7, 8. "d "Ls var. viride t. ourn., Mexic. Pl. 2: 11. : México. San L otosí: San Luis Potosí, s. T te 1328 o pt: isotipo, US 2855738). Paspalum planifolium E. Fourn., Mexic. 1. 2: 10. 1886. PO: México. San Luis Potosi: San Luis Potosi, s. a. Mo s.n. (lectotipo, designado por Chase, 1929: 28, Hie US 2942528! wen ex i um Scribn., Bull. 3(1): 19. 1892. TIPO: EE. UU. Texas: sep. 1883, V. Havard 3 (holotipo, US 2855997!). m p paa var. glabrum Vase . Sta. Univ. Tennessee i i “TIPO: Ee UU. Tennessee: Davidson rw Belle Meade, jul. Scribner s. = fetis designado por es 1929: 56, US 741 Paspalum remotum var. glabrum Vasey, Bull (m Bot. U E 36 (lectotipo, designado por Chase, 1929: 55, US 2855999!) Paspalum geminum Nash, Bull. New York Bot. Gard. 1(5): 34 TIPO: EE. UU. Florida: Lake Co., Eustis, visto; isotipos, N NY 6624 no visto, US 207693!). xd arsenei Chase, Contr. U. s. = Herb. 28: 63, f. 1. 1929, pa nov. 2 México. Puebla: Mayorazgo Puel a, 2120 m. 1 jul. 1907, B. G. Arsëne nur Fo = 1000431!, foto SI!; tds MO 841741!). Plantas perennes, con rizomas cortos, canas decumbentes a estoloníferas, porción erecta de 130 cm, 0.1-0.4 em diám., simples a ramificadas; entrenudos de la porción erecta de 7-20 cm, macizos a fistulosos, glabros, paj o con tintes violáceos; nudos densamente pe con pelos blanquecinos a glabrescentes. Vainas más cortas o más largas que los entrenudos, glabras a esparcidamente pilosas, estria- das, los márgenes membranáceos, glabros a pilosos hacia la porción superior, cuello glabro; lígulas membranáceas, de 1.54 mm, castañas; pseudoligula ausente o formada por pelos escasos hasta de 4 mm; láminas lineares o linear-lanceoladas, de 8-30 X 0.6- glabras, menos frecuente- agudo a setáceo, los márgenes escabrosos. Pedúnculos exertos o subexertos, hasta de 30 cm, glabros, estriados, cilíndricos a aplanados; inflorescencias terminales de 5-20 X (2-)4-7 cm; eje principal de (2-4-12(-18) em, aplanado, surcado, glabro; pulví- nulos escasamente pilosos, con os de mm; racimos (2-)3-12, ascendentes a divergentes, los basales alternos y los distales subopuestos; raquis de los racimos de 3-8(-10) cm X 1.2-2.1 mm, los distales reducidos, planos, verdosos, glabros, con los márgenes escabrosos, terminando en una espiguilla Uu eee ae | Volume 97, Number 1 Denham et al. 27 2010 Estudios en el Género Paspalum Figura 8. Paspalum i ton Rupr. ex E. Fourn. —A. Habito. —B. or de la lígula. —C. Porción del raquis de los pem. pedicelos. —D. E spuguilin, dum a del lado de la gluma superior. —E. Espiguilla, vista del lado de la lema inferior. —F. Antecio superior, vista dorsal mostrando la lema superior. —(. Antecio superior, vista ventral p la pálea superior. —H. Cariopsis, vista eds ar. ye Cariopsis, vista hilar. A-I de Reeder & Reeder 2611, MEX Annals of the Missouri Botanical Garden desarrollada; pedicelos en pares, desiguales, el superior de 0.8-1 mm, triquetros o cilíndricos, escabriúsculos; espiguillas distribuidas en 4 series, en ocasiones la inferior abortada. Espiguillas elip- soides a obovoideo-elipsoides, de (2.4-)2.6-3.2 X 1.3-2 mm, plano-convexas, túrgidas, gibosas, sub- agudas, pubescentes, pálidas o con tintes violáceos; gluma inferior ausente; gluma superior ligeramente más corta que la espiguilla a subigual, con el dorso pubescente, raro glabrescente a glabra, con pelos cortos adpresos, más largos hacia los márgenes u homogéneos, 3- a 5-nervia; lema inferior glumiforme, tan larga como la espiguilla, esparcidamente pilosa a glabrescente, con pelos adpresos, 3- a 5-nervia; pálea inferior y flor inferior ausentes. Antecio superior anchamente elipsoide, tan largo como la espiguilla, castaño a la madurez, crustáceo, pajizo, finamente papiloso; lema con papilas regularmente distribuidas en toda su superficie, aguijones y micropelos bi- y tricelulares hacia la porción superior, los márgenes enrollados sobre la pálea, 5-nervia; pálea de textura similar que la lema, con papilas, micropelos y aguijones; lodículas 2, ca. 0.3 mm; estambres 3, anteras de 1.4-1.6 mm; estigmas plumosos. Cariopsi elipsoide, de 2 X 1.2 mm; hilo elíptico, embrión 1/3 de la cariopsis. Distribución geográfica y hábitat. Sudeste de Estados Unidos de América, México y Cuba. Crece en suelos arcillosos, cerca de cursos de agua, en las laderas de los bosques caducifolios, entre 400 y 2000 m.s.m. Números cromosómicos. 2n = 60, 64 (Gould, 1966). Observaciones. Chase (1929) incluye en el grupo Livida un total de ocho especies y lo caracteriza por comprender plantas perennes, con cañas comprimi- das, láminas mayormente planas, y espiguillas de 2- 3.1 mm. Dentro de este grupo, separa a Paspalum arsenei de P. pubiflorum por tener la primer especie espiguillas plano-convexas, deprimidas (vs, llas turgentes, plano-convexas); este mismo criterio utilizan Mc Vaugh (1983) y Beetle et al. (1999). Sin embargo, al examinar un elevado nümero de ejem- plares, se verificó que este carácter es es morfológicamente afín a P. remotum, la que se diferencia por tener inflorescencias axilares, y espiguillas con antecio superior pálido a la madurez; además especies poseen una distribución disyunta, con P. remotum presente en Bolivia y Argentina. Material representativo examinado. . Habana: Habana, Cerro, Ekman 938 (G, US); near Zanja Real, Ekman 908 (US). EE. UU. Texas: Val Verde Country, Miller et al. 5747 (SI). MÉXICO. alientes: Aguascalientes, La Cantera, s.d., Calvillo s.n. (MEXU). Chihuahua: 10 mi. N of Ciudad Camargo, Reeder & Reeder 2611 (MEXU). ila: Palmer 515 (MEXU). Durango: Tlahualilo, La Jarita, Bermejillo, Rodríguez Castañeda 37 (MEXU). Gua- najuato: La Presa, Sohns 268 (US). Guerrero: Buenavista de Cuellar, González Quintero 1408 (MEXU). Hidalgo: Valle del Mezquital, Río de Tasquillo, s. coll. 161 (MEXU). Hernández 9388 (SI). K Zapote, Arséne 2693 (US). Morelos: carr. Chinameca- Tlaltizapan, ga et al. 7370 Monterrey, Hitchcock 5563 (US (MEXU). Puebla: Izúcar de Matamoros, cañada La Angos- tura, 16 km SE de Izúcar, Aragón 377 (MEXU). Zacatecas: Moyahua, Cerro La Cantarilla, 8.5 km S Moyahua por carr. 54, Enriquez 1316 (MEXU). 9. Paspalum remotum J. Rémy, Ann. Sci. Nat., Bot., ser. 3, 6: 349. 1846. TIPO: Bolivia. La Paz: Cotaña, “in valle calida sub monte Illimani”, 1839, J. B. Pentland s.n. (holotipo, P!; isotipos, OXF no visto, US 2855998! [fragm. ex OXF]). Figuras 2, 3F. Paspalum scrobiculatum L. var. pubigluma Hicken, Darwini- ana 1: 109. 1924. TIPO: Argentina. Salta: Quebrada del Río Toro y Río B 923, I. C. Vattuone 156 (holotipo, ST'; isotipo, SI!). Plantas perennes, rizomatosas, cañas decumbentes, arraigadas y ramificadas en los nudos inferiores, geniculadas a erectas, en ocasiones largamente estoloníferas, porción erecta de 30-90 X 0.4-0.7 cm; entrenudos de 3-15 em, comprimidos, estriados, macizos, glabros; nudos castaños, glabros. Vainas iguales a mayores que los entrenudos, flojas, glabras, estriadas, con los márge mbraná ; lisos, ondulados, con unos pocos pe la base. Pedúnculos 1 a 2, incluidos en la última vaina foliar, subexertos a exertos, hasta de 35 cm; inflor- escencias terminales y axilares emergiendo de la última vaina foliar; inflorescencias terminales de 5- 1420) x 410 cm; eje principal de 2-10 cm, aplanado, liso, glabro; pulvínulos con un mechón de pelos blanquecinos, rígidos, hasta de 4 mm; racimos 2 a 6, ascendentes, alternos, terminando en una espiguilla desarrollada; raquis de los racimos de 2- 10 x 0.12-0.2 cm, aplanado, glabro, verdoso o con tintes púrpureos, los márgenes escabriúsculos; pedi- celos en pares, desiguales, hasta de 1.2 mm, trique- Volume 97, Number 1 2010 Denham et a 29 Estudios en : Género Paspalum tros, escabritisculos; espiguillas — distribui- das en 4 series; inflorescencias axilares por un racimo solitari e elip- soides, de 2.8-3. 4-3. 6) X 1.6-2 mm, agudas, plano- convexas (concavo-convexas en Hunziker 1786), túrgidas, verde ¿eg a purpúreas, pubescentes; gluma superior y lema inferior lacada, membra- náceas, con el dorso finamente papiloso y homo- géneamente piloso, con pelos cortos, delicados, hasta de 0.3 mm; gluma inferior ausente u ocasionalmente argo de la espiguilla; gluma superior tan larga la espiguilla o levemente más corta, 5-nervia, con un nervio central, los restantes "— ales inferior glumiforme, tan | como la espiguilla, x inferior ausente, ocasionalmente pre- sente, rudimentaria, hialina; flor inferior ausente. io superior anchamente elipsoide, de 2.6-3.4 X 1.6-1.8 mm, crustáceo, fuertemente papiloso, pajizo, glabro; lema con papilas regularmente distribuidas en toda su superficie y micropelos bi- y tricelulares hacia la porción superior, los márgenes enrollados sobre la pálea; pálea de textura similar que la lema, con papilas y micropelos; lodículas 2, ca. 0.4 mm; esta d 3, anteras de 1.2 mm, cobrizas a purpüreas. Cariopsis no vista. nervia; Iconografía. Zuloaga y Morrone, 2005: 229. Distribución geográfica y hábitat. Noroeste de Argentina y Bolivia. Se halla en márgenes de selvas en lugares húmedos desde los 1200 a 2800 m.s.m.; es frecuente en áreas de cultivos, n = 40 (Hunziker et al., 1998). Número cromosómico. Observaciones. Esta especie se reconoce por su hábito rizomatoso, por la presencia de inflorescencias axilares y espiguillas túrgidas. Especie afín a Paspalum pul. véanse deno bajo esta espec ie. er ñ raquilla por dai ad antecio utri, como por ejemplo en el ejemplar Zuloaga 5826. Material representativo examinado. ARGENTINA. Ju- juy: Dpto. El Carmen: Ruta Nac. 9, camino de Jujuy a Salta, Abra de Santa Laura, Zuloaga 5826 (SI). Salta: Dpto. Caldera, Alto de la Sierra, Zuloaga & Morrone 3062 (SI). Tucuman: Dpto. Tafi, Tafi de 5 5 BOLIVIA. € Viscachani — Río Las Canoas on rd. from Tarvita to Azurduy, 1 & Serrano 14506 (LI n. Cochabamba: Cochabam . dier y Holway pr (US). La Paz: vic. Sorata. ed 1252 W) Tarija: Prov. Cercado, Valle de Tenis. n 182A q AL) Imatum Swallen, Phytologia 14: TIPO: Brasil, —' . 1967. Mato Grosso do Sul: betw. Campo Grande & Dourados, Lagoinhas, 400-500 m, 14-17 feb. 1930, A. Chase 10926 (holotipo, US 1500550!; isotipo, SI!). Figura 7. Plantas perennes, largamente ri comprimida, fl a; cañas erectas, d 0.2-0.3 cm, iie simples; tinm de » 15cm, los basal mid s, huecos, g glabros a pilosos. Ves nas predominantemente basales, mayores que los entrenudos, de 9-25 cm, comprimidas, quiladas, pilosas, con pelos rígidos, adpresos, las res glabras, los márgenes ciliados; lígulas M = 0.8-1 mm, truncadas, castañas, glabras; cuello hirsuto; láminas lineares, de 15-50 x 0.4— 0.6 cm, usualmen es, rígidas, ascendentes, densamente pilosas hacia la base y en los márgenes, anas o con los márgenes involutos, de base continuándose imperceptiblemente con la vaina, el ápice setáceo, las superiores reducidas exertos, hasta de 35 cm, indico. estriados, glabros; eje principal de 6-12 cm, aplanado, surcado, glabro; rescencias terminales de 9-16 X 2-3 cm; pulví- nulos con un mechón de largos pelos blanquecinos; únc racimos 3 a 8, ascendentes, alternos, terminando en una espiguilla desarrollada; raquis de los racimos de 20-60 x 0.6-0.8 mm, uini glabro, verdoso, los márgenes escabriúsculos; pedicelos en pares, hasta de 1 mm, triquetros, escabritisculos, glabros; espiguillas abortadas hacia Espiguillas elipacides, ps 24-3 el ápice del raquis X ]-1.2 mm, Egas amente plano-convexas, agudas a apiculadas, glabras, pajizas o verde pálidas; gluma superior y lema inferior subiguales, hialinas, finamente papilosas; gluma n larga come con un nervio c nik los restantes — ausente; gluma superior ta > la espiguilla, 3-nervia, als verdosos; lema inferior glumiforme, tan larga como la espiguilla, 3-nervia; pálea y flor inferior ausentes, Antecio superior anchamente elipsoide, de 2— 2.4 3 mm, crustáceo, papiloso, pajizo, ca. 0.4 mm más corto que la gluma superior y lema inferior; lema 5-nervia, con papilas simples y pelos bicelulares hacia el ápice, pálea similar a la lema; lodículas 2, ca 2 mm: estambres 3, anteras de 1.2-1.8 mm. Cariopsis no vista. Iconografía. Zuloaga y Morrone, 2005: 245. Distribución geográfica y hábitat. Se halla en el sur de Brasil, en Mato Grosso do Sul, y en Paraguay. en los departamentos Amambay y Canindeyú; crece en borde de lagunas y ríos, sobre suelos hümedos y arenosos. 243) Livida y la Zuloaga y Morrone (2005: especie en el Observaciones. ubicaron esta grupo relacionaron con Paspalum denticulatum, de la cual P. telmatum se diferencia por “incluir plantas con bases flabeladas, vainas aquilladas, espiguillas elip- Annals of the Missouri Botanical Garden soides, con gluma superior y lemma inferior más largas que el antecio superior, 3-nervias”. Filgueiras (1993) reevalúa las especies deseritas por Swallen (1967) y trata a P. telmatum como sinónimo de P. malacophyl- lum Trin., por considerar que su holotipo es similar al P. planiusculum (= P. malacophyllum), otra especie deserita por Swallen en la misma obra. Paspalum + especie tipo del subgénero Anachyris, se separa, al igual que el resto de los taxones de este subgénero, por presentar la lema surcada en la cara abaxial, con nervios conspicuos, y por las espiguillas naviculares. Recientemente, Oliveira y Valls (2008) incluyen a P. telmatum en la sinonimia de P. wrightii Hitchc. € Chase, especie perteneciente al grupo Plicatula; este grupo se distingue por incluir especies con espiguillas castaño oscuras, antecio superior del mismo color y lema inferior usualmente con pliegues transversales, Oliveira y Valls (2008) no citan material examinado y consideran que la coloración del antecio superior es variable en la especie. El examen de material tipo, y material de herbario de ambos taxones, permitió concluir que P. telmatum se separa de P. wrightii por tener vainas y láminas densamente pilosas, espiguillas pajizas o verde pálidas, con gluma superior y lema inferior más largas que el antecio superior, este último pajizo, no castaño a la madurez. » - BRASIL. Mato Grosso do Sul: Mpio. Bataguacu, Porto XV, Hatschbach 23523 (MO). PARAGUAY, Amambay: in regione cursus superioris fluminis Apa, Hassler 8247 (BM, C, MO, US). Canindeyá: Reserva N l ` Mbaracayú, Lagunita, Schinini & Dematteis 33252 (CTES, SI); s. loc., Hassler 8847 (US). 11. Paspalum trichophyllum Henrard, Blumea 4: 513. 1941. TIPO: Brasil. Pará: Ilha de Marajó, Faz. Gavinho, ene. 1918, A. Goeldi 165 (holotipo, - nO visto; isotipos, MO-912393!, US- 1039599! , W!). Figuras 7, 9. Paspalum denticulatum Trin. var. ciliatum Trin., Sp. Gram. 2: t. 1234. 1829. TIPO. Brasil. s. loc., s. coll. s.n. (holotipo, LE!; isotipo, SI). Paspalum trinii Swallen, Phytologia 14: 360. 1967, s wall y : 360. + Syn. nov. TIPO: Brasil. Ceará: Crathéus, 9-10 May 1934, J. R. Swallen 4507 (holotipo, US-1613382!; isotipo, K!). Paspalum pisinnum Swallen, Phytologia 14: 360. 1967, syn. nov. TIPO: Brasil. Piauí: betw. Fazenda Nacional & dcos, 4-5 Apr. 1934, J. R. Swallen 4217 (holotipo, US-1613175!; isotipo, U ! Paspalum goeldii Swallen, ytologia 14: 361. 1967. TIPO: Brasil. Pará: Estate Gavi j6 Island, June 1918, E. A. Goeldi 197 (holotipo, US-1039605!- isotipo, F- 551796), foto SI!) x ' P. Plantas perennes, cortamente rizomatosas; cañas floríferas de 30-90 X 0.2-0.4 cm, erectas, menos frecuentemente decumbentes hasta estoloníferas y arraigadas, simples, ocasionalmente ramificadas; en- trenudos de 4-15(-20) cm, estriados, glabros, compri- id ilíndri g l te h , raro macizos; nudos oscuros, glabros a pilosos. Vainas de 3-17 cm, us te más cortas que los entrenudos, numerosas en la base, lateralmente comprimidas, aquilladas, flojas, estriadas. slab d t pil hacia la porción basal, los márgenes membranáceos, glabros; lígulas de l-5 mm, membranáceas, castañas, glabras, decurr- entes, pseudolígula ausente o presente, con pelos hasta de 5 mm, cuello glabro; láminas lineares, de (3) 4-29 em X 1-58) mm, las apicales reducidas, numerosas en la base, erectas, involutas a planas, glabras o hispídulas, de base angosta y ápice acuminado, los má hasta de 40 cm, cilíndricos, acanalados, estriados, glabros; inflorescencias terminales, de 3-16 X 1-6 cm; eje principal anguloso a aplanado, finamente estriado, escabriúsculo; racimos 3 a 19, ascendentes, adpresos a divergentes del eje principal, alternos; pulvínulos ; raquis de los racimos de 1-6 cm X 0.3- 1 mm, aplanado, escabroso en ambas caras y los márgenes, éstos glabros o esparcida a densamente pilosos con pelos tuberculados, blanquecinos, hasta de l cm, terminando en una espiguilla desarrollada; pedicelos en pares, de 0.4—1.2 mm, glabros o híspidos, escabriúsculos; espiguillas imbricadas, distribuidas en 2 a 4 series, frecuentemente la inferior abortada. Espiguillas elipsoides a anchamente elipsoides, de (1.4-)2-2.3(-2.6) x 1-1 A(-1.7) mm, plano-convexas, no turgentes, de ápice apiculado, a veces redondo, pálidas o con tíntes violáceos, glabras, marcadamente escabrosas; gluma inferior ausente; gluma superior tan larga como la espiguilla, membranácea, marcadamente escabriúscula sobre los nervios, el resto de la superficie hispídula, 3-nervia, con un nervio central, los restantes submarginales; lema inferior glumiforme, tan larga como la espiguilla, 3-nervia, marcadamente escabriúscula re los nervios; pálea inferior y flor inferior ausentes. Antecio superior elipsoide, tan largo como la espiguilla, cartáceo, papiloso, pájido, glabro; lema superior con papilas simples, conspicuas, el ápice con aguijones, los márgenes fuertemente enrollados sobre la pálea; pálea imil il Í-k du. on: 0.2 mm, conduplicadas; estambres 3, anteras de 0.9— 1.2 mm. Cariopsis no vista. Distribución geográfica. Noreste de Brasil, en los de Pará, Piauí, Pernambuco, Ceará, Maranhao y Bahia, Guayana Francesa, Guyana y Bolivia, en el to Santa Cruz; crece en sabanas inun- dables, desde el nivel del mar hasta 500 m.s.m. Volume 97, Number 1 Denham et al. 31 2010 Estudios en el Género Paspalum A, Ay 7 NH EN BN ^ a 9. “ue mg Henrard. —A. Hábito. —B. Detalle de la lígula. —C. Porción del raquis de los racimos, baud: elos. —D. iguilla, vista del lado de la gluma pese —E. Espiguilla, vista del lado de la lema inferior. —F. Antecio superior, vista dorsal mostrando la lema superior. —G. Antecio superior, vista ventral mostrando la pálea superior. —H. Pálea superior, lodículas y filamentos estaminales. A-H de Killeen 1655, SI. Annals of the Missouri Botanical Garden Número cromosómico. 2n = 20, bajo Paspalum humigenum (Norrmann et al., 1994). Observaciones. Especie afin a Paspalum denticu- latum por tener espiguillas glabras; se diferencia por las espiguillas y los raquices marcadamente escabro- sos. Véase Chase (ined.) y Zuloaga y Morrone (2003) para discusión sobre la identidad del tipo de P. denticulatum var. ciliatum. Chase (ined.) incluyó en la exsiccata de Paspalum yllum material posteriormente citado por Salim (1967) al describir a P. goeldii, P. humigenum, P. pisinnum y a P. trinii. Así, en Chase (ined .) aparecen bajo P. trichophyllum los paratipos de P. goeldii, P. trinii, y los holotipos de P. humigenum y P. pisinnum. Zuloaga y Morrone (2003) consideran a P. goeldii y P. humigenum como sinónimos de P. trichophyllum. Los caracteres del porte de las plantas, námero de racimos, ancho del raquis y tamaño de las espiguillas usados por Swallen (1967) al describir a P. goeldii, P. humigenum, - pisinnum y P. trinii, resultan insuficientes en este análisis para diferenciar estas entidades, las que, en consecuencia, se incluyen en la sinonimia de P. trichophyllum. La escabrosidad de espiguillas y raquis *s constante en todo el material observado y se considera un carácter diagnóstico para la especie. Filgueiras (1993) considera a Paspalum goeldii, P. humigenum, P. pisinnum y P. trinii como iónicos racimos, caracteres que definen a P. trichophyllum. Material Merry examinado. BOLIVIA. Santa Grun Ñuflo de Chávez, 10 km SE of Concepción, Fa. Salta, Killeen 708 (G, LPB, MO); Est. Salta, 10 km S of Concepción, Killeen 1655 (LPB, MO, SI); Prov. Velasco » San Ignacio 35 km hacia W, I 113 (K, MO, SI, US). BRASIL. 1 Bahia: Rodovia para Sa aria da Vitória, ta Mec Seo 0D. Joazeiro, Dorsett & P Popenoe 406b Ceará: (US). Quixada, Swallen 4463 (US); Cratheús, Swallen 4510 (US). * Marajó i 169, 185, 193, (09) Kuhlmann 2135 (US), Black 8982 ( US), Swallen 4940 (US); Ilha de Mexiana, Huber 2737 (G), 2400 (G, E s. J É. Mk E á. M. dh 1994. " Catálo ogo de la Familia Poaceae en la Ie Argentina. Monogr. Syst. -178. Bot. Missouri Bot. Gard. 47: REVISION OF THE CARIBBEAN GENUS GINORIA (LYTHRACEAE), INCLUDING HAITIA FROM HISPANIOLA! Shirley A. Graham? A — “ ` ABSTRACT summarized for Ginoria and the putatively closely related genera Crenea Aubl., Haitia Urb., Lawsonia L., and Tetr. C. i i ime. Gi species make them highly vunerable to éatinction. Key : Caribbean, Cuba, Ginoria, Hi Lawsonia is sister to Ginoria ' y when Haitia is included in the genus. Phylogenetic analysis + Jimenezii Alain, a rare species from the Dominican Republic, is ; ta "TES uus eee Sr i, . ka x noria is minimally paraphyletic and possibly inoria based data. Phylogenetic dsl E tU u My based on the strength of the morphological evidence. Further pling among the putatively related genera is possible. Thirteen uba, i i five from Hispaniola, and one fro co and t les, taxonomic descriptions, illustrations, and distribution Three new combinations, G. buchii (Urb.) S. A. b.) S. A. Grah am, and G. americana Jacq. var. spinosa (Griseb.) S. A. Graham, are are brought into synonymy: G. spinosa Griseb. and G. davisii M. C. Johnst. Evolution of selected characters context. The endemic nature and rarity of the majority of aitia, Hispaniola, IUCN Red List, Lythraceae. y xar eee I CA Ginoria Jacq. (Fig. 1) is a small genus of the is closely similar in Hispaniola; the rare monotypic Tetrataxis Hook. f. from the Indian Ocean island of Mauritius (Graham & Lorence, 1978); and Crenea Aubl., a ditypie genus of rhizomatous shrubs from coastal northern South ' Field studies in Cuba we R ical Garden, P.O. Bo: 53 re Supported in part by grants from the American Council of Science Research Council. I thank Reina Echevarría, Pedro He Grah America (Lourteig, 1986). Although the species of poorly collected, more than half are endangered or critically endangered, and most, in the absence of fully comparative species descriptions, are poorly known taxonomically. The monograph of the genus (Koehne, 1882, 1903) includes just seven of the 14 species recognized in most floristic accounts today. Howard's (1975: 378) comment that “few monogra- phers have considered at one time all of the species of a genus for the pan-Caribbean area” is relevant to the present taxonomy of Ginoria. An initial morphologically based phylogenetic assessment of relationships among Crenea, Ginoria, Haitia, and Tetrataxis (Graham, 2002) included in a symposium on the historical biogeography of Car- ibbean endemics (Fritsch & McDowell, 2003) sug- gested that Ginoria was monophyletic only if the two Learned Societies of the Social Tera, Alison Graham, Charlotte Taylor, Alfredo Noa, Rafael Mm Sn sio cm 3 ] E». Frhovarría Graham ponided expertise in palynology nsae and Julie Morris rated on that were necessary to accomplish this study. @mobot.org. neci te x 299, St. Louis, Missouri 63166-0299, U.S.A. shirley.graham ANN. MISSOURI Bor. Garp. 97: 34-90. PUBLISHED ON 31 Marcu 2010. tS T RE E EI. Volume 97, Number 1 Graham 35 Revision of Ginoria (Lythraceae) Figure l. To : left, Ginoria americana; right, G. nudiflora. Middle row: -— G. rohrii; right, G. ginorioides. Bottom row: Ç “buchii. Monk top and middle rows by S. Graham: bottom row by H. Lic Annals of the Missouri Botanical Garden "OR, ia. shown in black Note €. M. s left nd The easternmost extension of the genus comprises Puerto Rico and the x Islands. species of Haitia were included in the genus. Overall support for the tree was weak and analyses were inadequate to determine the sister to Ginoria. A recent family-level phylogenetic investigation using data nuclear ITS region included one exemplar Ginoria. The study ‘ea a sister relationship to Tetrataxis and clade membership with Ammannia L./ Nesaea Comm. ex Kunth and Lawsonia L. (Graham et al., 2005). The present study revisits the relationships of Ginoria to its putative relatives Haitia, Tetrataxis, and Crenea through more extensive morphological/ anatomical comparisons and by additional phyloge- netic analyses of ITS sequences for six species of Ginoria. A revised taxonomy of Ginoria is presented with new keys, distribution maps, and illustrations of the species. Taxonomic History Ginoria was established in 1760 by Nicolaus Jacquin, who described G. americana Jacq. based on his Cuban collections. He named the genus after his benefactor and friend, the Marchese Carlos Ginori, successful founder in 1735 of the highly regarded Ginori fine porcelain factory near Florence, Italy, a company that remains in operation today as Richard- Ginori Porcelain. In 1792, the genus Antherylium Rohr & TM was dna from St. — by J. re Rohr and on by M. Vahl's species. diagnosis of A. prts Vahl, illustrated as A. rohni. More than half a century later, in 1866, the rich collections of Charles Wright from Cuba led the German botanist August Grisebach to describe G. glabra Griseb., G. spinosa Griseb., and (black dot at Dipl n ginorioides Griseb. (G. ginorioides (Gri- seb.) Britton). In 1880, William Hemsley added Antherylium nudiflorum Hemsl. from Oaxaca, Mexico. When Emil Koehne monographed Ginoria (1882) as part of his expansive work on the Lythraceae, he placed Antherylium in synonymy of Ginoria, added G. curvispina Koehne, and erected two subgenera for the seven species he recognized. His treatment of Ginoria remained unchanged in a monograph of the Lythra- ceae (Koehne, 1903) except for division of subgenus Euginoria Koehne) into sections the Koehne) and Dis- cospermum Koehne (Appendix 1). From 1912 to 1927, the explorations of Erik Ekman and Nathaniel Britton in Cuba and Hispaniola added seven species to Ginoria, which were described by Britton and Wilson at The New York Botanical Garden and by the Berlin botanists Ignatz Urban and Otto Schmidt. Since 1927, three more species have been described, bringing the total species to 17, more than twice the number recognized in the 1903 monograph. Nine species were recognized in Cuba by León and Alain (1953, reprinted 1974), all endemic to the island. In 1919, Urban erected the genus Haitia, based on H. buchii Urb. He ee Mu distinct "m ia by possessi the prominent lyx that th ior of the floral cup at the base of the sepals, and bd the 6-locular ovary, as opposed to the 3- or 4-locular ovary considered typical of Ginoria. A second species, H. pulchra Ekman & O. C. Schmidt, was described by Schmidt in 1927 who, at the same time, described G. callosa O. C. Schmidt with a 3- to 5-locular ovary Haitia has been unquestionably accepted in floristic A lll Volume 97, Number 1 2010 Graham Revision of Ginoria (Lythraceae) accounts of rege as distinct from Ginoria since its e (Urban, 1920; Moscoso, 1943; Liogier, 1986). Koe ne (1903) classified Ginorie and Tetrataxis together as only m unnamed series III in his tribe Nesaeeae subtribe Nesaeinae Koehne. Crenea represented series I in the same subtribe. MATERIALS AND METHODS FOR SYSTEMATIC OBSERVATIONS Data were gathered by examination of living specimens in the field in Cuba Mexico; from greenhouse-grown specimens siis through the Cienfuegos Botanical Garden in Cuba, Fairchild Tropical Garden in Miami, Florida, and Dr. George Proctor; and from study of exsiccatae (A, AJBC, CHAPA, CM, ENCB, G, GH, GOET, F, FF, FTG, HAC, HACC, HAJB, HCZ, HIPC, HJSS, HPVC, IPTH, JBSD, JE, K, LL, MEXU, MNHNC, MO, NY, S, TEX, UPRRP, US). Citations of herbaria follow Index Herbariorum (Holmgren et al., 1990) and are updated online at . The fol- lowing abbreviations from the list rw above are for Cuban herbaria not listed i F - Herbarium, National Enterprise for de Protection of Flora and Fauna, Villa Clara, Cuba; HCZ, Herbario de la Ciénaga de Zapata, Matanzas; HJSS, El Jardín Botánico = Sancti Spiritus; IPTH, E de MNHNC, nas; and | Jardin Botanico Herbario del Museo dk de Historia Natural, diana, In the citations of specimens examined, collectors’ names are limited to the family name unless confusion would result; the first initials are provided for all names in the Index to Exsiccatae at the end of the study (Appendix 2). Flower buds from field am agre h some counts we ixed in 3 ethanol:1 glacial acetic acid, Bird. to 70% alcohol for storage at 40°F, hydrolyzed 10—15 min. in IN HCl at 60°C, and stained in acetocarmine. Counts were made by using a Zeiss ‘a microscope (Carl plants for chromo Zeiss, Oberkochen, Germany) with phase contrast and 100X oil objective lens. Pollen samples were processed by the standard acetolysis method of Erdtman (1960). Pollen and seed coat morphology were observed with SEM after sputter-coating acet- olyzed pollen and untreated seeds with gold-palla- dium. Materials and methods used in molecular and morphological cladistic analysis of Ginoria are detailed i in the section on phylogeny. MORPHOLOGY AND ANATOMY HABIT Species of Ginoria range in habit from low suffruticose perennials to tall trees. Ginoria amer- icana, a suffruticose perennial, has the smallest habit, attaining 1.5 m or less in height. Gino (Hemsl.) Seis can reach 40 m in the us forests of Chiapas but is typically up to (Miranda, 1952), and G. jimenezii Alain is hara as 12-15 m in height (Liogier, 1968). The rest of the species are erect or sprawling shrubs of ca. 2 m to 7-8 m depending on local growing conditions and age. Most have a xeromorphic aspect with thick, shining, coriaceous leaves and are small trees reaching ca. deciduous or semi-deciduous. The branching pattern in the genus is frequently irregular by abortion of ent devel- from subterminal hs ie buds Stems of the current season are slightly 4-angled to narrowly 4-winged and often red-tinged. They become terminal vegetative buds and the subsequ opment of branches increasingly terete and gray-brown with age. Inter- nodes are often shorter than the subtending leaves and may become very short toward the tips of the branches. All species are deciduous during the dry season except G. americana, which grows rooted in streams or rivers or along their margins and retains leaves throughout the year. The two species of Haitia ve the same small perennial shrub habit and = Ë frequently have abortive buds as in Ginoria. In related genera, Tetrataxis is a small tree to 12 m and Crenea is a rhizomatous, suffruticose perennial with winged or 4-angled stems; both have normally Alca terminal buds. WOOD ANATOMY The wood anatomy of Ginoria has been investigated with Ç. americana, G. arborea Britton. Ç. — G. koehneana Urb., Tetrataxis, and Crenea (Graham & busua 1978; Baas & Zwaan, 1979) and for Haitia pulchra (Baas, 1986). The genera possess the wood anatomical features that characterize the order Myrtales to whic vestures in bordered pits of secondary xylem p two major Lythraceae belong, i internal phloem derived from bicollateral stems (van Vliet & Baas, 1984). They also display numerous plesiomorphic lythracean wood anatomical characters including diffuse vessels with simple palatino, scanty Sod ded parenchyma, and heterogeneous rays. Ginoria shares with Capuronia Lourteig, Galpinia . Br., Lawsonia, Lourtella S. A. Graham, Baas & o ia Sprague, and Padia L. the following anatomic ally derived features: chambered crystallifer- ous fibers, heterogeneous type II rays, and abundant septate fibers (Fig. 3A, B). Baas (1986) found the anatomy of H. pulchra to be identical to that of Tetrataxis and different from Ginoria by the absence of chambered crystalliferous fibers and presence of heterogeneous type I rays. However, in one specimen Annals of th Missouri Botanical Garden inori dada = ha i des. Photos f; from . gential section, with large yes. € usss fibers ( preparation by Baas and Zwe T SJRW 19996). ini à ypfenning (SJ. e vessels visible in tuse vessels and scanty y paratracheal parenchyma typical of Ginoria. E oe Ia, a nd right of phetossaph, ts type II rays, and chambere -urved stout spines of G. loshneuna M Has, M wo. E. vL d C america To T. spinosa (Graham 1135, MO). —D. callosa (Ekman 4619, MO). Scale bars: A, B = CM CR "oki (Proctor 39535, MO). —F. 6 * = 1 m i 3 E k Ñ | É i | E | | Volume 97, Number 1 2010 Graham 39 Revision of Ginoria (Lythraceae) of G. americana studied by Baas, crystalliferous fibers were absent and he indicated that a more extensive survey might well produce overlapping anatomical ranges among the genera. my in the more herbaceous Crenea differs extensively from the others, having a juvenilistic appearance with juvenilistic rays, no crystalliferous — few septate fibers, and no dark vessel contents. se anatomical specializations — e ides show extensive ET development (Baas & Zweypfenning, 1979; Baas, 1986), iil because the full extent of anatomical diversity in Ginoria is unknown, no wood anatomical characters are used to assess phylogenetic relation- ships in this study. NODES AND LEAVES Characteristic of all Ginoria and Haitia are prominent, buttressed stem nodes on which leaf scars are oriented at a 45^—90^ angle to the stem. Nodes are not conspicuously buttressed on mature stems of Crenea but can be conspicuous on young winged stems. Sturdy spines form at the nodes in half of the species of Gineria. The nodes of G. americana spinosa (Griseb.) S. A. Graham (Fig. 3C), G. iiim G. curvispina, G. lanceolata O. C. Schmidt, and C. rohrii (Vahl) Koehne are consistently armed by two to four erect or curved spines as a result of the extension and induration of the free ends of the winged stem tissue. In G. koehneana, robust spines are character- istically present (Fig. 3D), but spineless plants from the western part of the range have been found. Ginoria americana var. americana generally is spineless, but close examination shows that most specimens have various degrees of spine development, from mere nubs to — formed stout spines. The spines of C. spinosa are — long, NM ades ak unlike others of the genus. The orientation of spines can vary slightly on an individual plant from recurved to horizontal or ascending, but there is a typical orientation in each species. Haitia, Tetrataxis, and Crenea are spineless. ‘aves in Ginoria and its idunt are decussate, mostly sessile or subsessile, entire-margined, ovate to elliptic or lanceolate, and range from thickly membranous to coriaceous. Venation is brochidodro- mous with a strong intramarginal secondary vein. Typically, there is blade tissue present between the i pu vein and the margin (Fig. 3E, F), but in G. americana var. spinosa, G. curvispina, G. koeh- neana, an and G T ata the tissue is absent and the intramarginal vein forms a cartilaginous margin. In Ç. glabra and G. americana var. americana, the intramarginal vein of smaller distal leaves infre- quently merges distally with the margin. veins are shallowly to sharply ascending and range from three to six on each side of the midvein (H. pulchra) to eight to 20 per side in larger-leaved species (G. ginorioides, G. nudiflora, and H. buchii). Tertiary venation is obscure to visible phe 3E) sea in G. callosa (Fig. 3F), G. glabra, H. pulchra which secondary and tertiary veins are ial thickened, pale yellow, and the tertiary veins form conspicuous intercostal areolae. Tertiary veins in G. koehneana are also dense and thick but not yellow. TRICHOMES All species of Ginoria, Haitia, Tetrataxis, and Crenea are glabrous on all parts with the partial i of G. americana, the stems of which can be tly puberulent si minute, dark, unicellular en INFLORESCENCES Inflorescences in Ginoria, Haitia, Tetrataxis, and Crenea terminate in a da bud (polytelic sensu Weberling, 1988; blastotelic sensu Briggs & Johnson, 1979) as do 26 of the 32 genera in the Lythraceae (Graham et al., 2005). The polytelic inflorescences are basically racemes, i.e., simple inflorescences in which the primary axis bears lateral flowers. Flowering is acropetal. The formation of flowering shoots amon the species is exceptionally diverse due to incomplete differentiation between the flowering and vegetative branching systems (Koehne, 1884; Weberling, 1988) and the extent to which flowering lateral branches develop. Flowering lateral branches (“inflorescences” in the traditional sense) in Ginoria emerge commonly, but not consistently, at the beginning of a new season from the axillary buds on the vegetative shoot of the are brachy- flowering zone may convert to a primarily vegetative zone that bears single flowers at a few of its most nodes. Foliaceous leaves appear at later nodes of the brachyblasts, resembling the leaves of the main vegetative stem but smaller. As a new season's asts are initiated, the —— long shoot imn stem) growth of the new season gins and very often produces single flowers in the axils of the foliaceous leaves. Most flowers, however, form on brachyblasts. In the typical pattern for the genus, flowers arise: (1) on newly formed brachyblasts from buds of the previous season; (2) on brachyblasts emerging from buds in axils of stem leaves of the Annals of the Missouri Botanical Garden current season; and (3) directly as single flowers from buds in axils of stem leaves of the current season. Brachyblasts may elongate through several inter- nodes, as in Ginoria curvispina, forming racemes (botrya sensu Weberling, 1988). If the internodes are highly condensed, as in G. ginorioides, G. nudiflora, and G. rohrii, the leaves of the brachyblast are mere scales and the flowering shoot is umbelliform with both single flowers and condensed branches bearing two or more flowers arising in the same axil Brachyblasts in €. ginorioides are typically 5- to 12- flowered and form a showy, loose umbel. In G. rohrii, brachyblasts are 2- to 8-flowered and form an even looser subumbelliform inflorescence. Ginoria nudi- flora is notably multiflowered with eight to 20 flowers per umbel-like shoot. In G. americana, flowers are mostly solitary or two on a brachyblast in the axils of the vegetative long shoot; well-developed racemes are uncommon. Other species of Ginoria, Haitia, Tetra- taxis, and Crenea are variously 1- to 3(to 12)-flowered on short brachyblasts. The degree of shoot develop- ment and number of flowers produced vary continu- ously among the species of Ginoria to the extent that it is not possible to use differences in inflorescence development in phylogenetic reconstruction. Weberling (1988) suggests that the incomplete differentiation of the flowering short shoot or brachy- blast and the vegetative long shoot in Ginoria represents an evolutionary stage leading toward the type of fully differentiated system seen in Lagerstroe- mia L. In Lagerstroemia, flower formation is restricted to the brachyblasts and the long vegetative shoots are entirely vegetative. Lagerstroemia, however, has a monotelic (anthotelic sensu Briggs & Johnson, 1979) inflorescence, whereas Ginoria is polytelic, so a direct evolutionary comparison between inflorescences in Ginoria and Lagerstroemia is not possible. Timing of flowering versus leaf formation appears to be somewhat flexible in Ginoria. Most species begin flowering prior to or simultaneously with the expan- sion of the new season's leaves, mainly in February or March, and continue to flower until June or July. Exceptions may be G. callosa, G. glabra, G. jimenezii, and 6. koehneana, all of which appear to flower later, possibly from April through August. More extensive collections and observati quired to verify this pattern. Living collections of G. ginorioides in the Cienfuegos Botanical arden, Cuba, flowered in same or flower (pers. obs., 2003) but was said to flower in the area as late as June, well after leaf development. Under greenhouse cultivation, G. americana and G. rohrii were observed to flower after leaf formation. Herbari f G. rohrii collected in the wild P Flowering in G. rohrii is primarily from February to May, but flowers do appear intermittently at other times. Ginoria nudiflora began flowering in the greenhouse prior to new leaf expansion and continued to flower after leaves were fully expanded (pers. obs.). The ies has been collected in flower from March to June. Old fruits and pedicels tend to be persistent in Ginoria. Haitia buchii is known in leaf and flower from March to June and H. pulchra from February to July, approximately in the same season as Ginoria. Tetrataxis, at approximately the same latitude in the Southern Hemisphere as Ginoria and Haitia are in the Northern Hemisphere, is known to flower at least from February to May, with fruits observed in March and some pedicels and old fruits persisting into the next season as they do in Ginoria and Haitia. Crenea appears to flower and fruit throughout the year, with abundant young buds and flowers present from ca. August to November. FLORAL MORPHOLOGY Flowers of all perennial genera of the Lythraceae panthium) with valvate sepals surrounding a superior ovary (Fig. 4A). Beneath the base of the ovary, the floral cup in many of the genera is extended by an epipodium (sensu Troll, 1964; anthopodium of Briggs & Johnson, 1979), which is interpreted as the distalmost internode of the axis before the flower. The epipodium terminates basal y at a pair o bracteoles (prophylls) at the first node below the flower. In Ginoria, the epipodium varies in shape with the species, being slender and exceptionally long in G. americana (2-7.5 mm), stout in G. arborea (0.5— 1 mm), and absent in G. callosa. In most species it is slender and 1-3 mm. In the large flowers of Haitia buchii it is slender and 5-6 mm long; in the smaller flowers of H. pulchra it is stout and 1-2 mm long. The epipodium in Crenea (1.5-3 mm) and Tetrataxis (6— 12 mm) is broad and tapers gradually from the base of the ovary to the bracteoles. The bracteoles are typically thin and caducous in all the genera, but in C. callosa they are coriaceous and well developed. Flowers of all the Lythraceae are globose to subglobose or obovoid in bud, with four to six (rarely seven or more) deltate sepals. The veins or “ribs” that constitute the vascular supply to the sepals, stamens, and petals are usually visible on the floral cup and sepals. Outgrowths termed epicalyx segments (the appendages of Koehne, 1882, 1885a, 1903) develop at the sinuses of the lobes in the majority of genera of the family, although not always in all species. They Volume 97, Number 1 Graham 41 Revision of Ginoria (Lythraceae) Haitia pulchra Haitia buchii G. callosa G. americana G. ginorioides G. jimenezii G. glabra G. rohrii G. curvispina G. nudiflora G. lanceolata G. arborea G. koehneana FLOWER LENGTH (FLORAL CUP + SEFAL) |: Figure 4. Length of floral components for Ginoria species discussed in this ree —A. pee mun Ginoria flower composed of the € cup, sepals, and epicalyx node below the flower. —B. Length of flor; a n sepal; hat ch ar — range in length of the sepal. exhibit the greatest diversity of form in Ginoria and Haitia, where their shape and size are diagnostic of the species. Epicalyx segments are small, flattened, or corniform growths (GC. curvispina, Fig. 21C; G. ginor- ioides, Fig. 23B, C); enlarged pouch-like growths that are accompanied by additional ruffled tissue decur- rent on the subtendi ein (G. callosa, Fig. ; or encircling flanges as a result of the fusion of adjacent epicalyx segments (G. glabra, Fig. 25C; H. buchii, Fig. 18B; R. pulchra, Fig. 34B). They are absent in G. americana, G. arborea, G. jimenezii, G. koehneana, G. ebd G. nudiflora, and G. rohrii, and in Tetrataxis and Crene The total length of the flower cited in ee species descriptions is the sum of the measurements of the floral cup, sepals, and the epipodium. Although the epipodium developmentally is not part of the flower, it superficially appears to be part of the floral cup and is included in the total measurement for this reason. The length of the floral cup is measured from the base of the ovary to the sinus at the base of the sepal (Fig. 4A). The sepal length is measured from the sinus to the sepal apex. Total floral length in Ginoria varies “rib” or — illustrated han associa id bar bracteoles at he first and the epipodium of the sens d logi o the floral cu ed i — range in length of the floral cup ean from de m of the ovary to the sinus of the sepal; X- -pattern from shortest in G. koehneana (3—4.5 mm) to longest in G. callosa (8.5-11 mm). Flowers in Crenea are within the same size range (6-9.5 mm), are slightly longer (11-18 mm) in Haitia, and are longest in Tetrataxis (20-25 mm). Species in Ginoria vary considerably in the ratio of sepal length to floral cup length, raising the question of whether floral evolution in the genus involved an equal increase in floral cup and sepal length or whether one component increased nik over the other, approaching either a more open or a more tubular floral form. In G. arborea, G. koehneana, G. lanceolata, and G. rohrii, the floral cup is shorter than the sepals without overlap in length (Fig. 4B). These are also among the smallest flowers in the genus. In Ç. callosa, Haitia buchii, and H. pulchra, the floral cup is the longest part of the flower and the sepals are proportionally shorter without overlap in length. These are the largest flowers. In the remaining species of Ginoria, and in Tetrataxis and Crenea, the floral cup is shorter to equal the length of the sepals, and the lengths of the cup and sepals overlap. The ratio of floral cup to sepal varies from 0.2—0.5 in species in Annals of the Missouri Botanical Garden which the sepals are longer than the floral cup and 1.2-1.5 in species in which the floral cup is longer than the | obes. The evolutionary course of this LI I r. . E 3 . E 6 (see Character Evolution). The color of the mature floral cup, sepals, and/or ovary in Ginoria americana, G. callosa, G. curvispina, ginorioides, G. nudiflora, and Haitia buchii g > Flowers in Ginoria are basically 4- or 6-merous, but merosity is flexible, as it is in most other genera of the Lythraceae (Dahlgren & Thorne, 1984). Merosity as cited in the species descriptions refers to the basic condition that is exemplified by the number of sepals and petals prevalent in the species, with stamen number and ovary locular number being more variable, Occasional 5-merous flowers can be found on plants with predominantly 4-merous or 6-merous flowers. Infrequently, 7-merous flowers occur. The following species typically have 4-merous flowers: G. arborea, G. jimenezii, G. koehneana, G. lanceolata, G. nudiflora, and G. rohrii. Flowers are typically 6-merous in: G. americana, G. callosa, G. curvispina, G. ginorioides, G. glabra, Haitia buchii, and H. pulchra. Flowers of G. ginorioides can range from 5-merous to 7-merous on a single plant (pers. obs.). One specimen introduced from a wild population to the Cienfuegos Botanical Garden in Cuba produces flowers with i i number of petals and up to 55 stamens, further evidence of the floral plasticity in this genus. Flowers of Tetrataxis and Crenea are consistently 4-merous. Petals in the majority of Ginoria are large (to 20 x 15 mm in €. callosa) and showy. Petals in G. arborea and G. koehneana are exceptionally small for the genus (2-4 X 0.5-2 mm), scarcely exceeding the sepals. Clawed petals with claws to 2 mm long occur in G. americana, G. curvispina, G. ginorioides, G. glabra, 6. koehneana, and G. nudiflora. Four species have white petals: G. arborea, G. koehneana, G. nudiflora, and G. rohrii. Petal color is intense rose or rose-purple or violet-purple in the rest of Ginoria and in Haitia. White petals with purple venation can occur in H. pulchra. Petals are. absent in Tetrataxis and cream to white in Crenea. Petal length ranges from 2- 20 X 0.5-15 mm across the genera. The petals in Haitia are 12-14 X 10-14 mm, within the range of the larger-petaled species of Ginoria. Stamen numbers in Ginoria range from eight in G. lanceolata to 30 to 31 in G. a single flower. Four-merous flowers have (eight to)12 to 24(to 40) stamens and 6-merous flowers have 12 to 40(to 55) stamens. The 6-merous species, Haitia buchii, H. pulchra, and G. callosa, consistently have 24 or more stamens. The continuum of stamen numbers and plasticity of stamen production limit the use of specific stamen numbers as a reliable means of distinguishing species in Ginoria or separating Haitia inoria. Stamens in both genera are arranged in a single whorl at the distal margin of a smooth tissue layer that lines the floral cup extending from the base of the cup to the level of stamen emergence. The antesepalous stamens (inserted in front of the sepals) are solitary and only rarely proliferate, whereas the antepetalous ones as a result of chorisis appear in multiples of 2X to 6X the number of sepals (— 10 in cultivated G. ginorioides). Occasionally, a staminal filament divides after filament growth begins, produ- cing a dichotomous filament with two fully formed anthers (pers. obs. = In Tetrataxis there are four exclusively antepetalous stamens, and in Crenea typically 12 stamens occur in a single whorl, one at each antepetalous position and two at each ante- ous position. The number in Crenea can range from possibly eight (Lourteig, 1986) to 15. The position of the stamens on the floral cup varies from nearly basal, surrounding the ovary, to ca. l- 2 mm below the sinuses of the sepals at the margin of the cup. In Ginoria americana and G. curvispina, the stamens are nearly basal and an inner tissue layer is scarcely evident. In the other species of Ginoria and in Haitia and Crenea, an inner lining of tissue extends from the base of the ovary to the level of stamen emergence. This layer is glossy and apparently non- nectiferous in Ginoria and Haitia. The margin of this tissue forms a narrow, freestanding collar in G. nudiflora with the stamens emergent at its base (Fig. 6). The tissue margin is narrowly free in C. glabra, G. callosa, H. buchii, and H. pulchra; the stamens emerge along the free edge in these species. In C. callosa and H. buchii, the floral cup appears also to enlarge, forming a ring just at the base of the sepals on the inner surface. In all species except C. koehneana, the staminal filaments are long, densely packed in the bud, and long-exserted or partially curled back into the floral cup at anthesis. In C. koehneana, the stamens and petals are so short as to scarcely surpass the sepals, suggesting that the species may be self-fertilizing. Anthers in Ginoria, Haitia, and Tetrataxis are versatile, elongated, dehiscent by two longitudinal slits, and revolute. In Crenea, they are basifixed. The gynoecium in all genera consists of a superior, sessile, globose to oblong ovary that may be shallowly ed koehneana), and a small capitate to subpunctiform stigma. The stigma in Pn UE Tyler Di pw aN ree Me ke A A RUN Volume 97, Number 1 Graham Revision of Ginoria (Lythraceae) Haitia buchii G. callosa Haitia pulchra G. glabra G. ginorioides G. jimenezii G. koehneana G. curvispina G. nudiflora G. americana G. rohrii G. arborea G. lanceolata | MW 8 10 12 14 16 18 20 22 24 26 28 30 32 34 36 38 40+ RANGE IN SM NUMBERS 4-MEROUS S. GE 6-MEROUS SPECIES [_] Figure 5. G. d is wet at time of pollen receptivity (pers. obs.). Th Pleno condition at receptivity for other taxa is not know vary locules are separated by thin, pe as Nan attached to a thick, m axile placenta that is circular to triangular transverse section. A small opening is present at de Range in stamen numbers for Ginoria species discussed in this treatment. apex of each septum, so that the septa are incomplete. The taxonomic uH of Ginoria in the tri s thus in conflict with the tribal e by their ) was aware that Nesaeeae Koehn septa. Koehne (1885a: 31 Ginoria and Lagerstroemia lacked the character of igure 6. Ginoria nudiflora, interior of flower illustrating the narrow collar of tissue below the sinuses of the sepals at the level of stamen insertion (arrow); three staminal filaments visible (Gutiérrez B. 3099, MO). Scale bar = 2 mm. Annals of the Missouri Botanical Garden their tribe. Subsequent studies have shown that the septa are incomplete at the distal end of the locule v É noc du tob ¿th g as gil ¡BO the tribal division (Tobe et al., 1998). Nectaries are absent in Ginoria, Crenea (Tobe et al., 1998), and Haitia and present in Tetrataxis (Graham & Lorence, 1978). Flowers of Ginoria attract great quantities of bees for the abundant pollen they produce (pers. obs.). The fruits in Ginoria, Haitia, and Tetrataxis are dry, 2- to 6-locular capsules with septifragal dehiscence; the septa split longitudinally as the fruit matures. Carpels number three to six in 6-merous flowers and subseq they may split further. The sturdy style is retained at the apex of the placenta after capsular dehiscence. Crenea produces indehiscent capsules that split irregularly with age. SEEDS Seeds of Ginoria are minute, averaging 1.2 X 0.3 mm, and are produced in high numbers (Figs. 7, 8). Koehne erected two sections in subgenus Ginoria based primarily on differences in seed shape and thickness of the seed coat (Koehne, 1903). Seeds in section. Ginoria (= section Prismatospermum) were described as obovoid-prismatic, suboblique, retuse, and grayish white with a thick seed coat. Ginoria americana is the only representative of the section. Seeds in section. Discospermum were descri complanate and obovate-orbicular (G. curvispina), elliptic (G. glabra), or oblong-elliptic (C. ginorioides). The seeds of subgenus Antherylium Koehne were described as complanate (G. nudiflora and G. rohrii). Seed shape in Ginoria americana is not as disparate in the genus as originally described by Koehne. Although subrectangular seeds can be seen (Fig. 7A), variation includes more elongate seeds with a less rectangular-prismatic, more tapered obovate form like the seeds of G. curvispina (Fig. 7C) and G. callosa (Fig. 7D). The whitish seed color in G. americana reported by Koehne has not been observed; all seeds studied were golden brown. A major difference between seeds of G. americana and the other species is the presence in G. americana ofa thicker mesotesta co of uniformly tiny, densely packed, non- layered cells that must very effectively buoy seeds on their release into the streams where G. i grows. The seed coat of all other species is more fragile, and no dense spongy mesotesta is apparent in hand sections. Rather, the mesotesta is multilayered and the cells mostly collapse when dry. Seeds of other species are elongate and obovate, oblong-elliptic, falcate, convex abaxially and slightly concave adaxi- ally, with an obtuse to cucullate apex (Fig. 7C, D). The raphe extends the length of the concave adaxial side, terminating near the chalazal end. Seeds of G. nudiflora (Fig. 7B) and G. rohrii are exceptional, being longer, fusiform, and very fragile. Externally, the epidermal cells of the seed coat in all species are elongate, rectangular in outline, with straight to slightly undulating walls. Seeds of Haitia (Fig. 8) and Tetrataxis possess the same morphology as the typical Ginoria seed (Fig. 7C, ; Tetrataxis seed, fig. 2A in Graham & Lorence, 1978). Seeds of Tetrataxis are ca. 1 X 0.3 mm and virtually identical to those in H. pulchra. Seeds of Crenea are oblong, narrowly elongate, and slightly ` faleate but differ from those in Ginoria by the production of a large-celled float tissue on the adaxial surface and by their greater size at ca. 2.5 X 0.5 mm. Anatomically, th d tin Ginori lops from lanare or itagia (testa) and a bilay inner integument (tegmen). The innermost testal layer is sclerotic, and the exotegmen consists of small, more elongate, thick-walled tracheoids. This pattern agrees with the general pattern found in the Lythraceae (Corner, 1976: 176-177; Graham, 1995). The seeds of some Lythraceae, however, display a feature unique to all angiosperms, i.e., internally formed epidermal trichomes that evert from the cell upon wetting. These occur in 17 of the 32 genera, including Ginoria (verified in G. glabra, G. nudiflora, G. rohrii), Crenea, aitia pulchra, and Tetrataxis. The trichomes are simple, straight (as opposed to spiralled in some other genera), unornamented extensions 55—62 X ca. 8 um (Fig. 8A, B). The anatomy of Ginoria seeds has not been fully explored and could yield further information of phylogenetic and taxonomic value. The seeds of the Lythraceae produce oil in the embryo. The composition of the oil varies among the genera, with the majority of genera emphasizing linoleic acid (C18:2) as the primary fatty acid and palmitic acid (C16:0) as the secondary component ( ` os ly. Based ra, the seed oil is 65% C18:2 and 19% C16:0. The same pattern occurs in Tetrataxis; seed oils in Haitia and Crenea have not been analyzed. POLLEN MORPHOLOGY Pollen of Ginoria has been described and compared to putative relatives as part of a series of studies on pollen of the Lythraceae (Graham et al., 1985). It varies from slightly prolate to prolate-spheroidal and circular in cross section, and is tricolporate and heterocolpate (Fig. 9A, B). There are three equidis- giga e: kerap Sit asa atya = 45 A, C, D = 500 um; 42, US). —B. G. nudiflora 7 a a LY SMS e o n r ee A TA Lupe mI RN me M EB e disi 0, MO). Scale bars: 4 callosa (Ekman 48 Revision of Ginoria (Lythraceae) Graham 5, NY). —D. C. A LP zx: ZZ ca 4 v) 4 MA ^ i x m. Z PUT s < d x” j^ “ X — 7. dh. Wright 254 ( G. curvispina SEM micrographs of Ginoria seeds. —A. G. americana var. americana (Britton 6 $ Q E A aa n z e) * + N c o Mg 5° s Š — =r ba Il oo Gu. >N = = Annals of the Missouri Botanical Garden igure 8. Two individual seed trichomes. Scale bars: A — um; B = tant functional colpi and six shorter pseudocolpi, which are arranged in pairs between the functional colpi. Germination pores are circular and situated at e midpoint of each colpus. The pollen wall varies in thickness from 1.5-2.5 um, and exine sculpture varies Irom nearly psilate to distinctly scabrate. Grains are Seed of Haitia pulchra (Ginoria "e 2 —A. Wetted seed, a (raphal) view, trichomes extended. —B. 1923 (S). 30 um. A, B from Ekman s.n. in within the average size range for genera of the Lythraceae at 23-39 um polar diameter X 23-29 um equatorial diameter. Pollen characters do not vary sufficiently among the species to be significant taxonomically. The pollen of Haitia buchii and H. pulchra is indistinguishable from Ginoria except that Figure 9. Pollen en of Ginoria ginorioi des. —A - Photo by Joan Nowicke f from Ekman 18£ E campo view. —B. Polar view. 4 (US Arrows mark pseudocolpi. Scale bars: A, | | NN T YT LET I EN QR P INS VA T EC Volume 97, Number 1 Graham Revision of Ginoria (Lythraceae) the pollen wall is slightly thicker (Graham et al., 1987). The presence of six pollen pseudocolpi occurs in approximately one third of the genera of the d Ammannia, Crenea, Ginoria, Haitia, nthera A. Fern. & Diniz, Lafoensia Vand., ha eee Lawsonia, Nesaea, Pemphis J. R. Forst. G. Forst., and Rotala L. Pollen of Crenea differs from the other members of the 6-pseudocolpate group by its verrucate exine and by absence of margins (costae S along the colpi (Graham et al., 1985). The pollen etrataxis differs conspicuously from Ginoria e and that of other putative close relatives by lack of pseudocolpi, presence of promi- nent mesocolpal ridges, conspicuous apertural fields, and a psilate exine (Graham et al., js CHROMOSOME NUMBERS The basic chromosome number for the Lythraceae is — a number held by at least eight of the genera (Graham & Cavalcanti, 2001). Ginoria is a paleopo- lyploid with x — 28. Ginoria, Tetrataxis (x — 28), and Crenea (x — 32) have the highest basic numbers in the amily. chromosome number in Haitia is unknown. Within Ginoria the chromosome number is constant for the three species counted to date. Ginoria na var. americana (count published as C. Vitel G. nudiflora, and G. rohrii have 2n = 56 obe et al., 1986; Graham & a 2001). The constancy in chromosome number in early-diverging (G. nudiflora) and derived (G. inte and C. rohrii) species following phylogenetic hypotheses of this study suggests that ancestral Ginoria was a high polyploid prior to radiation in the Caribbean and that ioca was not accomplished through changes in number, as in some other genera of the family (Cr pi & Cavalcanti, 2001). Speciation in Ginoria most likely involved changes at the allelic level or chro al rearrangements rather than Jm or aneuploid events. A similar constancy in some number in the family is seen in the HR woody genus Diplusodon Pohl and is in contrast to the condition in the herbaceous genera Ammannia, Cuphea P. Browne, Lythrum L., and Rotala, where a wide array of aneuploid numbers and polyploid levels occurs. REPRODUCTIVE BIOLOGY Most species of Ginoria and Haitia initiate flower- ing in February or March, but flowering can commence as early as January or as late as June, depending on local or seasonal conditions or the species. The limited collection data available suggest that G. callosa, G. glabra, G. koehneana, and G. jimenezii flower from June to August. Flowers appear before the new leaves of the season, with the leaves, or after new leaf production. The appearance of flowers prior to new leaves does not seem to be a fixed species characteristic but is influenced by local conditions, possibly by the availability of water. - Phenological data reported here are gleaned primarily from exsiccata labels Pm pa: ne field observations siii and determine the lic of D to flowering time. inoria i be outcrossed as judged by the long style and exserted stamens. No data are available on reproduction for Crenea, Haitia, or Tetrataxis, dE. all havo dile exserted styles and stamens, Trees of G. nudiflora in n Museo attract great maet of bees for the abundant pollen produced during the brief weeks of flowering, and honey bees and euglossid bees have been observed on the flowers of G. americana in Cuba (pasa. mad The Sven of Ginoria are nectarless and observations of G. americana, G. curvis pe, 6. sinet G. nudiflora, me G. rohrii. Single plants of G. americana, G. nudiflora, and G. rohrii a iow mone neously) in a greenhouse accessible no seed, suggesting that they are till or have a low degree of self pollination. Most genera of the Lythraceae are self-compatible but require pollinators for pollen transfer (pers. obs.). No speci- mens of suspected hybrid origin have been noted in collections of the Cuban species of Ginoria. 1 have collect . americana and G. ginorioides within a meter of one another in Villa Clara, and C. curvispina and G. koehneana separated by a few hundred meters in coastal Las Tunas Province. In each case, only one species was in flower. Although the flowering periods among Gi species appear to show considerable overlap, actual number of days of flowering and stigma receptivity may be short. Ginoria americana flowers throughout much of the year. Trees of C. ginorioides at the Cienfuegos Botanical Garden, Cuba, display flowers with petals for only one week of the season (H. Garcia, pers. obs., 2003). The dry floral cups and dehisced capsules of the previous season frequently persist on strongly attached pedicels in Ginoria after flowers of a new season appear. HABITAT AND DISTRIBUTION All but two species of Ginoria are restricted to the Greater Antilles, where they are part of the extensive endemic flora of the islands of Cuba and Hispaniola (Santiago-Valentin & Olmstead, 2004; Appendix 3). Annals of the Missouri Botanical Garden The two exceptions are G. nudiflora, endemic to southern Mexico, and G. rohrii, whose range extends from the dry coastal forests of Puerto Rico eastward to the Virgin Islands. Six species are endemic to Cuba: G. americana, G. arborea, G. curvispina, G. ginor- ioides, G. glabra, and G. koehneana. Three species, G. callosa, G. jimenezii, and G. lanceolata, together with Haitia buchii and H. pulchra, are endemic to Hispaniola. Species of Ginoria are typically members of dry submontane forests or coastal thickets with a propensity for serpentine and calcium-based soils. No Ginoria or Haitia occur in Jamaica, although there are extensive karst habitats similar to those in Cuba and Haiti occupied by these genera. In Cuba, Ginoria is found in all three phytogeo- graphical provinces, Western, Central, and Eastern (Borhidi, 1996). Ginoria americana and G. ginorioides are the most widespread on the island, occurring in the three phytogeographic provinces, with G. amer- icana var. americana the most commonly occurring taxon. Because G. americana grows in a riverine habitat, it is not constrained by the same edaphic an climatic limitations that are imposed on other members of the genus in dry forests or on limestone. Ginoria ginori a on limestone in the Trinidad Mountains. Ginoria curvispina is common in the eastern part of the Central Province as a species of the isolated Las Villas, Camagüey, and Holguín serpentines in dry scrub woodlands and Overgrazed savanna and also on limestone in these areas. Disjunct populations at the extreme western end of Cuba in southern Pinar del Río grow on sandy soils. : spinosa has a limited distribution within the range of the nominal variety in Central Province in the same serpentine savannas and serubland as Ç. curvispina. Ginoria koehneana is another facultative serpentine species with three highly disjunct populations along the northern coast of Cuba. Those in the Western coast near Puerto Padre, also inland from th mangroves, on limestone. À single collection mad in 1916 is known from the Eastern Province growing in ferruginous soil on limestone in a dry forest. Two species, G. arborea and €. glabra, e e sympatric distributions on the southern coast in the Eastern Province, an area renowned for its rich, highly endemic, xeromorphic flora (Borhidi, 1996). The species grow in coastal thickets on limestone terraces and inland on slopes in dry forest. In Hispaniola, Haitia buchii and Ginoria jimenezii are dry woodland species on limestone, occurring in areas similar to those of G. ginorioides in Cuba. Distribution of H. buchii follows the principal mountain ranges of the island whose east-west axis extends from the Massif de la Hotte in Haiti into the Cordillera Central in the Dominican Republic. Ginoria jimenezii is isolated from H. buchii, occurring north of the Cordillera Central in the Dominican Republic in the Cibao Valley and north across the Cordillera Septentrional in dry forest close to the northern coast. Ginoria callosa, G. lanceolata, and H. pulchra are narrow endemics restricted to the coastal limestone cliffs and terraces of northern coastal Haiti, in habitats like those occupied by G. arborea and G. glabra in southeastern Cuba. At the eastern end of the range of Ginoria in Puerto Rico and islands to the east, the sclerophyllous G. rohrii grows in coastal forest and thorny thickets over limestone, habitats like those occupied by Ginoria in Cuba and Hispaniola. The species is occasionally also found in low coast woodlands flooded with brackish water. At the western limits of Ginoria, the large tree species G. nudiflora is an endemic riverine and low coastal forest species in southern Mexico, distributed from coastal beach thickets in Veracruz into low montane forests in Oaxaca and Chiapas. It is also found disjunctly in dry coastal hills bordering the Pacific Ocean in western Michoacan, Mexico, there possibly through accidental introduction (Fig. 33). PHYLOGENY The phylogenetic position of Ginoria within the Lythraceae and the phylogeny of the genus itself have n partially explored in two earlier publications. In a family-level study with nuclear ribosomal DNA (rDNA) ITS (ITS-1, 5.88 gene, ITS-2; Graham et al., sequences, G. americana was included as the single exemplar of the genus. Ginoria + Tetrataxis Volume 97, Number 1 Graham 49 Revision of Ginoria (Lythraceae) T . ITS GenBan molecular phylogenetic analysis of this study. k accession numbers and vouchers for new molecular sequences in Ginoria employed in the GenBank Species Origin Voucher accession number Ginoria americana (1) Cuba Graham 1137 (HAC) 407 G. americana (2 Cuba, cult. Fairchild Tropical Garden as G. glabra — FG-1753C (FTG) AY078420 G. cu Cu aham 1139 (HAC) EF407950 C. ji i Dominican Republic Garcia 3614 (MO) AY078422 G. koehneana Cuba Graham 1142 (HAC) EF407951 G. nudiflora Mexico Gutiérrez 3098 (MO) AY078418 G. rohrii Puerto Rico, Vieques Island Proctor 48846 (MO) AY078419 Although a full molecular phylogenetic investigation of E genus is not possible at this time due to the and/or EL of DNA for five endemic species of Gino. d the species of Crene Haitia, a new aa cladistic analysis of F data includes six species of Ginoria. A new morphological cladistic — is also presented with character selection and coding modified (Appendices 4, 5) from the earlier amo (Graham, 2002). MATERIALS AND METHODS Molecular investigation. Fresh or silica gel-dried leaves of Tetrataxis salicifolia (Thouars ex Tul.) Baker and six species of Ginoria were used as a source of DNA to study sequence variation in nuclear rDNA ITS (18S rRNA, ITS-1, 5.885 gene partial ITS-2). The sequences obtained were added to those presently available for 27 genera of the Lythraceae to (1) further test the I of Ginoria that was recovered earlier ne (Graham et al., 2005) and (2) initiate exploration of phylogenetic relationships in the us. GenBank accession numbers and uchers fi w sequences are listed in Table 1. Ruso published molecular accessions utilized in this study are detailed in Graham . (2005). Extraction procedures on 1 g a inco per sample followed Doyle and Doyle (1987) as modified by the use of 6X CTAB to A problematic polysacchar- ides (Smith et al., 1991). The ITS region was amplified by using primers 5 and š of White et al. (1990). Amplification reactions were performed as in Freud- enstein (1999) except that the buffer contained 100 mM Tris-HCl (pH 9.2), 30 mM MgCl», 250 mM KCl, and 5% ees sulfoxide (DMSO). Sequencing reactions used the BigDye kit from Applied Biosys- tems (Foster e "Cien U.S.A.) according to the manufacturer's instructions and were run on an ABI Model 377 sequencer (Applied Biosystems). The exceptions were G. koehneana and Tetrataxis, whose sequences were produced at Macrogen Inc. (Seoul, South Korea). Contiguous sequences were assembled with Sequencher (Gene Codes Corporation, Inc., Ann — Michigan, U.S.A.), aligned in Clustal X, and anually adjusted in MacClade 4.07 (Maddison & Maddison, 2000). Atte A from herbarium materials of the putatively in related genera Haitia and Crenea and from mpts to extract amplifiable silica gel-dried leaves of G. ginorioides were unsuccessful after repeated attempts. Morphological investigation. A data matrix of 19 taxa and 14 cue Pup bn was ne with k SCVUII Didi y usc ina morphological ladisti lvsis as 5 J lationships in Gi. i A dude data Ww was acid in the oa Two characters are vegetative and 12 are reproductive. The total number of characters was limited by close similarity among the i ood a leaf and pollen morphology and by a continuum in size, shape, and number of vegetative and floral components. Three quantitative floral characters (characters 4, 5, and 9), whose states are separated by numerical gaps, were included in the matrix. The floral characters of the rare G. lanceolata, previously known only from sterile material, were included in an analysis for the first time through discovery of a flower among material of a second collection. natomy, um parsimony analyses the RIMIS data sets were analyzed separately by using PAUP* version 4.0b10 (Swofford, 2002). For ITS analyses, Combretum Loefl. and Quisqualis L. in the Combretaceae and Ludwigia L. and Fuchsia L. in the Onagraceae were employed as outgroups. These two families are regarded as closest relatives to the Lythraceae (Graham et al., 2005). To test the monophyly of Ginoria in the morphologically based cladistic analysis, Crenea, Ginoria, Haitia, and Phylogenetic analyse of the ITS and Annals of the Missouri Botanical Garden Tetrataxis were included in the ingroup. The outgroup consisted of Ammannia, Decodon J. F. Gmel., Lagerstroemia, Lawsonia, and Nesaea. Decodon and Lagerstroemia represent more distant relatives in the family. All characters were unordered and equally weighted. All analyses were performed to completion by using a heuristic search and the following settings: 10,000 random taxa addition replications with 10 trees held at each step, tree bisection-reconnection (TBR) swapping and MULTREES option in effect, and branches set to collapse if minimum branch length is zero (*amb-"). Evaluation of clade robustness used bootstrap analysis with 100 replicates, 250 random addition replicates, no more than two trees saved for each stepwise addition, TBR swapping, and MULTREES in effect. RESULTS AND DISCUSSION The family-level ITS parsimony analysis including six species of Cinoria produced a single tree of length 2510, consisteney index (CI) — 0.43, and retention index (RI) — 0.63 (Fig. 10). The aligned length of the region was 714 characters, of which 443 (62%) were parsimony informative. All species of Ginoria are included in a strongly supported clade (96% BS) with Lawsonia at the base of the clade and Ammannia + Nesaea sister to Ginoria. The clade is one of the most strongly supported in the family as is its sister clade Duabanga Buch.-Ham.-Sonneratia L. f. (95% BS); in contrast, there is weak or n pport at t of the other deep nodes of the family phylogeny (Fig. 10). With the addition of five species of Ginoria to the new ITS cladistic analyses, Ginoria is shown to be paraphyletic. Ginoria jimenezii is sister to the rest of Ginoria, and Tetrataxis is included within Ginoria at the node above G. jimenezii. Bootstrap support for the clade Tetrataxis + G. nudiflora—G. curvispina is 78%. Ginoria amer- ican ea e RAE °p. Seb E I position genus. The terminal branches are long to 6. Jimenezii (27 changes), G. nudiflora (28 changes), and especially to Tetrataxis (45 changes). whereas only zero to nine changes appear on the subterminal and terminal branches of the derived clade G. rohrii-G. curvispina. Parsimony analysis of the morphological data set for this revision yielded 22 minimum-length trees of length 33 (CI = 0.67, RI = 0.78), and the strict consensus was highly unresolved (Fig. 11). One weakly supported unresolved clade (60% BS) eonsists of Ginoria arborea, G. koehneana, G. lanceolata, an C. rohrii. A second, more strongly supported clade (88% BS) consists of two species of Ginoria and two species of Haitia. Again, Ginoria is paraphyletic, with part of the genus forming a clade with Haitia. The a relationships of Ginoria to Tetrataxis and Crenea, the latter another possible congener, were unresolved in this morphologically based phylogeny. Ginoria is well supported (96% BS) in the ITS phylogeny of the Lythraceae as a member of the Afro- Asian clade composed of Lawsonia, Ammannia + Nesaea, and Ginoria + Tetrataxis, but the sister to Ginoria remains equivocally Lawsonia or Ammannia + Nesaea (the latter two genera most likely congeneric, Graham et al., 2005). ITS results further support the hypothesis that Ginoria is monophyletic only when Tetrataxis is included, whereas morphological results find Ginoria monophyletic only when Haitia is included. An independent test of these hypotheses employing all relevant taxa, including Crenea, is critical to fully understand the limits of Ginoria and its relationships to those genera with similar morpho- logical forms. The extensive changes in ITS that have accumulated with time in G. jimenezii, G. nudiflora, and Tetrataxis following divergence from a common ancestor taxa imply that they are considerably older an the numerous island-endemic species of Cuba and Hispaniola whose ITS sequences are closely similar to one another. The close ITS similarity of G. rohrii, G. koehneana, G. americana, and G. curvispina suggests their speciation in the Greater Antilles is relatively recent. The Puerto Rican species G. rohrii, which shares clade membership with the Cuban endemics in both molecular and morphological analyses, is not a close relative of G. jimenezii from the Dominican Republic, as might have been implied by their 4-merous, epicalyx-free floral morphology and close geographical affinity. In one of the two clades generated in the morphological analysis, two species of western-central Hispaniola (Haitia buchii and H. pulchra) occur with Ginoria glabra of southeasternmost Cuba and C. callosa of northwestern Haiti. Their relationship is supported by shared derived 6-merous flowers with rose-purple petals and a well-developed epicalyx. In the second clade, flowers are 4-merous, exceptionally small for the genus, lack an epicalyx, and have white petals (petal color unknown in G. lanceolata). All occur in eastern Cuba or Hispaniola. The range of C. koehneana also includes sites on the northwestern coast of Cuba. CHARACTER EVOLUTION Exploration of character change is limited by the underrepresentation of species of Ginoria in the molecular data set and by lack of a well-resolved phylogeny based on morphology. Some ancestral states of the genus can be interpreted, however, based on outgroup versus ingroup changes mapped onto the Volume 97, Number 1 2010 Graham 51 Revision of Ginoria (Lythraceae) Figure 10. A phylogeny of the Lythraceae based on salicifolia. i ITS sequences, including six species of Ginoria and Tetrataxis The one most parsimonious tree found: tree length — 2510, CI — 0.43, RI — 0.63. Superscript numbers indicate different collections of the same species. Bootstrap support values equal to or greater than 50% appear above the branches and L branch lengths appear below. ITS phylogeny. The earliest members of the genus were spineless shrubs or small trees with 4-merous flowers lacking an epicalyx. The ancestral flower had a floral cup approximately equal in length to the both toward longe perigynous cups with short sepals and toward reduced sepals. Divergence occurred - floral cups with long sepals. Stamens numbered between 12 and 18 and were inserted above the base of the floral cup, and the pollen had pseudocolpi. The three earliest-diverging species in this study, C. jimenezit, Tetrataxis salicifolia, and G. nudiflora, present these plesiomorphic features. Aside from the 52 Annals of the Missouri Botanical Garden Morphologically based phylogeny of Ginoria and Ha 11. Lawsonia, and Tetrataxis ; I = 0.78. Bootstrap ITS phylogeny, G. glabra and the species of Haitia have a prominent encircling epicalyx, which together with their 6-merous flowers and multiplicity of stamens promotes their clade relationship in the morphological phylogeny. Fruits changed from in- dehiscent or irregularly dehiscent capsules to dehis- cent capsules with thinner-coated, more elongate, less compressed seeds. Seeds in Ammannia/Nesaea, Cre- nea, Ginoria, Haitia, and Tetrataxis have simple internal epidermal trichomes and lack the densely packed homogenous spongy tissue found in trichome- less seeds of Lawsonia s the outgroup. The strict consensus of the 22 support values equal to or greater than 50% appear above the branche Ammannia Decodon Lagerstroemia Crenea Lawsonia Tetrataxis Ginoria jimenezii Ginoria nudiflora Ginoria americana Ginoria curvispina Ginoria ginorioides Ginoria rohrii Ginoria koehneana Ginoria lanceolata Ginoria arborea Ginoria callosa Haitia pulchra Ginoria glabra Haitia buchii itia using Ammannia, Crenea, Decodon, Lagerstroemia, most parsimonious trees: tree length = 33, CI = 0.67 BIOGEOGRAPHY first attempt to understand the historical biogeography of Ginoria from a phylogenetic perspec- tive was limited to results from a morphological phylogenetic study (Graham, 2002); it placed G. rohrii from Puerto Rico as the first-diverging lineage of the genus. Several biogeographical scenarios were ex- plored and it was ultimately concluded that (1) morphological characters were inadequate for basal resolution of the genus with confidence; (2) long- distance dispersal and random chance establishment Volume 97, Number 1 2010 Graham Revision of Ginoria (Lythraceae) played a major role in the evolution of the genus; and (3) radiation within Ginoria was multidirectional, both east to west s west pa une. The ITS i li, a narrow endemic of central ipani as the fivat-diverging lineage of the genus. At successive grades above G. jimenezii are Tetrataxis from Mauritius and then C. nudiflora from Mexico. One hypothesis to explain this wide disjunction is that ancestral Ginoria stock originated in eastern Afro-Asia where Lawsonia and Ammannia/Nesaea occur today. The ancestral stock then dispersed over a long period of time and over great distances in both easterly and westerly directions. No fossils of Ginoria-like plants have been reported anywhere in the world to test this hypothesis. However, fossils of Lawsonia-like seeds of British Columbia indicate existence of the clade in North America by 48.7 million years ago (Cevallos- Ferriz & Stockey, 1988; Little et al., 2004). Koehne essentially posed this — peii 1885b: 34), e that a “Gino ginated in north- astern Asia, subsequently weite in one direction n America and in another southwestward into India, where it gave rise to Tetrataxis, which then spread from India to Mauritius. How and when Ginoria or its ancestral form first arrived in the Caribbean or how more recent radiation and speciation proceeded in the Greater Antilles remain speculative in the absence of fossil evidence and a full phylogeny. Radiation of the genus in the Caribbean was clearly multidirectional, and long-distance wind and/or water dispersal and chance establishment played major roles in its evolu- tion. The phylogenetic ae of the South American genus Crenea, when determined, will also affect the ultimate interpretation of dee historical biogeography of Ginoria and relatives. An interesting dispersal story remains to be discovered to explain the wide inter- continental relationships of Ginoria and its relatives. Within Ginoria, some phytogeographic patterns of relationship accord with those found in the few other studies of plant groups in the Caribbean for which phylogenetic reconstructions are available (Santiago- Valentin & Olmstead, 2004). Zona (1990) in Sabal Adans., and Lavin (1993) in Poitea Vent. and related genera found sister ao between Mexican and Cuban species. Fritsch (2001, 2003) found the Hispaniolan Styrax ochraceus Urb. sister to S. radia P. W. Fritsch from southern Mexico and S. ai Griseb. from Cuba and Hispaniola sister to the endemic Puerto Rican S. portoricensis Krug & In Ginoria, Mexican-Greater Antillean relationships are seen with G. nudiflora from southern Mexico, G. koehneana from the north coast of Cuba, and C. rohrii from Puerto Rico and the Virgin Islands. Judd (2001) in Lyonia Nutt., and Lavin (1993) in Poitea found from the middle Eocene close relationships between species of eastern Cuba and north-central Hispaniola. Similar relationships are found between G. glabra in southeastern Cuba and G. callosa, Haiti buchii, and H. pulchra in western Hispaniola. Ginoria is absent from Jamaica and the i Antilles. Judd (2001) suggested the absence of Lyonia from the Lesser Antilles was because the genus had dispersed from Mexico/eastern North America and presumably had not had time to disperse as far east as the Lesser Antilles. For Ginoria, I suggest that the prevailing northeast trade wind pattern and the North Equatorial Current, both of which direct wind and water currents from Africa and from South America westward away from the Lesser Antilles and Jamaica toward Cuba (Hedges, 2001), have prevented or limited dispersal of fragile Ginoria seeds to the south and southeast. The length of time suitable habitats have been available for colonization may also be a limiting factor. The oldest, presently emergent lands in Jamaica are young at ca. 10 million years (end of the Miocene) in comparison with parts of Cuba and Hispaniola, where emergent land has been continuously available since about 40 million years ago (Middle Eocene; A. Graham, 2003a, b). Emergent islands in the Lesser Antilles are of various ages since continuous emergence, some possibly quite young (e.g., Barbados, 1 million years, fide Speed & Keller, 1993). Only a few species of the Lythraceae have managed to become established in the Lesser Antilles, and these are adventive herbs from South America or their derivatives (Graham, 1989, 2003). A similar distributional pattern is also noted in Styrax (Fritsch, ; pers. comm.). RATIONALE FOR TAXONOMIC CHANGES AT THE GENERIC AND SUBGENERIC LEVELS The phylogeny generated from cladistic analysis of ITS sequence data places Tetrataxis within the Ginoria lineage; ITS sequences for Haitia and Crenea are missing (Fig. 10). Morphologically based analysis nests Haitia within Ginoria but leaves the A to Tetrataxis and Crenea unresolved (Fig. only complete comparative analysis is e eiut thus, taxonomic changes are limited to those results that position Haitia within Ginoria. The relationships of Tetrataxis and Crenea to Ginoria remain to res E of Haitia depended on recogni- tion of several character states as unique to the genus. These were the presence of the epicalyx flange, the greater number of stamens, a 6-locular rather than 2- to 5-locular ovary, and a slightly larger stigma. The same continuous epicalyx flange present in H. buchii and H. pulchra is, in fact, present in Ginoria glabra. The Annals of the Missouri Botanical Garden highest number of stamens reported in either genus ranges from 34 to 40 in H. buchii (Fig. 5), but nearly as many occur in Ç. callosa (30 to 31), G. glabra (28), and H. pulchra (24 to 21). Stamen number does not separate the two genera, and the common occurrence of stamen idee: E Poe itin that stamen numbers are too lly significant at the genus level. The same may be said for locule number, which varies within species of Ginoria and could well vary by one or more locules in Haitia were more flowers available for examination. The difference in "imam size is not Fibre deii e in larger- regardless of the penas. There is no difference between iii and Haitia in pollen and seed morphology. anatomy does differ in some respects, but none of the species of Ginoria that are morphologically close to Haitia have been compared to Haitia, and regardless, wood anatomical characters in the Lythraceae are of a ized nature within the order and highly homoplastic (Baas & Zweypfenning, 1979). An in- dependent test of relationships employing molecular Sequences is desirable, but attempts to obtain DNA from the limited number of exsiccatae of Haitia have been unsuccessful. king any autapomorphic character to exclu- sively define Haitia and separate it from Ginoria, Haitia is subsumed within Ginoria and treated as its synonym from here on in this revision. Tetrataxis is retained for the present as distinct from Ginoria despite the partial ITS phylogeny that places it within Ginoria. Unlike Haitia, Tetrataxis has accumulated ny autapomorphic moi Ginoria and Tetrataxis primarily by basifixed anthers and float tissue in the seed. I defer possible synonymization of Tetrataxis and Crenea with Ginoria until relationships are better informed by more extensive molecular data, including that of Crenea and additional species of Ginoria. he subgeneric and sectional classification of Ginoria (Appendix 1; Koehne, 1903) was a time when only six species erected at s were known and without the strength of a suite of definitive features. The single distinction between subgenus Ginoria and subgenus Antherylium is 6-merous versus 4-merous flowers. It is not clear at this stage in our knowledge how many times the ancestral 4-merous floral form in the evolution of the genus may have given rise to the 6- me form or whether there were su ent reversals. No other morphological characters appear in combination with floral merosity to support the recognition of two subgenera. The division of subgenus Ginoria (subgenus Euginoria) into section Ginoria (section Primatospermum ) and section Dis- cospermum based on seed characters and stamen number is also unsupportable. Seed shapes in G. ber of section Ginoria, are more variable than Koehne knew. They range into the more complanate seed type seen in G. curvispina in section Discospermum, although some indeed are 4- angled and have a thicker seed coat. Stamen number is not valid either, being extremely plastic in most species (Fig. 5). The infrageneric classification of Koehne is not maintained in this revision. americana, the sole mem THREATS TO EXTINCTION The species of Ginoria endemic to Cuba and Hispaniola are under greatest threat. In Cuba, three species are particularly at risk. Ginoria arborea, G. glabra, and G. koehneana occupy specialized narrow habitats on coastal limestone and serpentine, and each is known from few localities. Their rarity is attested to by the few collections available, even though the areas have been studied floristically in recent years. Southeastern Cuba in particular has received special attention. because of the high numbers of endemic genera and species present there (Borhidi, 1996). On the beautiful northeastern coast at Puerto Padre, the Cuban government has built a hotel complex next to one of the few known localities for G. koehneana. More extensive development of the Cuban oasts for tourism is likely and threatens these exceptional habitats inoria species endemic to Hispaniola must be considered under extreme threat, if they are not already extinct. In Haiti, environmental destruction is well known; forests that once covered 93% of the land are now reduced to less than 2% (Brown, 2006). The forest-associated species G. callosa, G. lanceolata, and G. pulchra (Ekman & O. C. Schmidt) S. A Graham are known from just eight collections. Ginoria callosa has not been re-collected since its discovery by Erik Ekman in 1925. Ginoria lanceolata is known only from the two collections made by Ekman in 1925 and 1928. Ginoria pulchra is represented by three collections: the Ekman type from 1927, an Ekman collection from 1929, and a collection by Tom Zanoni in 1985, all from the type area where it is now exceedingly rare or possibly extinct (see further notes following the species description of G. pulchra). The sites of all three species are on the extreme northwest coast of Hispaniola, which, together with the eastern Cuban Pa province, has been called “the most prominent centre of speciation in the Antilles” P een 1996). Ginoria buchii (Urb.) S. A. Graham, with a range extending across the border i and the Dominican Republic, is E rare today, known from four collections, and has no Volume 97, Number 1 2010 Graham 55 Revision of Ginoria (Lythraceae) been seen since 1969. Searches for it since 1969 at former sites in the Dominican Republic have not been successful (for further details, see notes following the species description). In the Dominican Republic, G. jimenezii was considered “very rare” when originally described in 1954. It is known from the type and three additional collections, two of which are from a single sterile tree (R. G. García, pers. comm.). IUCN RebD Lisr ASSESSMENTS As is apparent from the limited distributional ranges and sparsity of collections, some species Ginoria might be extinct, and most of the remainder are at high risk of extinction. There are three exceptions: Ginoria americana var. americana with numerous populations throughout Cuba; G. curvispina, more localized in Cuba than G. americana but common within its range; and G. nudiflora, estab- lished in numerous localities in southern Mexico. Given the uncertain future protection of their habitats, the three are estimated as Near Threatened (NT) according to IUCN Red List criteria (IUCN, 2001). The distributions of G. ginorioides and G. rohrii are more fragmented with fewer populations. They are estimated as Vulnerable (VU). Endemic species of Cuba with narrow ranges and few known populations, i.e., G. americana var. spinosa, G. arborea, G. glabra, and G. koehneana are Endangered (EN). They could easily become critically endangered or extinct, especially if the coastal areas and the Sierra Maestra are developed for tourism without regard for their presence. The five species endemic to Hispaniola, i.e., G. buchii, G. callosa, G. jimenezii, G. lanceolata and G. pulchra, are Critically Endangered (CR). * NOMENCLATURE Ginoria has an unfortunate history regarding disposition of holotypes. T original ape hein used to describe the g ated, and it is unlikely to exist when one considers that few collections by him from the West Indies have survived (D'Arcy, 1970; Stafleu, 1971). Subsequently, two historical circumstances in the 1900s have necessi- tated designation of lectotypes or neotypes for 12 of the 22 names treated in this revision. In the first instance, names authored by three botanists working at the Berlin Botanic Garden (B), Ignatz Urban, O. C. Schmidt, and Emil Koehne, were based on collections at B that are no longer extant. A possible exception was the material studied by Schmidt and said to be still largely intact in B (Stafleu & Cowan, 1985: 259). None of the Ginoria holotypes designated by him, however, are present there today (C. Oberprieler, pers. m.). Secondly, the names proposed by August Crisebech (GOET) for new species collected by Charles Wright in Cuba present special difficulties because Wright’s collections were sorted according to a number assigned by Asa Gray to each species rather than by individual field collection numbers (Graham, 2005). Specimens bearing the same species number were collected at different times and in different places, their labels often lack specific collection data, and plants sharing the same species number some- times represent more than one species. complications associated with the Wright collections were investigated by Howard (1988), who selected lectotypes for many of Grisebach’s species. Because these were presented in microfiche form, they were not effectively published (McNeill et al., 2006 Art. 7.10 and 29.1), and it was therefore necessary to revisit the specimens and the nomenclatural choices mede and newly designate loctotypes (ustam, SUBE Grisebach names are cited with two wishes, The Wright number, i.e., the number cited by Grisebach in the protologue, is the species number assigned by Asa Gray to all collections of the same species on receipt of determinations from Grisebach. The number in par- entheses after the Wright number is a preliminary number that was assigned by Gray to a specimen prior to sending it to Grisebach. I have treated all specimens with the same Wright number as isotypes or as isolectotypes, although, strictly speaking, they may not have been collected on the same day, in the same year, or even in the same place as the lectotype. Taxonomic TREATMENT . 1760. Ginoria subg. Ginoria] sect. Ginoria Jacq., Enum. Syst. Pl. 5 Euginoria Koehne [= subg. Prismatospermum Koehne [= sect. Ginorial, oo (Engler) IV. 216: 248. 1903. TYPE: oe Rohr & Vahl, Skr. ne -Selsk. 2(1): 211, Ginoria su tab. 8. 17 su herylium (Rohr) e, Bot. Jahrb. Syst. 3 351. 1882. TYPE: Antherylium rohrii Vahl (= Ginoria rohrii (Vahl) Koehne). Ginoria subg. Koehne [= subg. Ginoria] sect. Euginoria Discospermum Koehne, Pflanzenr. (Engler) IV. 216: 247. 1903. TYPE: Ginoria curvispina Koehne [type of the section designated here from — the three species originally classified in the section]. Haitia Urb., Feddes Repert. Spec. Nov. Regni Veg. 16: 140. 1919. TYPE: Haitia buchii Urb. (= Ginoria buchii (Urb.) S. A. Graham). Deciduous subshrubs to tall trees, bark red-brown or red-purple on young growth, gray-brown and corticat- ing in thin fibrous strips on old growth; stems glabrous or rarely lightly puberulent, terminal vegetative bud Annals of the Missouri Botanical Garden often aborted; nodes enlarged, buttressed, the leaf scar forming a nodal shelf perpendicular to the stem; stems terete or 4-winged when young, terete with age, free ends of the wings in some species elongated and indurated forming 4 (less often 2) spines; spines short or long, thick or slender, blunt or sharp, erect, incurved toward the stem, spreading, or recurved. Leaves subsessile or petiolate, opposite (rarely sub- opposite), decussate or very rarely ternate, entire, ovate, obovate, lanceolate, elliptic, oblong, linear- lanceolate, or suborbicular, thinly to thickly membra- e or distinctly coriaceous and shining, venation brochidodromous with a membranous to thickened margin and an intramarginal v ein, or the intramarginal vein forming a distinctly cartilaginous margin, secondary veins typically visible, the tertiary veins less so and sparsely to densely reticulate, sometimes thickened on the abaxial leaf surface. Inflorescences simple racemes, or condensed umbel-like clusters, or flowers solitary, the flowers 1 to few (to 20) in the axils of the main and lateral shoots; pedicels Vibe slender, bearing bracteoles at the apex; bracteoles duous. Flowers 4- or 6(7) the sepals valvate, deltate; floral cup siete ils to shallowly so, membranous or coria- ceous, green or green turning red with age especially wë abruptly or w pudkudlly contracted below the absent; petals ovate, orbicular, or obovate ii aibi sometimes clawed, white, intense rose, or rose- or violet-purple; stamens 8 to 40 or more, inserted individually or multiplied on the floral cup along the distal margin of a tissue lining the inner surface of the floral cup, the tissue narrow and encircling the base of the ovary or extended distally, the distal margin not free, or minimally free at the distal margin or extended to form a narrow freestanding collar, staminal I flattened, glabrous, red or green, exserted, included, stamens sometimes crumpled back into de floral cup, anthers yellow, revolute; pollen prolate to prolate-spheroidal, tricolporate with 6 pseudocolpi, the exine psilate to distinctly m ovary 2- to 6- locular, globose to slightly de and 6-sulcate, the narrow, thin septal walls incomplete at the apex, the placenta central, ovoid to globose, enlarged at — style sturdy, persistent at the apex of the axile placenta in fruit, generally long-exserted; stigma small capitate to nA Fruit a dehiscent capsule, bro: r wine-red, moderately thick-walled, 2- to Salas the valves bipartite at the apex; numerous, small, crowded and irregularly fully covering the surface of the enl placenta, golden to light brown, elongate, prismatic with 3 or 4 poorly defined sides or bilaterally compressed, obovoid, retuse at the apex and tapering to the base or fusiform and tapering toward both ends; seed coat thick to thin and fragile; embryo straight, the cotyledons oblong-spatulate, ca. twice as long as the radicle. Key To THE SPECIES OF GiNORIA Two species that include both spiny and spineless plants appear twice in the key and are indicated iby an asterisk (*). length unless otherwise in dicated. Flower length i is measured from the base of the epipodium at the bracteoles to the apex of the sepals. la. Sepals and petals 4 lb. Sepals and petals 6 2a. Plants armed at the nodes by 4 (less often 2) spines : CHINE MEME TE, c wc aggere 3a. m — spreading to slightly ascending, 2— ps straight to sli recurved; leaves d e P to lanceolate, m x4- 15 mm; Haiti G. lanceolata horn-like, incurved or paliar: smsni Tn Wow E a AA 9X seeds narrowly fusiform; Fei: iN du the Lu AA 3. G. rohrii urved, — or P erect, 1-2 mm (rarely incurved in G. koehneana, which has leaves 10-25 X 5-20 mm); seeds obovate to ong-elliptic, concave-convex; Cuba $m" a d. a E MU w scarcely contracted to a stout a 0.5- ] mm 2. G. arborea 5b. Leaves obovate to suborbicular or oblong-elliptic, 10-25 X 5-20 mm, veins in ca. 8 to 10 FICA RAS A E A a pairs, tertiary veins thick, obscure; floral cup abruptly contracted to a slender „e ca. Leni a sls G. koehneana* 6a. "wn flow emose, mm; petals violet, 12-17 mm; Dominican es d 8. G. jimenezii 6b. Inflorescences loosely umbelliform, ios l to 20 per eS 3-8 mm; petals white or pale pink, A. A yy Yan q Ta. Leaves obovate to sibni or oblong-elliptic, 10-25 , margin white-cartilaginous; flowers I to 9 per Bosh Cuba . 9. G. koehneana* Tb. Leaves narrowly elliptic or TE 40-90 x 15- 35 margin membranous; flowers 8 A 20 per Ws Were u pu uu, 1. G. nudiflora 8a. BE x L 1 1 y A ra " p iD 9 "m dM V e vessels. s.s 11 9a. € Mm mm, "m e eae c qure E di. € americana w var. r. spinosa 9b. Spines 0.5-3 mm, robust, E spreading or BOE LII A AE 10a. Saal margin white-cartilaginous; epicalyx corniform S at the sinus between atia sepals; spines deny recurved, 1-2.5 mm a E E a s 5. Ç cunispina membranous; absent spines variously recurved, sarai or w ied Volume 97, Number 1 Graham 57 Revision of Ginoria (Lythraceae) 0.5-3 mm, — present €: pe developed ....... . americana* var. americana . Epicalyx absent, ae sinus ifs s free p thickened growth; ilm alender 2-75 nube co oL Resa ions ——— À la. G. americana* var. americana uous flange encircling the exterior p at the base of the sepals, or dis- bicis as a thickened growth at sinus between adjacent sepals; epipodium absent or present and stout or slender, 16mm ........ 12 12a. Epicalyx a continuous flange encircling the exterior of the floral cup at the base of the sepals 12b. Epicalyx discontinuous as an elongate or corniform growth at the sinus between adjace "t sepels, or a he L... k. — — = thick pocket narrowly winged or or thickened 13a. Epipodium slender, 5-6 mm; flowers — mm; Haiti and Dominican Republic ......... 3. C. buchii absent or stout to 2 mm; flowers ers 12 mm; leaves yellow- to gray- green adaxially and abaxially ptr or broadly ovate, 17-52 X 10-40 win Haiti... ere le eee s 2 G. pulus 14b. Flowers 6-9 mm; leaves dark adaxi- ally, paler green €— ovate-oblong or ovate- lanceolate, 20-90 . 7. G. glabra l5a. Epicalyx an cone « or pka x at the sinus between adjacent sepals; flowers mostly 5 to 12 per axil, loosely Lodi leaf — often undulate; Cuba . ginorioides 15b. _ dex a thick pocket-like lobe at p^ sinus een adjacent sepals, subtended by a narrow e wing or thickened rib; flowers 1 or 2 per axil; leaf margin plane; Haiti 4. G. callosa 1. Ginoria americana Jacq., Enum. Syst. Pl. 22. 1760. TYPE: Cuba. “Habitat ad ripas flu- viorum rupestres & glareosas in Cuba" (neo- type, designated [as lectotype] by Graham, 2005: 301, plate 91 of the protologue). Figures 1, 12 Subshrubs or shrubs, 1-2(—3.5) m; stems erect or laxly ascending, glabrous or peccet, tending to wine-red when young, branc (variety americana) or armed by (2 or)4 spines (variety americana and variety spinosa), in variety americana, the spines ranging from scarcely developed to stout, variously incurved, spreading, or recurved, 0.5-3 mm, in variety spinosa, the spines slender, acicular, erect, 5—9(-17) mm. Leaves with petioles 0.5—1 mm; blades s to narrowly elliptic or linear- oblong, 1 x mm, thickly membranous, deep green adaxially, p: i apex obtuse to acute, margin not cartilaginous and the intramarginal vein present ca. 3 mm inside the margin of larger leaves or merging with the margin on small leaves (variety americana), or cartilaginous and lacking intramarginal tissue (variety spinosa), second- ary veins in 3 to 10 pairs, acutely ascending, tertiary veins obscure. Inflorescences racemose, | or 2 flowers per axil on the main stem; pedicels 10—30(—40) mm, slender; bracteoles 1-5(-9) mm, linear to spatulate. lowers 6-merous, globose in bud, shallowly a nulate at anthesis, coriaceous, 7-17.5 mm, 5-15 m diam. at the floral cup margin, abruptly MU to a slender epipodium 2-7.5 mm; floral cup 3-5 mm, green or green tinged with red, intensely red-purple to dark red after anthesis; sepals 4—5 X 2.5-5 mm, deltate to ic ga deltate, erect to spreading; — 6, orbicular or dabas 7-15 X ca. P mm tu a claw 0-1 mm, bright aM stamens 12(to 16), surrounding the base of the ovary, inserted ca. 1.5-3 mm below the sinuses along the margin of a scarcely developed inner tissue layer, exserted beyond the sepals or partially crumpled into the floral cup, filaments 4—7.5 mm, anthers ca. 3 mm; ovary 4- to 5-locular, green turning ark wine-red; style 5-9 mm, exserted. Capsule globose, included; seeds 0.9-1.2 X 0.4-0.6 mm, subrectangular to obovoid, slightly bilaterally com- pressed or prismatic with 3 or 4 poorly defined sides. Chromosome number: 2n = 56 (Tobe et al., 1986; reported as Ginoria glabra). Discussion. Ginoria americana is the only 6- merous species (six sepals and petals) that has no epicalyx. Seeds are mostly more rectangular in outline and thicker-coated than the other species but vary, some approaching the type found in G. curvispina. Plants also vary greatly in pyi size and shape and numbers of flowers produced. distributed and most common species of the Cuban Ginoria. Ginoria americana var. ame throughout Cuba on rocky islands in streams and is the most widely ricana occurs ce oblong-linear leaves at the — end of the size range, with full or partial intramarginal venation. Young stems tend to be wine-red, and the shallowly campanulate floral cups become as they mature, in striking contrast to the showy rose- purple petals. The same coloration at maturation has n observed in G. buchii and G. callosa. — (in cultivation), G. americana var. ame orms deep wine in color multiflowered brachyblasts to 2 cm. Variety amer- icana is mostly unarmed but can produce inconspic- uous nodal knobs that sometimes develop unequally into one to four recurved, spreading, or incurved spines (e.g., as in Graham 1143, HAC, MO). Spiny and spineless plants of G. americana var. americana are determined separately in the generic key. In the vicinity of Santa Clara, province of Villa Clara, and in a few scattered localities in La Habana, Annals of the Missouri Botanical Garden Figure 12. Ginoria americana Jacq. var. americana. S). —C. Flower (Ekman 83, S. Matanzas, Camagüey, and Cienfuegos provinces, a distinctive, more spiny type of Ginoria americana bearing four notably long, slender, erect nodal spines PE i ic habit penti ils. Plants with this form are more shrubby with many short branches, have little or no anthocyanic coloration, and the i inal vein of the mostly smaller, thicker leaves forms the thickened margin of the leaf. At one site in —A. Habit (Graham 1145, MO). —B. Leaf, adaxial view (Ekman 83, Santa Clara, I observed spineless, large-leaved G. americana var. american, g 1 g I: tream at the base of a serpentine bluff and long-spined, small- leaved G. americana var. spinosa growing immediately above, rooted in cracks of serpentine rock. No intermediate forms were present (pers. obs.; Graham 1135, MO) Although th phological ext f the varieties are strikingly different, leaf shape and sizes Volume 97, Number 1 Graham 59 Revision of Ginoria (Lythraceae) Figure 13. Distribution of Ginoria americana Jacq. var. americana. and flower sizes overlap quantitatively. I have come to the same conclusion reached previously by Alain in an annotation on Wright 2545 (NY) to treat the spiny and Ë 1 , E lib Lek. | NP E between these taxa needs further study. The spiny type is given formal taxonomic recognition at the varietal level here on the basis of the consistent presence of the slender long spines, generally smaller elliptic-oblong leaves and small flowers, and what appears to be an edaphic restriction to dry, primarily serpentine, soils within the broad geographic range of the species. la. Ginoria americana var. americana. Figures 1 12 Juvenile stems green to red, glabrous to densely puberulent; nodes or some nodes incon- spicuously armed by robust spines 0.5-3 mm, the spines incurved, spreading, or recurved, some un- equally developed at a node. Leaves oblong-lanceolate to narrowly elliptic or linear-oblong, commonly 25-65 X 15-35 mm, intramarginal tissue present, the leaf margin membranous. Floral cups 10-17.5 X 8-15 t s wine-red with age. Chromosome number: 2n — 56 (Tobe et al., 1986; reported as Ginoria unt Distribution. Cuba, occurring throughout the island in the pro- vinces of Camagüey, Cienfuegos, Ciego de Avila, Ciudad de La Habana, Granma, Guantánamo, La Habana, Holguín, Las Tunas, Matanzas, Pinar del Río, Sancti Spíritus, Santiago de Cuba, and Villa Clara (Fig. 13). It is found along freshwater streams, on sandy or rocky stream margins, and among rocks in flowing rivers from m The autonymic variety is endemic to Phenology. Plants have been collected in flower beginning in December. They continue to flower and fruit through June. Old fruit often persistent from July to January. Common names. Clavellina del río, rosa del río (Echevarría & Graham, 2008). T ux specimens examined. CUBA. s. loc., Rugel 727 (GO amagüey: zona costera, Ie e Mar. 1987, m 3028 (HACC); — de un o ce San Felipe, O Apr. 198 - Méndez 3 3368 (HIPC): ca La on. El Pilar, Dec. 1984 Risco & Méndez 2544 (HAC, HAJB, HIPC). Ciego de siio: at Río Azul along the Carr. Central, 18 km N of Ciego de Avila, Mar. 1910, Britton et al. 6000 Mar. 1911, ie gr et al. 10279 (NY); San Blas, T Vegu ip cafetal Buenos Mar. 1986, Camacho et al. (HPVC); vic. of Cini Mae 1891, Combs 26 (CH. i NY) afluente del Río Hondo, Las Tapias, Nov. 1986, Expedición del HAC 37366, 37332 (HAC); 8 km S of El Jardín Botánico Cienfuegos in Soledad, 300 A . Hodge & Howard 4561 (A, oaquin, vic. of Soledad, Aug. 1941, Howard 6245 (GH, NY): San Blas, 8 Mar. 1930, Hunnewell 11548 (GH); Soledad, Harvard Tropical Garden, Feb. 1926, Jack 4070 (A, US), Apr. 1926, Jack 4532 (A, US); Limones, t Feb. 1927, Jack 4731 (A); Belmonte, Soledad, o, Apr. 1927, Jack 5082 (A); Soledad, Limones, EA 1927. Tack 5481 (A, US); Soledad, Limones, Oct. 1927, Jack 5551 (A); San Blas, La Sierra, Dec. 1928, Jack 6779 (US); entre San Blás y — Sierra del Escambray, Sep. 1975, Meyer 28266 (H Sierra San Juan, Sues San Blas, Nov. 1941, Morton pur (US); Trinidad Mtns., Buenos Aires, Feb. 1956, Morton 10380 (US); Golosa Linens, lass Soledad, Feb. 1903 t = ° P $3 Annals of the Missouri Botanical Garden Pringle 105 (GH); Belmonte Hill, Soledad, 26 Feb. 1928, Rehder 1123 (A); San Blas, i ” July P - & ç S ton ong Trinidad T July 1950, Smith 3071 (AJBC); rd. betw. Gavilanes & La Sierra, July 1936, Smith & Hodgdon 3172 (CH). Ciudad de La Habana: Guanabo, Campo ido, Loma de la Coca, Dec. 1 uL owe TM Sh e 83 (S); recu - 24169 (HAC; Val Valle de A sy Almendares, Dec n b 331 (HAC); Río ao, Sep. 1912, León Sip (HAC J: ea Naranjo, x s. 1908; León 486 (HAJB); Río Almen- dares, Feb. 1889, Molai 473, 474 (HAC); Calabazar, Nov 1909, Ponce 229 (HAC); , Jan. a lermann 351 (HAC, NY); ne: » Jan. 495 (HAC, HAJB, MO, NY, US), 4351 diet bene a Rio Yara, Nagua, May Acuña 15128 (HAC, pp cultivada en Maik: Nov. 1953, D 19038 (HA Ensenada de Mora, river valley, Mar. 1912, Britton et E 12953 (MO, NY, US); Santa Elena, | El Pobre, Clemente 6312 (GH, NY, US); Río Buey, Mar. 1943 ER , Gu 4/3 (HAC); Yate ateras, dy 1928, Castellanos 97 (HAC); banks of Cañas peto La Clarita, Feb. 1948, Clemente 5924 (GH); in Río Y 1511 (HAC) vie. . 1902, Pollard et al (GH, MO, NY, US); márgenes E Río Duaba, base campismo El Yunke, May 1 isco & Romano 9516 9, Berazaín 23150 (HAJB); Madruga, Apr. 1903, Shafer m (HAC); San Antonio, Apr. 903. shady brook ne riui (NY); near asphalt m i — — AC). "Les T Matanzas: a, June 1976, Berazaín & González 31967, pro 31974, 31979 a Yaití, Martius s.n. (MO); vic. of Mat San Juan River, Mar. 1903 Ceiba Mocha, in anzas, roc! in 3 Britton e et al. ye (HAC, NY); 7 Rm í, edge of broo| e S: US); Ciénega de a e (HAC); pue Ux 1849, Rugel 65 (L, NY). Pinar del Río: P. jaibón, Acuña 10573 (HAC), Dec. 1936, NM m E Bahía Honda, Mar. 1946, Acuña et 65 (HAC); Anero de Soroa, Jan. 1952, Acuña & Alain x (HAC); Rio us Rangel, Acuña 24168 (HAC); Río la Cajalbana, La La Palma, Jan. 1951, Alain died I rig NY, US); San Diego de los Baños barranco del Río San Diego, Apr. 1976, Alvarez de e et ul. 3150 RARE cet Me I i am pueblo, Oct. 1990, Areces 2136 (MNHNC); us 1905, Baker 2797 (A, GH, HAC, NY, US); Sagua, orillas del arroyo, Nov. 1968, Bisse & Lippold 10681 (HAJB, JE); La Palma, Loma Peluda de Cajalbana, Sep. 1970, Bisse 18331 (JE); San Diego : los Baños, valle del Río Los Palacios cerca de Seboruco, Dec. 1979, Bisse & Lip (HAJB, JE); Sudden. a orillas de Río Frío, Dec. 1978, Bisse et al. 38900 (HAJB); Potosí, en aguadales de los rocas del río, Feb. 1996, Bonet 7454 (IPTH); San Diego de Los Baños, Aug.—Sep. 1910, Britton et al. 6742 (NY, US); vic. of Guane alls, Río Portales, Mar. 1911, Britton et al. 9766 (NY); Río Manantiales, N of Candelaria, Feb. 1916, Britton et al. 14121 (NY); Río San Cristobal, El Brujo, May 1927, Fors 4367 (HAC); Río Los Portales, El Salto, Guane, Sep. 1987, Luis et al. 3804 (HIPR); Río Portales, Guane, orillas del río sobre carso, Mar. yi Méndez & Verdecia 1074 (IPTH); Río Portales, base de campismo, Mar. 1989, Méndez & Verdecia 4514 n Seite pom Ew Rangel, Sierra de Los i on 2 (US); Río Portales, Dec. 1911, Shafer ari (A, n MO, NY, US); San Gabriel to Santa Mónica, on rocks in = ° Bahía Honda to Baños Aguacate, roeks in brook, Dec. 1910, Wilson 9220 (NY); Río San Miguel below Mal Paso, Dec 1910, E 9302 (NY). Sancti Spíritus: Sierra del Escambray, a lo largo del sendero de Topes de Collantes hacia e: Salto del Caburni, a la orilla de rio, June 1993, Acevedo-Rodriguez et al. 5488 ane US); Topes de Collantes, los bordes de una cañada de bajo del acueducto, July 1974, Areces et al. y 76 (HAJB); orillas del Río Blanco, cerca de Poza Azul, May 1987, A et al. (^m pore. Rio Banao ey AIP EL Naranjal, Lomas de en el oo | ie 755, 781 ass "Sierra del ray, EK dela Vega, manantial en la carretera de dn Blás, Jan. 1967, Bisse & Duek 1114 (HAJB); Sierra del Escambray, bn del Burro, Nov. 1967, Bisse 4706 (JE); Loma pie rhe del Jobo), Nov. 1979, Bisse et al. 41140 (HAJB); T dad Mtns, Hanabanilla F. Falls, Mar. 1910, Britton et al pe (NY); Trinidad, Loma de Zayas, detrás del pismo Manacal, Dec. 1996, Calzada et al. 6153 (HPVC); anizares et al. 99 (HJSS); Las Damas, Sep. 1994, Castafieda 99 (HJSS); Lomas de Banao, Feb. 1920, Luna 219 (NY); Guamuhaya, márgenes del Río Las Cañas en el Campismo Manacal, Noa et al. 6409 (HPVC); vic. of Sancti Spíritus in river, Feb. 1912, Shafer 12160 (A, NY, US). Santiago de : Sierra Maestra, — del Río Magdalena, May 1971, Bisse & Lippold 19501 (HAJB); Río 1944, Clemente 2410 ( (HAC); Chirivico, Apr. 1944, mds & Chrysogone 3410 (HAC, NY); La Cl Feb. 1948, Clemente de la repre: ae HAJB); forest about Paso Estan near water in arroyo, Apr. 1909, Shafer 1579 (NY, US); Sevilla Estate, near Smp à Sep. 1906, T. Ter am 177 (NY). Villa Finca Guadalupe, Placetas, . 1952, Arusa I 7512 (HAC, NY); cuabales entre Santa o: ; Britton et al. 4669 (NY); palm barren, Clara, 1912, Britton & Cowell 13307 (NY) “ua la Grande, camino que va del IPUEC Miguel Diosdado Pérez Pimentel” a la Presa Alacranes, Nov. 1998, Duarte 7007 (HPVC); ; sabana al E de June 1932, León 15631 (HAC): Placetas, Cerro i 3 E x 7 Volume 97, Number 1 2010 raham 61 Revision of Ginoria (Lythraceae) Caicaje al Sur del Olivar, Apr. 1987, Noa & — 1539-A n € cerca de Arroyo Saguito, Rese . June 1987, Pérez 243 (MNHNO). ea U S.A. Finds Fairchild Garden #1753C, plot 33, from University of Havana Botanical Garden via Keim 29. Mar. 1982, A. Bird s.n. (MO), Gillis 7963 (MO). Locility unknown: Ramon de la Sagra s.n. (A). lb. Ginoria americana var. spinosa (Griseb.) S. A. G : Cuba. “Cuba or.," C. Wright 2545 p.p. (71200) (holotype, GOET!; isotypes [restricted to the hes so annotated in this mixed collection], nc GH!, HAC!, MO!, NY!, S [2])). Figure 14. Juvenile stems reddish brown, glabrous or sparsely pubescent; nodes conspicuously armed by 4 brown, slender, aciculate, rigidly erect, spines 5-9(-17) mm. Leaves elliptic-oblong, 10-25 X 5-10 mm, intramar- ginal tissue absent, the intramarginal vein forming a cartilaginous leaf margin. Floral cups 7-12 X 5- 10 mm. Chromosome number: unknown. Distribution. The variety is endemic to Cuba, in the provinces of Camagüey, Cienfuegos, La Habana, Matanzas, and Villa Clara on dry, rocky serpentine sites from 50-500 m (Fig. 15). Phenology. Plants have been collected in flower and fruit from March through June. me. Clavellina espinosa (León & Mean 1953; Roig y Mesa, 1963). Discussion. Grisebach described Ginoria spinosa from the single sheet of Wright 2545 at GOET, without knowledge that Wright 2545 is a mixed collection of two spine-bearing species. The holotype is exclusively G. spinosa. M lacks a printed label but bears a handwritten one with the Gray and Wright — the species name, a brief diagnosis, and "Cuba oc Wr 1863" in Grisebach's hand. Other sheets of this number include both G. americana var. spinosa and G. curv ispina (GH, HAC, MO, S [2}), -— G. — var. spinosa (NY-Torrey), or only ispina (/ US). Field labels of Wright 2545 (CH) infine plas were collected in: Villa Clara; Sancti Spíritus/Villa Clara at Río Agabama on 18 January near Villa Clara on 19 January; in Pinar del Río at San Cristobal on 7 and 17 April; and in savannas and '; along rivulets along margins of streams at Charco del Toro on April 17. The collections made in Pinar del Río are C. curvispina. Those from the vicinity of Villa Clara include G. spinosa and C. curvispina (the other species in the mixed collections of Wright 2545 [= 1200]. Additional specimens examined. CUBA. Camagiey: Río Los Montesitos, May 1985, Méndez & ipeo 8036 (HIPC). : San Blas, Veguitas, cafetal Buenos 1 May 1984, Noa 562 (HPVC). Habana: Canasí, cerca del central Elena, July 1970, Bisse & Lippold 1 7523 (HAJB, Pe arroyo en Loma de Galindo, n de Fitoquimicos 27081 me Matan- zas: in cuabales NW of ra ae i Matanzas, SE of Canasí May 1923, Ekman 16517 (NY, S). Villa Clara: Santa Clara, rro de Pelo de Malo, May 1974, Alfonso et al. 131, 186 ritton et al. 10243 LIE palm barren, Sa 3308 (NY, US); Santa Clara ^ Parri 2003, Graham 1135 (FTG, HAC, MO); rd to eS Bop 4-8 km S of Santa e serpentine barrens, June 1955, Harvard Course in Tropical Botany 121 (CH, NY); 6 km W of Santa Clara, Harvard Course in Botany 875 (GH); € km S of Santa Clara, — 121 (AJBC); Trinidad Mtns., 10 km W of Santa Clara, Jun Aug. 1941, Howard 5063 (cH. NY, S, US); El €—— om 1998, Méndez et al. 10019 ig Santa ae alrededores de la Presa Gramal, E HPVC); Santa Clara, La Hoya, cuabal, May e ifa et al. 470 (HPVC); frente a la entradad del aeropuerto, ue de galería, May 2001. Noa & Méndez 7373 (HPVC); near Santa Clara in serpentine savanna, July 1950, Smith 3109 (AJBC); rocky bed and banks of river 10 km E of p. Clara, July 1936, Smith & Hodgdon 3204 (GH, NY, S 2. Ginoria arborea Britton, Bull. Torrey Bot. Club 39: 13. 1912. TYPE: Cuba. “Thicket, Leeward Point, United States Naval Station, Guantánamo Bay, Cuba, March 1909,” N L. Britton 2217 (lectotype, designated by Graham, 2005: 301, NY 84338!; isotypes, NY 84337!, US!). Figure 16. Tall shrubs or small trees to 8 m, ca. 2.5 dm DBH; stems with short terminal branches, glabrous; nodes armed by 4 spines 1-2 mm long, the spines enlarged at the base, horn-like, recurved to spreading. Leaves often crowded at the tips of the branches, sessile; blades linear-oblong to lanceolate or infrequently obovate, 10-40 X 3-16 mm 8 mm, coriaceous, the surfaces varnished y resin, shining, bright green adaxially, green abaxially, base acute or narrowly attenuate, apex obtu , commonly ca. 20 X se, mucronate or retuse, margin slightly cartilaginous, intramarginal vein present, 0.3-0.5 mm inside the margin at widest leaf diameter, secondary veins in 3 to 5(to 8) pairs, acutely ascending, tertiary veins slender, visible abaxially. Inflorescences I(to 3)-flowered highly re- duced brachyblasts, some flowers also solitary in the axils on vegetative shoots; pedicels 9-12 mm, slender. lax; bracteoles to | mm, narrowly linear. Flowers 4- merous, globose in bud, shallowly campanulate at anthesis, thickly coriaceous, 4-5 mm, ca. 3 mm diam. Ki r Annals of the Missouri Botanical Garden < == SA 2cm NN E SK WW ee nee ji Figure 14. Ginoria americana var. spinosa (Griseb.) S. A. Graham. —A. Habit. —B. Node with aciculate spines. A, B from Graham 1135 (MO). at the floral cup margin, scarcely contracted to a stout epipodium 0.5-1 mm; floral cup 0.5-1 mm, green; sepals 2.734) X 15-1.7 mm, narrowly deltate, erect; epicalyx absent; petals 4, broadly obovate, not clawed, 2-4 X 0.5-1 mm, scarcely exceeding the sepals, white, the margins erose above the middle; stamens 12 to 14, inserted ca. 1 mm below the sinuses along distal margin of the inner tissue layer, well- exserted beyond the sepals, filaments 3.5-5(-7) mm, anthers ca. 1 mm; ovary 3- to 4-locular, green; style ca. 6 mm, exserted. Capsule ovoid, included; seeds 1.4-1.5 X 0.4—0.5 mm, compressed, concave-convex, obovate-oblong-elliptic. Distribution. Ginoria arborea is endemic to Cuba, in the provinces of Guantanamo and Santiago de Cuba (Fig. 17). It grows in thickets, on dry hills, and on coral reefs from m. Phenology. The species flowers primarily from February to May. It has been collected in old fruit in Volume 97, Number 1 Graham Revision of Ginoria (Lythraceae) Figure 15. Distribution of Ginoria americana var. spinosa (Griseb.) S. A. Graham. November (Ekman 15780, NY) and in new fruit in March (N. L. Britton 2217, NY) Common names. 1963). Granado, jaspe (Roig y Mesa, Discussion. | Ginoria arborea, an apparently rare or at least rarely collected species in Cuba, is most similar to G. koehneana. Both have flowers that are thickly coriaceous, 4-merous, have inconspicuous white petals, and are among the smallest in the genus. However, miei the floral epipodium is stout and scarcely racted in G. arborea, it is slender and =a bind below the floral na. Ginoria arborea is a tree to 8 m tall; C. o init is currently known as a large shrub or small tree to 4 m. The species bear similar spines (not scored for G. arborea in Graham, 2002). Leaves of G. arborea vary widely in size from one plant to another but are smaller and more linear-oblong than the mostly obovate-suborbicular leaves of G. koehneana In addition, leaves of G. arborea have three to five(to eight) prominent secondary vein pairs, and the adaxial leaf surface is coated with a shining resin. In C. koehneana, leaves have secondary veins in pairs of eight to 10, dense tertiary venation, and the adaxial leaf surface is free of exudate. The species grow in similar coastal habitats on rocky limestone soils in eastern Cuba, although G. arborea is restricted to the southeastern coast and G. koehneana is found only on the northern coast with the exception of one collection from interior Guantanamo near San German. Floral morphological similarity, geographic proximity in eastern Cuba, and morphological cladistic analysis support a sister relationship. Few flowering specimens of either species have been collected. Ginoria arborea especially needs to be relocated, and fertile collec- tions of both species need to be made to better understand the species’ variation and relationship. dditional specimens examined. CUBA. Guantanamo: lomas al E del a E Mariana (Siguato), 5 km al NO de San Antonio del Sur, May 1980, Alvarez de Zayas et al. 43136 (HAJB); San oer del Sur, 4 km ONO del pueblo, Feb. 1976, Areces et al. 29964 (HAJB, JE); San Antonio del Sur, 4 km al ONO del pueblo, Feb. 1976, Kidd et al. 31375 o a la mina del Mina del Yeso, monte seco, Apr. 1972, Bisse 21 "D 9 (HAJB. JE); alrededores de Tortuguilla, manigua costera, Apr. 1972, Bisse 21830 (HAJB, JE); D al E del Abra de . Jan. 1977, Bisse et al. (HAJB); Abra de Mariana, loma al O del edi p^ 1978, Bisse et al. ae (HAJB); Abra de Mariana, loma al E del Abra, Feb. 1979, Bisse et al. 39076 (HAJB); loma al N de i AJ a 1977, Bisse et d 39471 P on the shore, Nov. 1922, Ekman 15780 (NY, S, US). Santiago de Cuba: Sibone manigua costera cerca de la Playa Berraco, Apr. 1969, oat 14570 (HAJB, JE); Daiquiri, in thickets on coral reef, Nov. 1916, Ekman 8363 (NY, S, US 3. Ginoria buchii (Urb.) S. A. Graham, comb. nov. E Haitia buchii Urb., X Repert. pec. Nov. Regni Veg. 16: 141. 1919. TYPE: Haiti. “In montibus prope Jacmel in praeruptis siccis 300 m, June 1916 flor.” W. Buch 1181 (lectotype, designated by Graham, 2005: 302, GH!). Figures 1, 18. Slender shrubs to 3 m; stems with branches of the season somewhat compressed, faintly 2-angled; nodes unarmed. Leaves with petioles 3-4. mm; blades narrowly ovate to ovate, 50-130 X 30-65 mm, typically ca. 75 X 35 mm, chartaceous, glabrous, green adaxially and abaxially, base rounded, w JC SH SO, BER RR GAS Cy 3 i e i j | : | 1 | : | | I I | I | | | 64 Annals of the Missouri Botanical Garden d x ^ 5 = GS Figure 16. abaxial view (N. L (Bisse 21 769, JE). —F. Flower (Ekman 15780, S). Britton 2217, NY). — rarely acute, apex acute or short-acuminate, margin branous, intramarginal vein present, 1-3 mm inside the margin at widest leaf diameter, secondary veins in 8 to 20 pairs, nearly horizontal, shallowly ascending, tertiary veins moderately visible, reticu- late. Inflorescences 1- to 3(to 6)-flowered highly reduced brachyblasts, some uw also solitary in the axils of the í dicels (18—) 20-30 mn, slender, lax; LE 0.7-1. 5 mm, ovate. Flowers 6-merous, subglobose in bud, shallowly campanulate at anthesis, coriaceous, 14-18 mm, 10 mm diam. at the floral cup margin, abruptly contracting to a slender epipodium 5-6 mm long; floral arborea Britton. e Habit (Bisse n 769, JE). —B. Leaf, = view (Ekman 8363, S). —C. Leaf, D. Leaf, iew (Ekman 8363, S). —E. Node with four horn-shaped spines cup 4.5—6 mm, green, turning wine-red within; sepals 4.5-6 X 5-6 mm, the apex acuminate-deltate, 0.5— 0.8 PE a, delexed, sl ae speading v to akal ightly encircling the exterior 6 thes oral cup at base of the sepals, ca. 1 mm wide at the sinuses, narrowing to 0.5 mm between sinuses; petals 6, obovate, 12-18 10-14 mm, not clawed, rose-purple; stamens 34 to 40, tissue layer, well-exserted, filaments 7-10 mm, anthers ca. 4 mm; ovary 6-locular, slightly depressed, 6- sulcate, turning dark red; style 10-14 mm, exserted. Volume 97, Number 1 2010 Graham Revision of Ginoria (Lythraceae) Figure 17. Distribution of Ginoria arborea Britton. Capsule a Meus p the margin of the floral cup; se mm, compressed, concave- convex, o. innen buchii is endemic to Hispa- niola, growing in Haiti and the western Dominican Republic, on steep reine cliffs from 300—700 m (Fig. 19) Distribution. Phenology. Flowering occurs from March through June, with mature fruits beginning in April. Discussion. Possibly the most beautiful of the Ginoria species and one of the most beautiful endemic shrubs of Hispaniola, G. buchii has large, dark green shining leaves and multi-staminate flowers resembling wild roses (Fig. 1). The undulating mp (the epicalyx) aaa the 6-merous floral cup an iis elongate epipodium at the base of de floral p are S. for the species. Ginoria glabra, also with 6-merous flowers and an encircling epicalyx, differs by a short, stout epipodium or the epipodium missing and by leaves with specialized, thickened yellow veins. Botanists from the Jardín Botánico in Santo Domingo have sought on several occasions without success to relocate the species at Río Arriba del Norte, where it was last collected in 1969. A dam at Sabaneta to the south has turned part of this area where it n the Río San Juan into a reservoir (T. Zanoni, pers. comm.). Liogier (pers. comm.) remem- bers his ilium was made above Río Arriba del Norte on the slopes leading to the mountain crest. Liogier (1986) refers to an additional collection from Haiti, “Grand Goave, Thomazeau,” to a collector. without reference Additional specimens examined. DOMINICAN REPUB- LIC. San Juan: in ravine of Rio Arriba del Norte, N of Sabaneta which is N of San Juan, Apr. 1969, Liogier 14693 (GH, NY). HAITI. Ouest: Massif de aww Grand-Bois, rd. Thomazeau to Cornillon, in gorge de la Gascogne, steep P cliffs, Mar. 1926, Ekman 5676 = MO, 5, US). Sud: Massif de la Hotte, eastern group, Grand-Goàve, Trouin, steep cliffs at Riviere cb es Apr. 1926, Ekman 5942 (GH, S). 4. Ginoria callosa O. C. Schmidt, Ark. Bot. 21A(5): 17. 1927. TYPE: Haiti. “Massif du Nord, prope Port-de-Paix, in cacumine montis Haut-Piton, ad o “wak dubium orientalium 1200 m flor” E. L. Ekma alt., 4619 bic T de Graham, 2005: 301, NY!; isotypes, A!, C not seen, EHH not seen, GH!, LL!, MO!, E^ S [2]!, US [2]!). Figure 20. Small trees to 6 m; stems with many short terminal branches, glabrous; nodes unarmed. Le the tips of the des, “ao 1-4(—7) mm; blades broadly em less often orbicular to oblong or obovate, 18—48(-75) X 10—28(—40) mm, thickly membranous to coriaceous, shining, green ign yellow-green ially, with a mucronate tip, margin plane, slightly inrolled, 0 Leaves crowded at se attentuate, apex ro intramarginal vein present, inside the margin at widest leaf diameter, midvein prominent, secondary veins in 7 to 10(to 14) pairs, ascending, tertiary venation thickened, pale yellow, coarsely reticulate with large areolae. Inflorescences l- or 2- flowered highly reduced brachyblasts; pedicels 12— 23 mm, sturdy, erect; bracteoles 2—3 mm, ovate- suborbicular. Flowers 6-merous, globose in bud, shallowly campanulate at anthesis, thickly coriaceous, 8.5-11 mm, 6.5-10 margin, epipodium mm diam. at the floral cup absent, the base of the flower immediately subtended by bracteoles; floral cup 5— 6 mm, green, turning wine-red within; sepals 3.5—5 X Annals of the Missouri Botanical Garden Figure 18. Ginoria buchii (Urb.) S. A. Graham. —A. Habit. —B. Flower. A, B from Ekman 5942 (S). 2.7-4 mm, narrowly deltate, semierect to erect at anthesis, spreading in fruit; epicalyx a thickened pocket-like growth, ca. 2 mm wide at the sinus between adjacent sepals, extending below each sinus along the vein to the of the floral cup as a narrow undulate wing or thickened rib 1-1.5 mm wide; petals 6, obovate, 14-20 X 11-15 mm, deep rose-purple, becoming paler with age; stamens 30 or 31, inserted ca. 2 mm below the sinuses on the distal edge of the narrowly free margin of the inner tissue layer, exserted, filaments ca. 7 mm, anthers 1-15 mm; ovary 3- to 6-locular, tuming wine-red; style 10— 15 mm, exserted. Capsule globose, depressed, in- cluded; seeds ca. 0.9 X 0.2 mm, compressed, obovate. Distribution. | Ginoria callosa is endemic to Haiti and ta ben EE " E fO... A E E J JF - of the mountain on the eastem slope at 1205 m (Fig. 19). Phenology. Flowering probably begins in June; flowering specimens have been collected in August. Mature fruits are present in September. Common name. Cuaresmilla espinosa (Roig y Mesa, 1963). Discussion. Ginoria callosa is a well-defined species with coarsely reticulate, yellowish-veined leaves that are crowded at the tips of the stem and a unique epicalyx consisting of a large pocketed lobe at each sinus that continues as a thickened rib or narrow Volume 97, Number 1 2010 Graham Revision of Ginoria (Lythraceae) Figure = Distribution of Ginoria buchii (Urb.) S. A. Graham, G. callosa O. C. Schmidt, and G. jimenezii Alain on Hispaniola. wing downward along the vein to the base of the floral cup. The bud, viewed from the apex, is scalloped in outline due to the extended pocket-like epicalyx segments. Ekman, collecting on the northwestern coast of Haiti in 1925, found the species common at the edge of the forest at the type locality slightly southeast of Port-de-Paix. It apparently has not been collected since. ul = specimens examined. HAITI. Nord-Ouest: = $ 4 Nord, Port-de-Paix, Haut-Piton, top of the mtn., on m ort, 1205 m, Apr. 1925, Ekman 3722 (S); 20 Sep. 5 [fruit], Ekman 4870 (LL, MO, S). 5. Ginoria curvispina Koehne, Bot. Jahrb. Syst. 3: 349. 1882. TYPE: Cuba. C. Wright 2545 p.p. (= 1200) (lectotype, designated by Graham, 2005: 301, MO!; isotypes [restricted to the branches so annotated], GH!, HAC!, MO!, NY!, S [2], US). Figure 21. Ginoria parviflora Urb., Feddes Repert. Spec. Nov. Regni 18: 20. 1922. TYPE: Cuba. Camagüey: “prope D in savannis solo humido, m. April. flor.," [2- i zs 1912], N. L. Britton, E. G. Britton & J. F. Cowell A 148 (lectotype, designated by Graham, 2005: 302, úl NY!; isotype, US!). ie microphylla O. C. Schmidt, Feddes Repert. Spec. "e Regni Veg. 24: 78. 1927. TYPE: Cuba. Holguín: : n^ in silva litorali, solo calcareo, 20. 5. 1916," E. Bee 7325 (lectotype, designated by Graham, 5: 302, NY!; isotype, S!). Ec 1—5 m; stems glabrous; nodes armed by (2)4 ya wasa recurved spines 1—2.5 mm long, the is orn-like, yellow, turning brown with age. ves sessile or petioles to 1 mm; blades narrowly lanceolate-oblong, narrowly elliptic to linear, or infrequently suborbicular, 3—60 X 2-15 mm, often much smaller in the inflorescence than on the main stem, coriaceous and shining adaxially, opaque abaxially, base acute to rounded, apex obtuse and apiculate, acute on linear leaves, margin white- cartilaginous, formed by the intramarginal vein, secondary veins in 6 to 10 pairs, sharply ascending, tertiary veins obscure. Inflorescences 1- to 3(to 8)- flowered brachyblasts, flowers also solitary in the axils of the main stem leaves; pedicels 10-23 mm, slender; bracteoles 1-2 mm, linear or filiform. Flowers 6- merous, subglobose in bud, campanulate at anthesis, membranous, 4.5-8.5(-10) mm, 4-7 mm diam. at the floral cup margin, contracting to a short, slender epipodium 0.5-1.5(-3) mm long; floral cup 2-3 mm, green, often turning wine-red within; sepals 2.5-3 X 2.25 mm, deltate to narrowly deltate, erect to spreading at anthesis; epicalyx corniform growths at the sinus between adjacent sepals, 0.3-0.5 mm; petals 6, suborbicular to broadly ovate with an erose, frilly margin, 5-10 X 5-9 mm including a claw 0.5-2 mm, pale to medium purple; stamens (12 to)14 to 18(to 25), surrounding the base of the ovary, inserted 2-2.5 mm he margin of scarcely stamens inserted singly, the antepetalous stamens single or if proliferated, then doubled or tripled at the insertion point, inner tissue layer scarcely developed, filaments 4.5-7 mm, anthers ca. 1 mm; ovary 3- to 5- locular, turning wine-red with age; style 9-10 mm, exserted. Capsule globose, reaching the apex of the sepals at maturity; seeds ca 5 mm, compressed, obovate to oblong-elliptic. Annals of the Missouri Botanical Garden Figure 20. Cinoria callosa O. C. Schmidt. —A. Habit. —B. Leaf, abaxial view. —C. Flower. A-C from Ekman 4619 (S). Distribution. Ginoria curvispina is endemic to Camagiiey and Las Tunas, with a few scattered localities in Cienfuegos, Holguin, Matanzas, Villa Clara, and Pinar del Rio (Fig. 22). It is found on serpentine and lateritic soils in coastal and subcoastal habitats, in semideciduous mesophyllous to xerophyl- lous thickets, spiny matorral, and in anthropogenic, periodically inundated, palm savannas from 0-100 m. Phenology. Flowering and fruiting are primarily from February to June. Common name. Cuaresmilla espinosa (Roig y Mesa, 1963). Discussion. | Ginoria curvispina is a straggling shrub PE. 1 LI EET £ sE 2 + t , flower size, and stamen number. Leaves on a single branch may be suborbicul ul piculat tip ly linear with an acute tip, and leaves of the main stem are often three times larger than those of the short branches. Stamens vary from 12 to 25 on flowers of a single plant. Consistent characteristics of the species are ickened cartilaginous margin of the leaves, the presence of four stout, homy, deflexed nodal spines, and the corniform, deflexed growths forming the epicalyx. The type specimen of Ginoria curvispina Koehne at B was cited by Koehne as Wright 2545 p.p. because some of the other sheets of the same number were mixtures of G. curvispina and G. americana var. spinosa (G. spinosa Griseb.) Grisebach based C. spinosa on the same Wright number, but the specimen he studied at GOET was exclusively G. spinosa. Urban i i 1 ; AAN A n f f Volume 97, Number 1 2010 Graham 69 Revision of Ginoria (Lythraceae) Fi eer sh gure 21. Ginoria curvispina Koehne. —A. Habit. —B. Node with four spines. —C. Flower. A-C from Ekman 17006 (S). in E 2 parviflora as closely allied to G. curvispina uz ct in having ovate-oblong or oblong-linear is d opposed to lanceolate-oblong leaves in G. ae and flowers half as large with fewer a = to 15 stamens). Schmidt described C. in yi Ey as having smaller leaves (3-12 X 2.5- bids smaller flowers (ca. 4 mm long) with fewer ib ^ 12) than c. curvispina. More extensive RR of G. curvispina now demonstrate a much dE ge $ morphological variation and size that ^ MI fferences among the species. Lacking other characters to separate G. microphylla and G. a from C. curvispina, the species are relegated ispina. parviflor, to the synonymy of G. curvi i dditional specimens examined. CUBA. s. loc., “Cuba oriental," 1890, Morales 375, 475, 495 (HAC). Camagüey: Cubitas, Feb. 1929, Acuña 5172, 5173 (HAC); sabanas del camino de Cubitas, Limones, Aug. 1950, Acuña & Rodríguez 16299 (HAC); Sola, Feb. 1981, Alvarez de Zayas et al. 43778 (HAJB); Cayo Guajaba, cerca de la loma de los Hornos, Feb. 1981, Alvarez de Zayas, A. et al. 43791 (HAJB); Maniguas al N de Montes Grandes, May 1976, Areces et al. 31478 (HAJB); Cayo Sabinal, camino del embarcadero de Carraguao a los montes de El Siete, Jan. 1976, Areces 31753 (HAJB): (NY, US); savannas near üey, arroyos, Apr. 1912, Britton et al. 13113 (MO, NY, US); Cayo Sabinal on the path from Corte Jicote to “El Fuerte,” Oct. 1922, Ekman 15524 (S); Santayana in palm barrens on serpentine, June 1924, Ekman 19049 (S); 26 km N of Camagiiey on rd. to Sierra de Annals of the Missouri Botanical Garden Figure 22. Distribution of Ginoria curvispina Koehne. Cubitas and Paso de Lesca, 4 m W on gravel rd. to Loma Hierro, Mar. 2003, Graham 1139 (HAC, MO); Derramade del Coating, Mar. I Herrera 2996 (HACC); Sillas de Versalles, Cayo Palomo bosque de galería, Oct. 1986, I 4069 (HIPC); Méndez & Avila dig in Coco, Sep. » A. Pérez 790-793 (MNHNC); E madero del Cagüe 1987, á atanzas,” May 1915, ); Cayo Romano, Oct. 1909, Shafer (NY, S= vic. of Tiffin [Truffin], Nov. 1909, Shafer 2878 iu S : Jagüey . Jesus Menéndez, El Verdecia & Yero 3575 (IPTH); Guayabal, Amancio Rodrí- guez, Mar. 1990, Verdecia £ Brull 372 (IPTH); Mpio. Jesus Menéndez, Playa Genovesa, La ura, Noy. 1989, Verdecia € Brull 2781 (IPTH); Mpio. Jesus Menéndez, Blanca, June 1989, Verdecia 3676 aiea pen Jesus Menéndez, Las Nuevas, Apr. 1992, Verdecia et (IPTH); Mpio. Jesus Menéndez, camino a Pozo Blanco, Playa Herradura, Oct. 1993, Verdecia 6850 (IPTH); Vista Hermosa, Omaja, Matibaeva sabana con palmas, Nov. 1994, Verdecia & Bonet 7043 (IPTH). ei Ciénaga de Majaguillar, Martí, May 2004, Oviedo 42322 (HAC) Pim ar del Río: Salad i in thicket, Oct. 1920, Ekman 11549 (S); Iejenes, S < S. Bresto, May 1928, Fors 4787 (NY); Charco del Toro, N 1986, Manitz et al. 60393 (HAJB); Los Palacios to San Juan de Zayas near water, Jan. 1912, Shafer 11810 (A, MO, NY, i ibarién, Cayo Las Brujas, Farallén de la Bosw. May 1999, Castafieda 6913 (HPVC). 6. Ginoria ginorioides (Griseb.) uri po Torrey Bot. Club 39: 13. 1912. iplusodon ginorioides Griseb., Cat. Pl. nk E 1866. Ginoria diplusodon (Griseb.) Koehne, Bot. Jahrb. Syst. 3: 350. 1882, nom. illeg. TYPE: Cuba. “Cuba occ.," [Pinar del Río], C. Wright 2546 (— 1125) (holotype, GOET!; isotypes, A!, GH!, HAC!, MO!, NY [2]!, S!, US!). Figure 23. Shrubs or small trees to 7 m; stems glabrou unarmed, the outer edge of the nodal bed sometimes forming small knobs. Leaves with petioles 1—3(-7) mm; blades broadly elliptic to oblong, 30-90 (-110) X 20—50(-65) mm, membranous to chartaceous, green adaxially and abaxially, base acute to attenuate, apex acute to obtuse, margin membranous, often undulate, intramarginal vein present, 2-5 mm inside the margin at widest leaf diameter, secondary veins in 10 to 20 pairs, shallowl ascending to ascending, tertiary veins visible, whitish, reticulate. Inflorescences (1 to)5- to 12-flowered hi ghly reduced hencbyldasts to ca. 6 mm long, loosely umbelliform, some flowers also solitary in the axils of the main stem leaves; pedicels (7—)5—35(-43) mm, slender; bracteoles 0.5-2. mm, scarcely deve eloped. Fi 6-merous, subglobose in bud, campanulate at anthesis, thinly coriaceous, 9- A A E I Volume 97, Number 1 2010 Graham Revision of Ginoria (Lythraceae) a Ginoria ginorioides (Griseb.) Bri Floral bud (Bisse 13173, JE). ae 1 K mm diam. at the floral cup margin, ee oa slender epipodium 2-3 mm; floral cup 2535 gica to wine-red within; sepals 44.5 X a O deltate, erect; epicalyx discon- «id ined a elongate to corniform, straight or multiplied in rs 3 mm; petals 6 (indeterminately (111-1420) a cultivated plants), ovate to obovate, Vas lig (4—8.5-11 mm including a claw l- i ka M stamens 18 to 24 (to ca. 55). distal chm i E mm below the sinuses along the PU on the inner tissue layer, the antesepalous M. ing or slightly exceeding the sepals, the inde: i included, filaments 3—4 mm, sod vinh mm; ovary 3- to 4-locular, turning wine- age, style ca. 7 mm, exserted. Capsule globose, on. —A. Habit (Ekman 13742, S). — B. Flower (Ekman 13742, S). —C. included. reaching the apex of the sepals; seeds ca. 1.5 x 0.3 mm, obovate to oblong-elliptic. Distribution. Ginoria ginorioides is endemic to Cuba, occurring in the provinces of Pinar del Rio, La Habana, Ciudad de la Habana (cultivated), Matanzas, Villa Clara, Camagüey. Cienfuegos, Sancti Spíritus, Holguín, Santiago de Cuba, Guantánamo, and on Isla de la Juventud (Fig. 24). Habitats are dry rocky bluffs, low xeromorphic woods, and semi-deciduous or evergreen forested hillsides. The plants are facultative for serpentine soils at elevations of O to ca. 1000 m. _ Ginoria ginorioides flowers and fruits from February to June, with the peak period primarily Annals of th Missouri edd Garden Figure 24. Distribution of Ginoria ginorioides (Griseb.) Britton. in March and April. Flowers typically appear prior to full development of the new season's leaves Common names. Cuaresmilla árbol, júpiter árbol (León & Alain, 1953; = y Mesa, 1963 Ginoria ginorioides is a species of Wawaq pe spineless shrubs or trees distinguished by large leaves with undulate margins, prominent reticulate veins, and wide intramarginal tissue. The leaves are the largest produced by the genus in Cuba and are exceeded only by the largest leaves of G. buchii in Hispaniola. The elongate to corniform epicalyx segments, prominently visible on the buds, are diagnostic. In flower, the light rose- purple flowers form loose, showy, umbel-like clusters. A specimen in the Cienfuegos Botanical Garden transplanted from an unknown site in the wild is particularly attractive as a horticultural shrub because the flowers have multiplicative petals, and up to 55 stamens. Britton records G. ginorioides as a tree to 7 m tall at sea level in Cienfuegos and as a shrub on the southern slope of the Trinidad Mountains (Britton, 1912). Flowering typically precedes leaf production. The type of Ginoria ginorioides was collected in March 1863 at Finca Retiro near Taco Taco, Pinar del Río, where Wright stayed from June 1862 to August 1864 (Howard, 1988; field notes of Wright 2546, GH). Additional specimens examined. A. Camagiiey: Rio Maximo, “sa aa de Cubitas, May 15 Raga 6092 (HAC, HAJB). Cienfuegos: Sierra del Matagua de la Vega, Mar. 1969, Bisse 13173 (JE); Sierra del Escambray. cafetal de Buenos Aires, Mar. pos als Fico 13173 (HAJB); Sierra del Escambra arroyo a de Buenos Aires, Aug. 1972, Bisse 23253 aru; ma del i, erase l Pico San 976, Bisse et nos San ae ar. 1942, Gonzales 655 (A, NY, S); Jardín Botánico de Cienfuegos, garden plant A original source unknown, Mar. , Graham 1144 (HAC, MO); Buenos — hrs A cliff, Hüniesell 11577 (GH); b Vegas de Ma San Blas, La Sierra, Apr. 1928, Jack 5967 (A, ri s K. Sol n t» LIRE Buenos Aires, Apr. 1930, pues 7899 (US); , Buenos Aires, e hills, Apr. 1930, Jack po (AJBC); hills near San Blas, Feb. 1928, Rehder 1165 a Mina Carlota, SE of Cumanayagua, le 1938, Senn Ciudad de la H Universidad de la Habana, Feb. 1925, Acuña 14301 (HAC), Mar. 1906, van Hermann 2677 (HAC). Guantánamo: coa, entre boca de Jauco y Monte Cristo, May 1968, Bisse & Köhler 8053 (HAJB, JE). Holguín: Julio A. Mella, Pinares = come alto de la Estrella, May 1983, Bisse et al. s.n. (HAJ e la Juventud: camino de Cayo Piedras a Punta hs Este, s: 1980, Alvarez de Zayas et al. 41947 (HAJB); rm — Punta del Este desde Cayo Piedras; Apr. 1974, Beraza Pinos, en ge camino de Cayo Piedra a Ponin del pe May 1975, Lippold et al. 26187 (HAC, HAJB). La Laguna de Ari abo at the edge of Río E low forest, ve 1922, Ekman 13742 (NY, S, cm San Antonio de Los Baños, May 1915, León & Alcine 5029 (GH, HAC, HAJB, = Us, 5200 (HAC). Matanzas: coral-rock cliffs, valley of imar, Mar. 1903, Britton et al. 446 (HAC, N del Río: Consolación del Sur, pineland hills at Juan Moreno, Apr. 1920, Ekman 10871 (NY, S, US); Sierra — los Organos, gtupo del Rosario, in the desfiladero de Rio S Cruz on steep limestone rocks, Mar. 1923, Ekman 16405 (S; Cabo San ntonio, Expedición Ira Bot. Nacional Jardín 5136 (HIPR); uanahac. i 4718 (HIPC); carretera que v va al y primer “Fitalia, Gusnsha- cabibes, Mar. 1989, Méndez & Verdecia 4843 (HIPC); cerca Faro, Cabo San Antonio, de 1924, Roig 3249 (HAC, NY); cerca del faro, Cabo de San Antonio, Apr. 1924, Roig 8548 (HAC). Saneti Spi : en la cresta del dics Potrerillo, Apr. 1959, die 6700 (HAC, HAJB); falda S de las Lomas de "rd Nov. 1975, de Zayas et al. D (HAJB); S de i. lomas de Banao, Areces et al. 45158 (HAC), DATEI a ta Volume 97, Number 1 2010 raham Revision of Ginoria (Lythraceae) HAJB 28787 (HAC); La Sabina Potrero del Consejo Area Protegida El Naranjal, Lomas de Banao, Mar. 1993, Béquer 303 ST ee mogote, camino a El Naranjal, Area Protegida El Naranjal, Banao, Aug. 1994, Béquer et al. 6661 (HACC); Trinidad Mtns., dm Grande to Trinidad on ridge, Mar. 1910, Britton & Wilson 5474 (NY, US); Trinidad, Río Tayaba, rocky bank, Mar. 1910, Britton et al. 5560 (NY, US), 5577 (NY, Jus) Río Sen Juan on cliff, Mar. 1910, Britton et al. 5858 (NY), 5900 (NY, US), 5903 (NY, US); Topes de Collantes, ogote Mi Retiro, base de la loma, May 1999, Castafieda & Vera 6837 (HPVC); in the foothills on the rd. from Trinidad to San Juan de Letran, Mar. 1924, Ekman 18919 (S); mtns. of the Siguanea-Trinidad group, Pico Potrerillo, on the top of this mtn., Mar. 1924, Ekman 18966 (S); Pico Potrerillo, Apr. 1987, Noa et al. 1453 TT pue Mi Retiro, al O de Pico Potrerillo, May 1990, t al. 3843 (HPVC); Topes de Collantes, a 1971, m 27224 red Río San Juan, Escambray, May 1986, Martínez & Trujillo 9020 (H IPC). Santiago de Cuba: Florida Blanca, Mar. E T e (HAC). Villa Clara: Cuabales del Escambra Clara, Apr. 1954, Alain 3965 (GH, HA de Pelo Malo, - 1979, Alfonso et al. 153 "e Santa Clara city, palm barren, Mar. 1910, Britton et al. 6083 (N Mar. 1911, eei & Cowell 10188 (NY); Santa Clara city at a brook, Apr. 1922, Ekman 14052 (NY, S); Santa Clara city, in charrascales along brooks, Mar. 1924, Ekman 18824 (NY, S, US); Santa Clara, La Cumbre, Mar. 1924, Ekman 18973 (S); Santa Clara, El Playazo, Area Protegida Cubanacán, a 1 km el restaurante “La Parrillada" en el Centro Recreativo Arco Iris, Mar. 2003, ven 1136 (HAC, MO); 10 km S of Santa Clara in wet ravines in serpentine area, July 1950, Howard et al. 122 (^, AJBC); bois of Río Primero, near ar a Clara, Mar. 1934, m 16076 (GH, HAC, NY, US); Santa Clara, Corojito, Feb. 1997, Matos et al. FF 590 (HPVC); Olla, panteaguas desde e casa a Copey, Feb. 2000, Matos FF 1725 (HPVC) La Hoya, May 1983, Noa et al. 427 (HPVC); La Hoya, Santa Clara, May 1984, Noa et al. 560 (HPVC); alrededores de la presa — June 1 1985, Noa = (HPV ino de Las Clavellin i wd ion, Noa & Castañeda 3933 (HPVO: te Cli -£ T 1991. Noa 4095 (HPVC); med Cuchilla, E penam June 1987, A. Pérez 244 (MNHNC). 7. Ginoria glabra Griseb., Cat. Pl. Cub. 106. 1866. TYPE: Cuba. “Cuba or.,” C. Wright 2544 (= 91) (lectotype, designated by Echevarria & Graham, GOET!; isotypes, A!, GH [2]!, GOET!, HACI, MO!, NY!). Figure 25. montana Britton & P. Wilson, Bull. Torrey Bot. Club 50: 43. 1923. TYPE: Cuba. Granma/Santiago de Cuba: "Sierra Maestra, Oriente," farallón Regino, Alta Maestra, 24 July 1922, León 11009 ead with E. K. Ekman 14614] (holotype, NY!; isot GH!, HAC». Small shrubs 1-2 m; stems with ascending branches, glabrous; nodes unarmed. Leaves with petioles 2-6 mm; blades ovate-oblong or ovate- M 20-90 x 7-35 mm, coriaceous, glabrous, green and shining adaxially, paler duris base acute to rounded, apex acuminate-obtuse or merely obtuse, margin thickly membranous, intramar- ginal vein present, 0.5-3 mm inside the margin at widest leaf diameter or sometimes partially merging with the margin on smaller leaves, secondary bem in 5 to 10 pairs, subhorizontal to ascending, te veins obscure, thick, yellowish, densely re dta Inflorescences 1- to 3(to 6)-flowered brachyblasts, 3— 25 mm, subumbelliform, some flowers also solitary in the axils of the main stem leaves; pedicels (9-)16- 24 mm, slender, erect or lax; bracteoles ca. 2.5 mm, broadly ovate to spatulate. Flowers 6-merous, globose to obovoid in bud, campanulate at anthesis, membra- nous, 6-9 mm, 5-7 mm diam. at the floral cup margin, contracted to a stout epipodium 0.5-1.5 mm or epipodium absent; floral cup 3-3.5 mm, gree sepals 2.5-4 X € mm, propr deltate, pente to mostly SUULISI Jefl continuous flange 0.3-0.4 mm aie, encircling the exterior of the floral cup at the base of the sepals, slightly broadening at each sinus to form a small lobe ca. 0.5 mm wide; petals 6, obovate, 11-20 X 8.5- 11 mm including claw 1-1.5 mm, rose-purp urple; stamens 28, inserted 1-1.5 mm below the sinuses of the sepals, on the distal edge of the narrowly free margin of the inner tissue layer, exserted, filaments 3— 4 mm, anthers ca. 1.7 mm; ovary 4- to 5-locular, slightly depressed, shallowly 6-sulcate, green; style ca. 7 mm, exserted. Capsule globose, exsert rted ca. 2 mm; seeds 0.8-1 X ca. 0.2 mm, compressed, obovate to oblong-elliptic. Distribution. Ginoria glabra is endemic to south- eastern Cuba, occurring in the provinces of Granma, Santiago de Cuba, and Guantánamo (Fig. 26). It grows in gallery forests, montane rainforests, and on rocky slopes in coastal matorrral between 10 and 500 m. Phenology. The species has been collected in flower and fruit in July and August. Flowering possibly begins in May or June, and fruits persist into the next flowering season. Common names. Clavellina de ón, cuaresmilla de paredón (León & Alain, 1953; Roig y Mesa. 1963). Discussi Diagnostic features of Ginoria glabra include: sien nodes, petiolate ovate-oblong or lanceolate leaves with an obtuse apex that is often rous flowers with a number were collected at Potosí in October a = the pebbly bed of the [Yateras] Pus? "e 2 localities ca. 20-30 km north no Guantánamo. According to Howard, orrespondence e from Gray to Grisebach (Howard, 74 Annals of the Missouri Botanical Garden 1Omm 5mm * Figure 25. Ginoria glabra Griseb. —A. Habit (Ekman 14614, S). —B. Leaf, abaxial view (Ekman 14614, S). —C. Flower (Ekman 14614, S). 1988: appendix 3), the Yateras District was *in the elevated district back of Santa Catalina de Guantá- namo where the collector's [Charles Wright's] princi- farallón La Perla, at Monteverde, Guantánamo, which is probably in the type area. The type of Ginoria montana, León 1 1009, was collected on the steep rocky slopes of Loma Regino to the west of Pico Turquino and ca. 200 km west of the type area of G. glabra in Guantánamo Province. Ginoria montana differs from G. glabra only in having leaves with slightly denser, yellowish tertiary veins and a more acute leaf base. Flowers on the type of C. montana are immature but display the same undulate encircling epicalyx as G. glabra. Mature flowers and leaves on Seifriz 1046 from the southern slopes of Pico Turquino in the general type area of G. montana compare favorably with those of G. glabra. The Volume 97, Number 1 2010 Graham Revision of Ginoria (Lythraceae) Figure 26. Distribution of Ginoria glabra Griseb. differences between G. glabra and G. montana, as far as they are presently known, do not justify recognition of two species. Seeds distributed as G. glabra, Fairchild. Tropical Garden FG-1753C, originating from the Botanical Garden, University of Havana, Cuba, were used for chromosome counts (Tobe et al., 1986) and molecular analyses (Graham et al., 2005). This collection is now correctly identified as G. americana Jacq isi specimens examined. CUBA. Granma/San- € Cuba: Sierra Maestra in steep rocks of Loma Regino. July 1922, Ekman 14614 (NY, S). G : y Monte Cristi, Bisse s.n. E : 2 (GH, HAC. NY, US); banks of Río Mino, Maise [Maisí], Oct. 1938, e 18571 (GH, HAC, NY, US); Río Mayo, Maisí, Oct. 1938, Matos 18571 (HAC); farallón La Perla, Feb. 1911, hale 8784 TH NY, US). Santiago de Cuba: línea antigua de Firme guadores, Santiago, Nov. ls yrs 4872 (HAC); Sierra Maestra, July 1922, León ); Pico Turquino, S slopes, July 1940, Seifri 1046 (US). rqu pes, July ifriz 8. Ginoria jimenezii Alain, Brittonia 20: 157. 1968. TYPE: Dominican Republic. “In woods, very rare, Jaiqui Picao [Jaiqui Picado], Santiago Prov., Jul. 1954," F. Jiménez 2684 (holotype, US!; isotype, US!). Figure 27. Small trees 4-15 m; stems glabrous; nodes unarmed. Leaves with petioles 1-2 mm; blades narrowly elliptic-lanceolate or oblong, 20-68 X 8- 29 mm, thickly membranous, glabrous, opaquely green and somewhat pr. adaxially, paler and yellowish green abaxially, base acute, apex obtuse, often with a mucronate tip, margin membranous, intramarginal vein usually present, 1-2 mm inside the mg at widest leaf diameter, secondary veins in ca. 10 pairs, ascending, rates d veins obscure, finely. reticulate. In, cemose, flowers solitary or paired in A. axis of is leaves; pedicels 15-35 mm, os lax; bracteoles 1-1.5 mm, subulate. Flowers 4-merous, subglobose in bud, campanulate at res thickly coriaceous, 8-9 mm, a m diam. at the floral cup margin, contracted to an epipodium 1-3 mm; floral cup 3—4 mm, green; sepals 3-4 X 2.54 mm, deltate, esa a at anthesis; epicalyx absent, the sinuses of the sepals sometimes slightly thickened; petals 4, oblong- obovate, 12-17 X 8-11 mm, violet; stamens 16 to 24 (possibly more), inserted ca. 2-3 mm below the sinuses at the distal margin of the inner tissue layer, filaments 6-7 mm, anthers ca. 1.6 mm; ovary 4- ocular, green; style 6-10 mm, exserted. Capsule globose, probably included; seeds unknown. ion. Ginoria jimenezii is — to the Res Republic, occurring in the em provinces of Santiago and Espaillat in n ds and along the margin of an arroyo with Mora Benth., Manilkara Adans., Tabebuia Gomes ex DC., Vitex L., and Eugenia L. at elevations of 60-520 m (Fig. 19). Phenology. The flowering and fruiting period of this api is eer pasty » is — April-July. in June and July and one ve flowering collection was made in September. Discussion. This rare species is recognized by the combination of unarmed nodes, elliptic-lanceolate or Annals of the Missouri Botanical Garden = =s Figure 27. Ginoria jimenezii Alain. —A. Habit ( Y E SAR., £ oblong leaves to 68 mm long, and solitary thickly coriaceous flowers that lack an epicalyx. It is known at the present time from a single apparently sterile tree at the site near Gaspar Hernández. Botanists from the National Botanic Garden in Santo Domingo who have made several visits to re-collect the species have not found the tree in flower. Additional specimens examined. DOMINICAN REPUB- HIC. : 8.5 km al E de Gaspar Hernández, Jan. 1992, García & Jiménez 3614 (JBSD, MO); 8.5 km al E de Gaspar Hernández, 800 m al S de la carretera, en la del arroyo El Guano, Mar. 2001, Garcia & Pimentel 7411 938, (JBSD). iago: Manacla, en vera arroyo, Sep. 1 Canela L. s.n. (NY, US). 4-merous, 9. 5 ` = = Garcia & Jiménez 3614, MO). —B. Flower. —C. Petal (B, C from Canela Ginoria koehneana Urb., Feddes Repert. Spec. Nov. Regni Veg. 18: 20. 1922. TYPE: Cuba. Guanta » "in parte centrali-septentr. prope San Germán in sylvis rarissima, m. Aug. fruct.," S Aug. 1915, E. L Ekman 6356 (lectotype, designated by Graham, 2005: 301, NY!: isotypes, S!, US!). Figure 28. Cinoria thomasiana Alain, Revista Soc. Cub. Bot. 10: 30. abales de 1953. TYPE: Cuba. Pinar del Rio: “Cu J Cajálbana, Junio 10, 1950,” J. B. Acuña & Bro. Alain 16182 (holotype, HAC! [transferred from SV]. Small trees to 3 m; stems much branched, the branches short with abbreviated internodes 3-20 mm Volume 97, Number 1 2010 Graham 77 Revision of Ginoria (Lythraceae) Ginoria koehneana Urb. —A. Habit. —B. Leaf, abaxial view. — C. Flower in fruit with dehisced capsule. A-C Figure 28. from Ekman 6356 (S). long, glabrous; nodes armed by 4 strong, horn-like spines of 1-2 mm, the spines recurved, spreading, or slightly erect, or (in Pinar del Río) spines sometimes much reduced or absent. Leaves sessile, crowded toward the tips of the stem; blades obovate to suborbicular, less often oblong-elliptic or elliptic, 10-25 x 5-20 and mm, coriaceous, green shining adaxially, opaque abaxially, base sharply acute, apex obtuse and often apiculate, margin white- cartilaginous, in inal vein present, 0.2-1 mm inside the margin at widest leaf diameter, secondary veins in 8 to 10 pairs, acutely ascending, tertiary veins thick, obscure. Inflorescences l- to 9-flowered brachyblasts, loosely subumbelliform, some flowers Annals of the Missouri Botanical Garden Figure 29. Distribution of Ginoria koehneana Urb. also solitary in the axils of the main stem leaves; pedicels 6-17 mm, thin, lax; bracteoles 0.3-1 mm, lanceolate-linear. Flowers 4-merous, globose in bud, shallowly campanulate at anthesis, thickly membra- nous to coriaceous, 3-4.5 mm, ca. 4 mm diam. at the floral cup margin, abruptly contracted to a slender epipodium ca. 1 mm long; floral cup 0.7—1, green; sepals 2-3.5 X 1.5-2 mm, narrowly deltate with short acuminate lip, erect to slightly spreading at anthesis; epicalyx absent; petals 4, ovate-triangular or oblong, 2.5 X ca. 2 mm including a claw ca. 0.5 mm, scarcely exceeding the sepals, White; stamens (12 to)1 4 to 16, inserted ca. 0.5 mm below the sinuses aleng the distal margin of the inner tissue layer, included to scarcely exceeding the sepals, filaments 0.5—0.8 mm, anthers ca. 0.5 mm; ovary 2- to 3-locular, green; style ca. 3 mm (fide Urban), included or short- exserted. Capsule globose, included; seeds 0.5-0.7 x ca. 0.1 mm, compressed, obovate or oblong-elliptic. Distribution. Ginoria koehneana is endemic to Cuba, appearing disjunctly in northwestern and north- easter Cuba, in the provinces of Pinar del Rio, Las Tunas, Holguin, and in central Guantanamo (Fig. 29). t grows on rocky serpentine and limestone soils in semi-deciduous woods and in xeromorphic matorral inland of mangroves near the coasts at 0—100 m. Phenology. | Ginoria koehneana has been collected in flower from June through August, and fruits are present on specimens collected in August. Common names. Yema de huevo, guairaje espi- noso (León & Alain, 1953; Roig y Mesa, ). Discussion. Ginoria koehneana is a large, much- branched, spiny shrub or small tree with thickly coriaceous leaves crowded on short secondary branches. It is typically armed by strong, short spines, although spineless specimens have been noted in northwestern Pinar del Río. Flowers are 4-merous, small for the genus, and mostly fall away with their slender epipodium soon after flowering. Few collec- tions have been made and where the species grows, collectors have noted its rarity. We found a single sterile tree with new leaves in a dense inland thicket on Serpentine rocks adjacent to mangroves at Puerto Padre, Las Tunas, in the month of March, but on two occasions were unable to relocate the species at former collection sites in northwestem Pinar del Rio. The close floral similarity and probable sister relationship to G. arborea are noted under that species. The holotype of the westem Cuban Ginoria thomasi- ana has ascending, slightly incurved spines and elliptic leaves, whereas another western collection, Ekman 17406 (NY), has no spines and obovate leaves. Ginoria koehneana from eastem Cuba has descending, slightly recurved spines and mostly obovate leaves. Variation in spine development and leaf shape has been documented in a far more commonly occurring species, G. americana, so that such variation in G. koehneana is not unique to the genus. Given that G. koehneana and G. thomasiana have identical flo d allowing for variation of spine position and leaf shape, the two species are considered conspecific, a conclusion the author of G. thomasiana subsequently reached (Liogier, 1969: 114). Additional spec examined. CUBA. Guan : San Germán in forest, laterite on limestone, Aug. 1916, Ekman 7428 (NY, S, US). Holguín: Loma del Templo, al Ode la bahía del Naranjo, Oct. 1978, Bisse et al. 38193 (HAJB). Las Tumas: Jesús Menéndez, Las Resbalosa Saya, Oct. 1991, Brull & Verdecia 5432 (IPTH); La Saya, Puerto Padre, Feb. 1930, Curbelo 206 (HAC); coast at La Volume 97, Number 1 2010 Graham Revision of Ginoria (Lythraceae) Resbalosa, Puerto Padre, Aug. 1930, Curbelo s.n. (NY); La a La Saya, Puerto Padre, July 1932, Curbelo 229 C, NY); proximidades de Puerto Padre, June 1932, d 24166 (HAC, HAJB); Playa Cobarrubias, ca. 100 m from Hotel Cobarrubias at the intersection of the main rd. to the playa and the rd. to Antiguo Rancho, Mar. 2003, Graham 1142 (FTG, HAC, MO); La Isleta Manatí, matorral xeromorfo costero, May 1995, Verdecia "ge PTH). del Río: La Cajálbana, Dec. 1949, Acuña & Alain 8997 (HAC); cuabales de Cajálbana, Dec. os, Acuña « Alain — (HAC); cuabales serpentinosos, Loma de la Cajál Palma, Dec. 1949, Alain & dis 1203 (GH, HAC); M Morrillo, Taseuna, Cayo Alfiler, al final del cuartón de Las Carabelas, Mar. 1987, Colaboradores del Flora de Cuba 62522 (HAJB); Finca Toscano, Bahía Honda, Mar. 1987, Méndez 3302 (HIPC); Finca Toscano, Bahía Honda, Aug. 1986, Olviedo & Delgado 3149 (HAC, HIPCR); Toscano [finca near Playa el Morillo], in manigua bordering on ares, a tree, very rare, Sep. 1923, Ekman 17406 (NY, S). 10. Ginoria lanceolata O. C. Schmidt, Ark. Bot. 21A(5): 16. 1927. TYPE: Haiti. “Peninsula id. prope Port-de-Paix ad Saline id. versus, mense Aug. 1925,” E. L. Ekman 4575 (lectotype, designated by Gra- ham, 2005: 301, NY!; isotypes, EHH not seen, GH,, S [2]!, US [2])). Figure 30. Small trees with deeply furrowed bark, height unknown; stems with short terminal branches and internodes, glabrous; nodes armed by (2 to)4 spines, the spines slender, spreading or slightly ascending, 2— 4 mm, tips straight or slightly recurved. Leaves with petioles to 1 mm; blades narrowly ovate-lanceolate to lanceolate, 10-25 X 4-10(-15) mm, coriaceous, shining and gray-green adaxially, paler abaxially, secondary veins in 5 to 10 pairs, sharply ascending, tertiary veins obscure. Inflorescences composed 0 few solitary flowers in the leaf axils; pedicels 8- 10 mm, slender, lax; bracteoles unknown. Flowers 4- merous, obovoid in bud, campanulate at anthesis, thickly membranous, 5—5.5 mm, 44.5 mm diam. at the floral cup margin, abruptly contracted to a neri epipodium ca. 1 mm; floral cup 1-1.5 mm sepals 2.5-3 X ca. 1.5 mm, narrowly deltate with acute apex, erect at anthesis, remaining erect in fruit; epicalyx absent; petals unknown; stamens 8, inserted ca. 0.5 mm below the sinuses along the distal margin of the inner tissue layer, the 4 antesepalous stamens slightly exceeding the sepals, the 4 antepetalous ones included, filaments 3-4.5 mm, anthers unknown; ovary 3-locular, color unknown; dictis length unknown. rown, oblong, equal to or exserted ca. 0.5 mm beyond apex of the sepal; seeds ca. 0.8 x 0.1 mm, compressed, obovate to oblong-elliptic. Distribution. A rare endemic of Haiti i in re ment Nord-Ouest (Fig. 31), lanceolata i known from the type and one other collection. Both collections are from limestone terraces at ca. 50 m. Phenology. Ginoria lanceolata has been collected in flower and old fruit in March; the sterile type collection was made in August. Discussion. The collections made in 1925 and 1928 by Ekman remain the only known examples of the species. Flowers and fruits of Ginoria lanceolata are described here for the first time from the sparsely flowered Ekman 9696, the type number being sterile. The species uniquely combines slender, spreading nodal spines, lanceolate leaves 25 mm or less with sharply ascending secondary veins, and a margin formed by the intramarginal vein. The = is distinctly xeromorphic. Ginoria lanceolata is most similar to G. arborea, a species restricted to extreme southeastern Cuba, which differs by linear-oblong, not ovate-lanceolate to lanceolate, leaves and 12 to 14 stamens versus eight in G. lanceolata. In the protologue, Schmidt compared leaves of G. lance to the dissimilar leaves of G. koehneana, which are typically obovate with a distinct intramarginal vein. The flowers of G. lanceolata, however, are similar to PE of G. koehneana and G. arborea; all are 4- merous and among the smallest in the genus. Egal the three species also share the same pecialized habitat type, growing on limestone in coast ei areas. It is remarkable that in extreme northwestern Haiti, Ginoria is represented by three narrowly endemic species of very different morphology, and unfortunate that all are rare or conceivably now extinct. Ginoria pulchra was rediscovered on a precarious cliff side at its type locality in 1985 (Zanoni et al. 33439), but neither G. lanceolata nor G. callosa has been re- collected since Ekman found them in the 1920s. There is hope that inacessibility to the steep limestone cliff habitats of the latter two has preserved them, as it did for G. pulchra, at least until 1985. Additio: imens ined. HAITI. N E Presque ile du Nord-Ouest, Port-de-Paix, limestone terraces W of Saline-Michel, Mar. 1928, Ekman 9696 Ginoria nudiflora (Hemsl.) Koehne, Bot. Jahrb. Syst. 3: 351. i Basionym: Antherylium nudiflorum Hemsl., . PL Nov. Mexic. 1: 13. 1878. TYPE: E Oaxaca: “Sierra San Pedro Nolasco, Talea, ete., " C. Jurgensen 956 (holotype, K!; isotypes, G!, K!). Figures 1, 32. Ginoria davisii M. C. Johnst., Southw. Naturalist 1: 39. 1956, syn. no v. TYPE: Mexico. Veracruz: “about 40 mi north 11. Annals of the - Missouri Botanical Garden 2mm C Figure 30. of Chachalacas,” 29 Mar. 1955, L. I. Davis & E. B. Kincaid, Jr. 55-8 (holotype, TEX!; isotypes, GHI, MEXU!, SMU!). Shrubs to tall trees, 5—40 m; stems glabrous; nodes unarmed. Leaves sessile or petioles to 2 mm; blades narrowly elliptic or lanceolate, 40-90 x 15-35 mm, membranous, glabrous, bright green adaxially, paler abaxially, base attenuate, apex acuminate to generally long-acuminate with acute tip, margin membranous, i inal vein present, 1.5-3 mm inside the margin at widest leaf diameter, secondary veins in 11 to 13 pairs, nearly horizontal, gradually arcuate, tertiary veins thin, obscure. Inflorescences 8- to 20- flowered brachyblasts 1-15 mm, umbelliform, rarely flowers also solitary in the axils of the main stem leaves; pedicels 4-10 mm, slender, mostly erect; bracteoles 0.8-1.5 mm, narrowly linear. Flowers 4- Ginoria lanceolata O. C. Schmidt. —A. Habit. — B. Leaf, abaxial view. —C. Flower. A-C from Ekman 9696 (S). merous, obovoid in bud, shallowly campanulate at anthesis, membranous, 5-8 mm, 3-3.5 mm diam. at the floral cup margin, green or occasionally wine-red within, gradually contracted to a slender epipodium 1-3 mm; floral cup 2-2.5 mm, green; sepals 2-3 X 3- 9 mm, narrowly deltate, erect to spreading at anthesis, ultimately strongly deflexed in fruit; epica- lyx absent; petals 4, suborbicular to narrowly obovate, (436.57 X 3-5 mm including a claw ca. 0.5 mm, pale pink to white; stamens 12 to 16 or 28 to 40, inserted 0.5-1 mm below the sinuses at the base of a freestanding collar ca. 0.5 mm wide, the collar formed by the expanded distal margin of the inner tissue layer, stamens exserted, filaments 4-6.5 mm, anthers ca. 1.5 mm; ovary 3(or 4)-locular, green, turning red with age; style 5.5-11 mm, exserted. Capsule subglobose to oblong, exserted 2-5 mm beyond the Volume 97, Number 1 2010 Graham Revision of Ginoria (Lythraceae) > . — _ 10km 18e} 72° a lanceola Ginoria pulchra Figure It Distribution of Ginoria lanceolata O. C. Schmidt and G. pulchra (Ekman & O. C. Schmidt) S. A. Graham on Hispanio deflexed lobes of the floral cup; seeds ca. 2 X 0.3- 0.4 mm, fusiform, fragile. Chromosome number: 2n — 56 (Graham & Cavalcanti, 2001). Distribution. Ginoria nudiflora is endemic to Mexico, distributed in the states of Chiapas, Oaxaca, Veracruz, and Michoacán (Fig. 33). It inhabits primary and secondary subdeciduous forest slopes and gallery forests from tall evergreen forest to coastal lowland short forest. It occurs in deep sandy soils and on limestone at elevations of 24-2733 m. P henology. Ginoria nudiflora produces flowers primarily from March through June. Flowers begin to appear in the axils of last season's leaf scars before or with the appearance of the new season's leaves, and flowering continues as leaves expand. The capsular fruits, enclosed by the dry floral cup, are persistent on pedicels from April through November. Common names. — In Chiapas, pataté, a Tzeltal name from the area of El Real, ca. 60 km E of Ocosingo; in Oaxaca, agame; in Veracruz, guayabillo (Graham, 1991). Discussion. Ginoria nudiflora is the only con- tinental species of the genus. It is recognized by the long-acuminate leaves with a strong intramarginal vein, and by the dense umbelliform clusters of white- petaled flowers that appear just before or with the new season’s leaves. In full flower, the trees attract great numbers of bees and other insects that visit for the abundant pollen (pers. obs.). Miranda (1952) de- scribed G. nudiflora as “one of the most beautifu trees in Chiapas, which has an abundance of beautiful trees.” He found it to be the dominant tree in some places along the Río Santa Cruz, Chiapas. In Veracruz, it is common for miles in low coastal, semi-deciduous short forest. It is not known whether the presence of the species in western Mexico near coastal Michoacán is a natural disjunction or possibly the result of an early introduction from coastal Veracruz through shipping. Ginoria davisii was described as a small tree with 12 to 16 stamens, whereas Koehne (1903) cited G. nudiflora as having 28 to 30 stamens. The type of Antherylium nudiflorum at Kew includes a sketch on which stamens are noted to be “sometimes nearly 40.” Extensive collections of G. nudiflora now document the typical stamen number as 12 to 16, but with occasional increases in floral merosity and stamen proliferation, as happens in other Ginoria species. Ginoria davisii thus falls within the circumscription of C. nudiflora. specimens examined. MEXICO. Chiapas: E ín. 32 km N-NW of Soyalo along rd. to opainala above Chicoasén, Mar. 1973, Breedlove 34029 (MO, NY); Mpio. Ixtapa, along the Río Laja, 5 km N of Ixtapa, May 1973, Breedlove 35078 (MO, TEX); betw. Ixtapa nzalez L. et al. s.n. (MEXU); bank Laja, on the Ixtapa-Soyalo rd. NE of Tuxtla Gutiérrez, at 5 km N of Ixtapa, Apr. 1993, Graham 1099 (MO); Mpio. Chicoasén, i tiérrez—Chicoasén, Apr. 1987, Martínez S. 20146 (MO); Santa Rita al Real, E of Ocosingo. Miranda 7138 (MEXU); erca de Banavil, al E de El Real. Mar. 1951, Miranda 7184 (MEXU, US; N de Ixtapa, Mira 7494 (MEXU) Mic án: Mpio. Aquila, 4 km camino Aquila-La Placita, Guerrero C. (ENCB); comán, Aquila, Mar. 1941 . US); Atenquique, hacia del Camalote, 26 km al NE de El Ranchito, Soto N. & Torres Annals of the - Missouri Botanical Garden Figure 32. Ginoria nudiflora (Hemsl.) Koehne. —A. Habit. —B. Flower. A, B from Soto N. & Torres C. 2849 (MO). C. 2817 (MEXU, MO); en Aquila, Mar. 1981, Soto N. & Torres C. 2849 (MO). Oaxaca: Mpio. Soyaltepec, Tuxtepec, 1 de Temazcal, camino al vertedor, Cortes 264 (MO); Mpio. Soyaltepec, Tuxtepec, 3 km al S de la Temascal, Cortes 867 (MO); Monte Mistaca[?], Mar. 1845, Galeotti s.n. (N Y, US): Chiltepec, Tuxtepec, Martínez C. 1336 (ENCB, MEXU, MO); Tuxtepec, Raffauf & Giral s.n. (ENCB); Valle Nacional, Mar. 1919, Reko 4153 (US); ux S de Reforma, ya en el (MEXU, MO, NY). Verae E opan, alrededores de La Laguna de La Mancha, orilla de manglar, Nov. 1975, Acosta/Dorantes A-640 (MO); detour to Chilapa, camino Playa Vicente a El Nigromante, Chavelas et al. ES4201 (MEXU); Dos Ríos, Mar. 1930, Mell 510 (NY. US); Montebellow, a orilla Papaloapan, Miranda 4278 (MEXU); cerca y al S de Ciudad Alemán (O. de Papaloapan), Mar. 1956, Miranda 8278 (US); orilla N de la Laguna de iérrez B. 3085, 3092, 3094 (MO); Mancha, Apr. 1988, Gutiérr l km N de La Boca de Laguna de La Mancha, Novelo 403 (MEXU, MO); Mpio. Veracruz, Neveria, carr. ant nacional Xal arindo, Apr. 1988, Gutiérrez B. 3101- La Mancha, Novelo 430 (MO); Ci Alemán, cerca de Tres Valles, Paray 1922 (ENCB, MEXU); La Granja, selva de Ginoria, Sousa 1739 (MEXU). 12. Ginoria pulchra (Ekman & 0. C. Schmidt) S. A. Graham, comb. nov. Basionym: Haitia pulchra Volume 97, Number 1 2010 Graham Revision of Ginoria (Lythraceae) MEXICO — 200 km Ginoria nudiflora @ Figure 33. Distribution of Ginoria nudiflora (Hemsl.) Koehne. Ekman & O. C. Schmidt, Ark. Bot. 21A(5): 18. 1927. TYPE: Haiti. “Peninsula septentr.-occid. in Móle St. Nicolas ad Baude Grande-Mer, in declivibus m. [3] Jul. 1925 flor.," E. L. Ekman 4448 (holotype, S!; isotypes, EHH not seen, S!, US [2]!). Figure 34. Shrubs 1-2.5 tall; stems glabrous; nodes unarmed. Leaves with petioles 2-4 mm; blades suborbicular or broadly ovate, 17-52 X 1040 mm, thickly coriaceous, yellow- to gray-green adaxially and abaxially, base rounded to shallowly acute, apex obtuse, frequently with a small mucro, margin thick, intramarginal vein present, ca. 1 mm inside the Pan. widest leaf diameter, secondary veins in 3 to " es shallowly ascending, secondary and tertiary veins thickened, coarsely reticulate, pale yellow. Inflorescences 1- to 3(to 5)-flowered highly reduced brac yblasts in the axils of the main stem leaves; pedicels 15-28 mm, sturdy, erect; bracteoles 1.4— 1.7 mm, ovate-elliptic, coriaceous. Flowers 6-merous, subglobose in bud, shallowly campanulate at anthesis, CRO, 11-12 mm, 10 mm diam. at the floral cup magin, contracted below the ovary to a short, stout epipodium 1-2 mm; floral cup 6-7 mm, green; sepals 4-5 X ca. 5 mm, deltate, the lobes rolling outward, spreading to strongly deflexed in fruit, encircled on the inside of the floral cup by a raised ring of tissue; epicalyx a continuous, slightly undulating, thickened flange 1-2 mm wide, encircling the exterior of the floral cup at the base of the sepals; petals 6, obovate, "es 14 X 11 mm, intense rose, violet-purple, or white with pinnate veins purple (Leonard & Leonard 13168); stamens 24 to 27, inserted 1.5-2 mm below the sinuses of the sepals on the distal edge of the narrowly ree margin of the inner tissue layer, exserted, filaments 6-10 mm, anthers 2-2.5 mm; ovary 6- locular, slightly depressed, 6-sulcate, green; style 8- 11 mm, exserted. Capsule included, reaching the margin of the floral cup; seeds 0.8-1 X ca. 0.3 mm, compressed, concave-convex, obovoid to oblong- elliptic. Endemic to Haiti, Ginoria pulchra is known only from the type area on the extreme northwestern coast (Fig. 31), growing on calcareous terraces and palisade cliffs above the sea in an arid, cactus desert-like zone at 100 m. Phenology. The species flowers and fruits from February to July, with peak flowering probably in February and Marc iscussion. Ginoria pulchra is immediately dis- tinguished from all other species of the genus by the thick, yellowish to gray-green, suborbicular leaves. lt shares with G. buchii in Haiti and G. glabra in Cuba morphological features of the genus: an epicalyx encircling the exterior of the floral cup, and stamens 4 or more in number. Ginoria pulchra is a rare, critically endangered species due to the extensive destruction of natural vegetation in Haiti (Sergile & Woods, 2001). Zanoni, collecting in 1985 in the type area, found the plant growing from the side of a liff in an area otherwise decimated by oal makers. Hopefully, the species has survived there due to the near inaccessibility of the site. Ekman, in field notes on the holotype. wrote that the species was collected on the steep ascent of the Annals of the Missouri Botanical Garden 2cm Second terrace at Baude Grande-Mer and that it occurred at similar localities at Bap à Foux. Additional s ns examined. HAITI. N Vic. of Móle St. Nicolas, arid plateau of Cap du 929, nard en la carretera costera a Jean-Rabel, Feb. 1985, Zanoni et al. 33439 (GH, MO, S). 5mm B Figure 34. Ginoria pulchra (Ekman & O. C. Schmidt) S. A. Graham. —A. Habit. — B. Flower. A, B from E. L. Ekman 4448 (S). 13. Ginoria rohrii (Vahl) Koehne, Bot. Jahrb. Syst. TYPE: Virgin Islands [U.S. Virgin Islands]. St. Croix: “HB Vahlii ex Insula St. Crucis, mis. Dr. von Rohr” (lectotype, designated by Graham, 2005: 298, C digital image!; isotype, C digital image!). Figures 1, 35. eser eM s wet tappe este SI PvP Stati esc een ea EEG CO eS tn ie eee qe. Volume 97, Number 1 2010 Graham Revision of Ginoria (Lythraceae) Shrubs or small trees to 7 m, slender trunk to ca. 1 dm DBH; stems glabrous, young stems 4-angled or 4- winged; nodes armed by (2 to)4 spines 1—4 mm, the spines robust, incurved to erect. Leaves decussate, tioles 1-3 mm; blades broadly glabrous and shining adaxially, paler , base acute, rarely rounded, apex obtuse, sometimes also slightly mucronate, margin membranous, intramarginal vein present, 1-3 mm inside the margin at widest leaf diameter, secondary veins in 8 to 11 pairs, sharply ascending, tertiary veins obscure. Inflorescences 2- to 8-flowered highly reduced brachyblasts, flowers also solitary in the axils of main stem leaves; pedicels 4-13 mm, slender, lax; bracteoles 0.2-5 mm, linear. subglobose in bud, shallowly campanulate at anthesis, thin, membranous, 6.5—7.5 mm, ca. 3 mm diam. at the floral cup margin, abruptly contracted below the ovary to a slender epipodium 0.5-2 mm; floral cup l- 1.5 mm, green; sepals 3.5-5 X 2.2-3 mm, narrowly deltate, erect to spreading; epicalyx absent, the margin of the sinuses sometimes slightly thickened; petals 4, obovate-orbicular, 7-7.5 X mm including a claw 0—0.5 mm, slightly exceeding the sepals, white; stamens 12 to 16(to 20), inserted ca. 0.5 mm below the sinuses of the sepals along the distal margin of the inner tissue layer, exserted, filaments 9-13 mm, subequal, anthers ca. 2 mm; ovary 2- to 4-locular. Capsules oblong, reaching the apex of the sepals; seeds ca. 2.5 X 0.3 mm, narrowly fusiform, fragile. Chromosome number: 2n = 56 (Graham & Cavalcanti, 2001). Distribution. Ginoria rohrii is distributed in Puerto Rico, especially on the eastern and southern coasts of the island, on Vieques Island, and in the Virgin Islands on St. Croix, St. John, St. Thomas, e Guana Island, and Virgin Gorda (Fig. 36). In curs in dry coastal forests and thickets, on rocky bie on seasonally flooded ground, and in coastal sands fro Phenolo, Ginoria rohrii flowers from February to May, with the flowers appearing before the leaves. Flowers and fruits appear intermittently at other times, the old flowers and pedicels often being retained into the next season. lowers 4-merous, aoe names. Rosa de ciénega, ucarillo, cer- n Puerto Rico, serrazuela; in Tortola, sugar-an (Little et al., 1974). Discussion. This easternmost species of Ginoria is a spiny shrub or small tree primarily of upland, dry, spiny coastal thickets but is occasionally also found in brackish, flooded low woodlands. The unique combi- nation of characters defining G. rohrii includes broadly elliptic to obovate leaves with a prominent intramarginal vein, two or four stout nodal spines, and 4-merous, deeply lobed flowers with white petals. The species was cited from Haiti by Mayerhoff and Eggers (Liogier, 1986), and as an introduction to St. Vincent (Koehne, 1882, citing Eggers as the source). I have not been able to verify these citations. A specimen of G. rohrii (Eggers 3307”, US) labeled “Santo Domingo” is doubtfully from there; the collection number is out on the label and the specimen is aci very similar to Eggers 307 (GOET) from Puerto Rico. Ginoria rohrii has also been recorded Bu the Dominican Republic based on a misidentification (Canela L. s.n., US) of the rare G. jimenezii. There is no sound evidence that G. rohrii was ever part of the flora of Hispaniola. jardo: Bo de San Juan, Nature Reservoir Headland, Mar. 1994, Axelrod 7608 (NY, UPRRP); "see soil near Salinas, Apr. 1993, N. L. Britton & E. G. Additional specimens examined. E RICO. Fa- abezas, Cabezas irre, su n et al. 60. 4 (N Y); Playa de Fajardo, Mar. Cabeza de J 954. Little 16427 (NY, US); Sabana gars ar. 1935, Sargent 202 (US); prope Salinas rae in sylvis ote Feb. 1885, Sintenis Es A. GH, GOET, US); Pt. Fajardo ad litora maris, Apr 1885, Sintenis = (A); = May 1885, Sintenis 1595 (JE, MO, NY, S, US); rope Guanica in sylvis ad Lagunam, Fe 1886, Sintenis 5836 (GH, EN prope Naguabo in sylvis litoralis ad 886, Sintenis 5486 (GH, MO, NY, S. e 1407 (A, CM); Punta Fajardo, dryland thickets near the lighthouse, Mar. 1966, Wagner 988 ( CM, MO). Vieques: and, dirt rd. a ie. i i Lagoon and sea, s.n. (MO); just NE of Laguna Kian ni, i, Sep 53 48846, 49271 (MO) s. loc., Jan s. loc., Woodbury s.n. (MO). mein ae I-land: P. Palm Ghut, iex 1987, Proctor 43473 (NY from "Moravian church, June 1985, Aceve (NY); East End Quarter, E of Southside Pond, Aug. 1987. Acevedo R. et al. 1827 (NY); Cob Gut, Jan. 1990, Acere nd Qu arter, es Line L 1992. North coastal 940, ridgi 121 (A. A. NY, rima loc., Feb. 1906, Raunkiaer s.n. FS); San Annals of the Missouri Botanical Garden Ginoria rohrii (Vahl) Koehne. —A. Habit. —B. Axillary inflorescence and nodal spines. —C. Flowers. A-C Figu from E, kasies 307 (JE). [sic] Thomas, 1827, Wyder 46 (NY). Tortola: Fish Bay to oad Town, Brüton & Shafer 906 (NY, US); Fort Hill (Baughen Bay), cliffside belo coastal hills, Little Dix Bay, nal. 219 (NY); s. loc., Jan. 1919, Fishlock s.n. (US); s. loc., June 1969, D 23812 (NY, d s. loc., Woodbury s.n, (MO). loc Canis et Porto-Rico, Mi -— cem Mh Dr. West s.n. (C [Hb. Vahlii] digital ExctupEp NAMES oe enema: (Kunth) Spreng., Syst. Veg. 475. = Adenaria floribunda Kunth. New giis (Kunth) Spreng., E Veg. 2: 475. 1825. — ria floribunda Kun Antherylium pur E Spreng., ik Veg. 2: 475. 1825. — Adenaria floribunda Kunth. Ginora L., Sp. PL s. E 642. 1762 [and numerous l subsequent authors Volume 97, Number 1 2010 Graham Revision of Ginoria (Lythraceae) PUERTO RICO —— E Ginoria rohrii @ Figure 36. Distribution of Ginoria rohrii (Vahl) Koehne in Puerto Rico and the Virgin Islands. Orthographic variants exist for Ginoria. Index Kewensis 2.0 lists a number of species employing the orthographic variant: Ginora americana L., Ginora curvispina Koehne, Ginora diplusodon Koehne, Ginora glabra Griseb., Ginora nudiflora Koehne, Ginora rohrii Koehne, and Ginora spinosa Griseb. The names attributed to Koehne (Bot. Jahrb. Syst. 3: 349-351) and Grisebach (Cat. Pl. Cubens. 106) are not present in those publications. Gi i noria americana Griseb., non Jacq. in Koehne, Pflanzenr. (Engler) IV. 216: 249. 1903. j noria americana Griseb. is a misidentification for - spinosa Griseb. and G. curvispina Koehne Ginoria Sesse & Mog. ex DC., Prodr. 3: 89. 1828. Pro _ = Heimia Link. Ginoria flava Sesse & Mog. ex DC., Prodr. 3: 89. 1828. Pro syn. = Heimia salicifolia Link. Ginoria syphilitica Sesse & Mog. ex DC., Prodr. 3: 89. 8. Pro syn. = Heimia salicifolia Link. Literature Cited Baas, P. 1986. Wood anatomy of Lythraceae—Additional genera (Capuronia, Galpinia, Haitia, a and Pleur ophora). Ann. Missouri Bot. Gard. 73 — —— & R. C. V. J. Zweypfenning. im od anatomy of E Acta Bot. Neerl. 28: 117-1 1, A. . Phytogeography and Vegetation Ecology of E Cuba. Akadémiai Kiadó, itus T ba nggs, B. G. & L. A. S. Johnson. -~ Evolution = the és Evidence from inflorescence structure B n. Soc. New South Wales 102: 157-256. be N. L. 1912. The genus Ginoria in Cuba. Bull. Torrey . Club 39: 12-14. Brown, L. R. 2006. Plan B2.0: Rescuing a Planet Under KP ERA in Trouble. W. W. Norton & Co., Cevallos-F erriz, S. R. S. & R. A. Stockey. 1988. Permineralized . L (Mili, E ` a.f British Columbia: DL . Canad. 2 e 66: 303-312 Corner, E. J. H. 197 6. The Seeds of Dicotyledons, 2 vol. voi ie Press, Cam wie ik 37, 176-177.] Dahlgren, R. € R. F. Thome. 1984. The order Myrtales: en variation, and relationships. Ann. Mis- souri Bot. Gard. 71: D'Arcy, W. G. waq Jacquin names, some notes on their typification. Taxon 19: 554—560. 1987. A rapid DNA yoy leaf t Doyle, J. J. & J. L E rocedure for small quantities of fresh .&S. ep. Cuba, = A. Pl. Vasc. 14: 1-52. The gen method. A revised a Bot. Ti E 985. Confidence limit on phylogenies: An i 191. -— y 3 Fritsch, P. 'W. 2001. m and biogeography of the flowering plant genus St (Styracaceae) based on chloroplast DNA restriction sites and DNA sequences of the esa transcribed spacer region. Molec. Phylogen. Evol. 19: 387 ———. 2003. pen geographic origins of Antillean Styrax. Syst. Bot. 28 421-430. dice A CTS NA McDowell. phy ^» phylogeny of Caribbean cites oO a Syst. 28: 376-377 raham, A A. 2003a. Historical Do of the Greater Antilles. Brittonia ies 351-383 — iy tole and Cenozoic € cen region. Syst. Bot. 28: 3 e Nowicke, J. J. Skvarla, S. A. Graham, v. e und & Palyno = and — of the onment S. Lee. 1985. — . I. Introduction and ge through Ginoria. mex: J. Bot. I im . 1987. puya ii systematics of the Lythraceae. II. Genera Haitia through Peplis. J. Bot. 74: Annals of the Missouri Botanical Garden , S. Graham, J. W. Nowicke, V. Patel & S. Lee. 1990. Palynology and — of the Lythraceae. III. Genera Physocalymma thro hs da addenda, and con- clusions. Amer. J. Bot. 77: 1 Graham, S. A. 1989 eus 426-440 in R. A. n (editor), Flora of le tae Antilles, a 5: Harvard University, Jamaica Plain, D n Pp. 1-94 in A. Gómez-Pompa (editor, ad E Instituto de Ecología, A. C., Xalapa, Veracruz, Mexico. ———. 1995. Innovative "d morphology in Lythraceae. Amer. J. Bot. 82(Suppl.): 132. — par Phylogenetic oni viit and biogeography of the endemic Caribbean genera n ra , and Haitia cc) Cilia J. Sci. 38: 195-204. 2003. Biogeographic — a Antiles Lythra- ceae. "ont brit Bot. 28: 41 . 2005. I— some names in the Lythraceae, with e" on names by A. Grisebach. Harvard Pap. —304. & T. B. Cavalcanti. 2001. New chromosome counts in the Lythraceae and a review of chromosome numbers in the family. Syst. Bot. 26: , J. Hall, K. Sysma & S-H. Sh. 2005. Le analysis of th ue Int. J. Pl. Sei. 166: 995-1017. & R. Kleiman. 1987. Seed lipids of the Lythraceae. ee ee Ecol. 15: 433-439. H. Lorence. 1978. The rediscovery of I m r^ (Lythraceae). Bot. J. Linn. Soc. k. S. B. 2001. Biogeography of the West een z overview. Pp. 15-33 in C. A. Woods & F (editors), n of the West Indies, A ed. CRC Press, Boca Raton Holmgren, P. R, N. E "gres & L. C Barnett. 1 Index Herbario ronx. ems of the jan 1492— 1800 i in e Lesser Antilles. e Missouri Bot. Gard. 62: Charles Wright in Cuba 1856-1 Chad Chdesc Hole Arnold d arvard Uver y, Jamaica Plai Judd, W. S. 2001. Phylogeny and biogeogra aphy of Lyonia sect. Lyo S Pp. 63-75 in C. A. Woods & F. E. Sergile (editors), Bi of the West Indies, 2nd ed. CR Boca tx Florida. TOME E. 1882. Lythraceae monographice describuntur. Ginoria Jacq. Bot. Rm Syst. 3: 346-352. eae monographi - 1885a. Lythraceae monographice describuntur. Der Bau der Bliiten. Bot. Jahrb. Syst. 6: 148. - 1885b. Lythraceae e monographice describuntur. Die mec Verbreitung der Lythraceen. Bot. Jahrb. Syst. 7: 1-6 . 1903. EL Pp. 1 n A. Engler (editor), Das Piinius IV, 216, Mie 17. Wilhelm ed r Leipzig. Lavin, M. 1993. Biogeography and systematics of Poitea (Leguminosae). Syst. Bot. Monogr. 37: 1-87. León, Brother & Brother Alain. 1953 [reprint 1974]. Flora de Cuba 2: 392-394 Liogier, A. H. 1968. Novitates Antillanae. III. Brittonia 20: 148-161. . 1969. Flora de Cuba Suplemento. Editorial Sucre, Consens: . La Flora de la Española. IV. Vol. 64, Serie Cientifica 24. Universidad Central del Este, San Pedro de H. Wadsworth. 1974. Trees of Puerto Rico and the Virgin Islands, Vol. 2. U.S. pe of Agriculture, Forest Service, Washington, e S. A, R. A. Stockey & R. C. Keating. 2004. llaqtanpa like leaves from the Middle Eocene Princeton chert and comparative leaf histology of Lythraceae sensu lato. Amer. J. Bot. 91: 1126-1139. 986. Revisión del Genero Crenea Aublet 142 W. P. Maddison. 2000. MacClade, vers. 4.07. bier Associates, Sunderland, Massachus' etts. McNeill, J., F. R 006. International Code of Botanical Nomenclature (Vienna Code). Regnum Veg. 146. hito F. 1952. E Yapusqa de Chiapas. Vol. 1: 99; eee de Prensa z, Méxi Gin. Cat. Fl. Domingensis 1: Roig y Mesa, J. T. 1963. Diccionario Botánico de Nombres Vulgares Cubanos, 3rd ed. San ntiago de las Vegas, Santiago-Valentin, E. & R. G. Olmstead. 2004. Historical biogeography of Caribbean plants: Introduction to curren knowledge and possibilities from a phylogenetic perspec- tive. Taxon 53: 299-319 Sergile, FRESCA Woods. 2001. Status of conservation in 547-560 i Speed, R. C. & C. A. Keller. 1993. Synopsis of the geological evolution of Barbados. J. Barbados Mus. Nat. Hist. Soc. 3-139 Stafleu, F. A. 1971. Introduction to s of the 1763 edition of N. J. Jacquin, Select. irpium American- arum Historia, dis F7—F32. Hafner Publishing, New York. — ——- & R. Cowan. 1985. Taxonomic Literature, ed. 2. V. W. Junk b.v. Publishers, The Swofford, D. L. 2002. PAUP*4.0b10: Phylogenetic M Ure Parsimony Que Other es, Sunde: rlan Tobe, H. P. H. Raren & Š À Gun. 1986. Chromosome counts for some Lythrace. str. (Myrtales), and the ce Taxon 35: 13-20 — S. A. P. Raven. 1998. Floral morphology and “lun in "m sensu S cit - J. Owens & P. J. Rudall (editors), ve Biology: Royal Botanic Gardens, Richie Volume 97, Number 1 Graham 89 Revision of Ginoria (Lythraceae) Ie W. 1964. Die Infloreszenzen. Typologie und Stellung Aufbau des Vegetationskorpers, 1. I Deskriptive Mor- iua der Infloreszenzen. II Typologie der Infloreszen zen. Gustav Fischer, Jena. Urban, I. 1920. Flora Domingensis. Lythraceae. Pp. 469—4 in = Urban (editor), Symbolae ‘ete Vol. un raeger, E zig. ài Vliet P. Baas. 1984. Wood anatomy es page oars dl o Myrtales. Ann. — Bot. Gard. 7 Weberling, F. 1988. The architecture of inflorescences in the Myrtales. Ann. Missouri Bot. Gard. 75: 226— White, T. J., T. Bruns, S. Lee & J. bi s 1990. Aoglificoiion rect sequencing of fungal ri mal RNA genes for phylogenetics. Pp. 315—322 in a Innis, D. Gelfand, J. Sninsky & T. J. White (editors), PCR Protocols: A Guide to Ms and Applications. Academic Press, Diego. . A monograph of Sabal (lisnato O es, Aliso 12: 583-666. APPENDIX 1. I of Ginoria by Koehne (1903). Names in brac are currently accepted names following this revision. Subgenu Ne Koehne [subgenus Ginoria]: Flowers typically 6-mero Section Pm mum Koehne [section Ginoria]: Seeds obovoid- -prismatic, stamens (10)12 to 7 G. americana, G. spinosa [= oo G. glabra s Antherylium (Rohr & Vahl) Koehne: Flowers typically aliam G. nudiflora, G. rohrii APPENDIX 2. Numbered collections £ Numbers in parentheses correspond to the nu the species in the text and in the List of n below. "delis numbers in boldface indicate type numbers LIST OF SPECIES l. Ginoria americana — var. var. iban ; (Griseb) S. A. Graham Ginoria arborea Britton Ginoria buchii (Urb.) S. A. Graham Ginoria callosa O. C. Schmidt Ginoria curvispina Koehne inoria — S ^ (€ Britton Ginoria glabra G Ginoria jimenezii Alain Ginoria koehneana 10. Ginoria lanceolata à. C. Schmidt ll. Ginoria nudiflora (Hemsl.) Koehn 12. Ginoria pulchra (Ekman & O. C. Schmidt) S. A. Graham 13. Ginoria rohrii (Vahl) Koehne - pu FP Ke mcm ue» m Acevedo-Rodríguez, a): Acevedo-Rodríguez, P. et al. 1827 (13), 3221 (13), 5137 mra costa/Dorantes A-640 (11); Acuña, J. 5172 (5), 5173 (5), 10573 (1a), 10760 (1a). 17144 (5), 19038 (1a), 24165 (1a), 24168 (la); Acuña, J. & E. 1 : Acuña et al. 16182 (9); Alain, Bro. 1737 ME 3965 59. 6700 ©. dr o x. (9), 16182 (9); Alfonso, O. 31375 (2), 31478 (5), 31753 (5), 45158 > Arias, I. et al. 61566 (5), 62072 (la); Avila, J. et al. 3028 (la), 3045 (5); Axelrod, F. 4981 (13), 7608 (13), ses (la). Berazaín, z & pere ; 31967 Qu), 3. 31973 (1s), 31974 (la), 31979 (1a); Bisse J. 645 (1a), 5006 (1b), 7727 (2), 8053 (6), 9 (la), 10681 (la), 10183 (2), 13173 (6), oa (2), 17523 (1b), irs (1a), 21769 (2), 21830 (2), 23253 (6); Bisse, J. & Duek, J. 1114 (1a); Bisse, J. & Köhler, E. Ter d ); Bisse, J& Lipol, 13175 (6), ow (la), 19501 (la); Bisse, J. & Rojas, L. , J. et al. 21091 (5), 30919 (6), 33974 (2), Lus (1b), 36577 (2), 38193 (9), 39076 (2), 39305 O, 39471 (2), 39689 (la), 41140 (a). 44904 (La); net, W. 7454 (1a); Borhidi, A. et al. 11 D. t 34029 (11), 35078 (11), 50647 (1D, "51661 (11); Britton, N. L. et al. 131 (13), 446 (6), 2217 (2), 2368 (5), 5560 (9. 5577 (6), 5858 (6), 5900 (6), 5903 (6), 6024 (13), 6083 (6), 6093 (1b), € v 12953 an, 13113 (5), 13148 (5); Britton, G. Britton 210 (13), 10123 09. 10126 (13); Britton, N LR nd oat 6); Britton, L. & J. A. Shafer 06 013) 1502 Q) mae DE, L & P. vin 5474 (6); Brull, G. C. and R. Verdecia 5432 (9); a L 6913 (5); Castañeda, I. & N. Vera 6837 (6) Chavelas, J. et al. ES4201 (11); Clemente, Bro. 2410 (la), 4872 (1), 6312 (1a); Clemente, Bro. & 4, Bro. 5924 a Clemente, Bro. & Chrysogone, Bro. 3410 ye Colaboradores del Flora de Cuba 62522 (9); Canit; R. 26 (la); Cortes, L. 264 (11), 867 (11); Curbelo, M. 206 (9), 229 9), 24166 (9). "1 D'Arcy, W. G. 50A a3, mn 182 (13), 1824 (13); Daris, L I. & E. B. Kincaid, 11): 007 (la). asa, É 52 (13), a SHE 307 (13). 4583 (1a): Ekman, E. L. 83 (1a), 2790 (1a), 431 ee 10). 4619 (4). 5676 (3), 6356 (9). 7 i im s (La), 9696 (10), 10221 Aia pt (6), 11549 5). 13742 (6), 14051 (1b), 14052 (6), 1 : | : (2), 16405 (6), 16517 (1b), 17006 (5), 17406 (9), 18608 (la), 18824 e. jm i (6), 18973 (6), 19049 (5); mer phone: 37332 uli ernando, n jr (1a), 369 (la); F L£ 201 ix Tw und 2444 o, 2> (5); unkuk, LW. 219 (13), A. J. 436 a ménez, x 3614 (8); Garcia, R. & Pinunit, H. = (8); Gillis, . T. 7983 (la); Glassman 09 (1b): (6); Graham, S 199 (1 D, són 1136 (6). deben io. T iwo D o 144 (6). 1145 (1a); Grouddzinska : mic ge * 1); Gutiérrez B., C. pale (11), 3092 P 11 a. 3103 (11). ` mins a ne 121 (1b), 875 (1b): — H A. ng (la), 4561 (la) Hi menli, F. v. 11548 (la), 11577 “Jack, J. G. 4070 (1a), 4532 (la). us (1a), 5082 (la). 5481 (1a), 5551 (1a). 5967 (6). 5969 (6), 6779 (La), 7028 (6), 7899 (6), 7970 (6); Jiménez, F. 2684 (8); Jurgensen, C. 956 (11). 90 Annals of the Missouri Botanical Garden Lago 24 Hispaniola: Haiti: G. buchii, G. callosa, G. lanceolata, G. 69 (1a); p R. 24169 (1a); v Bro. 331 (1a), 68 (7), 1 (6), » 17649 (5); Leonard, E. . C. & Leo Liogier, A. 14693 (3); Lippold, H. et al. 26187 (0; Liule, E. 16427 (13), 23812 (13); Luis, M. et o Manitz, H. et al. 60393 (5); Marie-Victorin, “Bro. 6004 60047 (la); Mee C., G. 1336 (11; E <. E. Ais ç (y ínez V. & Ti illo, R. 9020 (6); Matos, J. et 90 (6), 1725 (6); Matos, A 18571 (A Mell, D. 510 (11) Minds d 3302 (9), 3368 y naa IT J. 7385 (5), 7. (5); Méndez 8036 (1 b); Méndez, cr & Trujillo, R. 3557 (5 ES ia, R. 992 (6), 1013 (o, 10 1074 (la), e (la), 4641 E 4718 (6), 4843 (6); (5), 4069 (5), 10019 (1b); Meyer, K. ae 66 (la); Minanda, F F, 7138 an, 7184 an, 7494 (11), 8278 (11); M aN * 4 375 (5), 3 p 474 (la), T ‘61 85 171 (13); Morton (5); om 4402 m 10380 tis bt V. & Acuña, J. 3847 (la). Noa, A. 4095 (6); Noa, da à: Castañeda 153 n. 3933 (6); Noa, A. & Méndez, E. 7373 (1b); Noa, A. et al. 3 06 (1b), ride (6). pega 560 (6. er (6), 1453 (6), 3843 Olviedo, r SE 5 ES im PN 22 (11); Pérez, A. 243 A 244 (6), 790 (5), aray, L. 1 a 6, NS 793 (5); E 3809 (5); Pollard, L. 39 (1a); Ponce, R. 2 le, C. G. 105 (la); 535 (13), pin (13), 49271 (13). Rehder, A. 1123 ta edis y ie E P. 4153 qus R& , R. 6278 (5); Risco, R. & Méndez 2544 (1a); Kask a ana „R. 9516 (12; Roig y Mesa, 5 T. 3249 (6), 5172 (5), 8548 (6), 11069 (7): Roig & Luaces 825a (S Rois et al. 5999 (5), 6092 (6); Rugel, F. 65 (la), a). a) Sargent, F. H. 202 2 (13); Schafer, J.A. 270 mie ped a), 2403 (13), 2640 (5), 2878 (5), 8784 (7), 11201 (la), 11810 (5), 11890 (a), 12160 (la); Seifritz, W. 1046 (T); S n 3172 (1a), 3204 (1b); Soto N., Sousa M. 1739 (11), 7281 (11); Stahl, A. 74 (13); Stuchlik, L. 272: > 4 (6). Tellez, O. 405 (11); Torres C., R. 2817 (11), 2849 (11) 8154 (11). - 3804 (la). uS R. $0 (9. ne (5), s > 22 S iie " (9); Verdecia, net Bull E 323 (5), s: d 2781 (5), pie = Lo T Yero, M. 3575 (5); san Hermann 351 (la), 495 (1 1839 (1a), 4351 (1a). wes “a Wagner, R. J. 864 (13) 988 (13), 1407 (13); s T. et al. 3203 (11): Wright, C. 160 (la), 2544 (7), 2 Un se "e S B «as 2546 (6); Wyder, H. 46 vow T. et al. 33439 (12). 9 p.p. APPENDIX 3. Distribution of Ginoria species by country. Mexico: €. nudiflora Cuba: G. americana, G. arborea. G. curvispina, G. ginorioides b iln Fue A pulchra. Dominican Republic: G. buchii, G. LE Puerto Rico and the Virgin Islands: C. ApPENDIX 4. Character list for morphological matrix. L. leaf vena thin, brown or scarcely visible; l= — yelovish, > raised areolae. 2 so ; 1 = pre . Inflorescence: d — ending in a vegetative bud (blastotelic or polytelic); 1 = ending in a flower e or aeo lic). Floral = 4;1 = 6; 2 sepal length: P = 02-05 (floral cup shorter and int longer); 1 = 0.7—1 (floral cup and sepals approximately equal length); 2 = 1.2 or greater (floral cup longer pie ne T. Petal color: O = white or pale pink; 1 = rose to purple; 2= absent 8. Inner fl t distal — narrowly fre a t distal margin; 2 — expanded as a ode collar. 9. Lowest stamen number: 0 — Bor less; 1 = 12 to 18; 2 = 24 or more. 10. Pollen pseudocolpi: 0 = absent 11. Pollen exine: 0 = scabrate; = striat 12. Fruits: ^j = = khas 1 = indehiscen 13. Seeds: 0 = compressed, obovoid, AE or fusiform; 1 = not compressed, obpyramidal. 14. Seed mesotesta: 0 — multilayered; 1 = homogenous, nonlayered. 1 the margin ; 1 = pre = asume = tmm APPENDIX 5. Morphological matrix for cladistic analysis. Outgroup Ammannia 00002 aa001 3100 Crenea 00001 00001 1100 00020 11000 b011 Lagerstroemia 00111 0a001 a011 Lawsonia 00101 00001 2111 Tetrataxis 00001 02000 2000 0a011 01011 0000 G. arborea 01000 00011 0000 G. buchii 00011 21121 0000 C. callosa 10012 11121 0000 C. curvispina 01011 11011 0000 ginorioides 00011 11011 0000 C. glabra 1001121121 0000 G. jimenezii 00001 01011 0000 koehnea 01000 00011 0000 G. lanceolata 01000 02001 0000 G. nudiflora 00001 00211 0000 G. pulchra 10012 21121 0000 G. rohrii 01000 00011 0000 = ine ee a = Oand 1; b = 0 and 2. CHROMOSOMES OF NEOTROPICAL RUBIACEAE. I: RUBIOIDEAE' Michael Kiehn? ABSTRACT r presents Puro data for 130 accessions of 91 species « or subepeciio taxa ev 26 genera of This Neotropical Rubioideae (R or 11 genera, and for 71 species and subspecific taxa. A survey of the karyolagical arra (chromosome numbers, a i DI The a discussion hology) for Neotropical Rubioideae is giv ven. morpho relationships an Face in the Rubioideae is bui s; ords: aryology, Neotropics, EAE Rubioide. Chromo: numbers, k ped of the karyological information f ossible taxonomic A of the M are iue. In the course of comprehensive karyosystematic studies on Rubiaceae (Kiehn, 1986, 1995), existing data for Neotropical members of the family were compiled and numerous new counts were made. Up to now, karyological information on New World Rubia- ceae has been very limited, with the few published data scattered in the literature. Based on detailed literature studies (especially new molecular phylogenetic ap- proaches) and the new chromosome data, implications for an understanding of radiation, adaptation, evolu- tion, and systematics of the investigated groups of the Rubioideae are discussed. A second paper (Kiehn, in prep.) will explore the other representatives of the Rubiaceae, recently united in one subfamily (Cincho- noideae) by Robbrecht and Manen (2006). MATERIALS AND METHODS š ological investigations are based on field fixations or fixations from plants cultivated at the Botanical Garden of the University of Vienna, Vienna, Austria (HBV). Fixations of meristematic tissues (actively growing root tips, young flowers or apices for counts of mitotic numbers, young flower buds for meiotic investigations) were made in a freshly mixed 3:1 solution of ethanol (96%):glacial acetic acid. In most cases, fixations made from germinating seeds TR pretreated with 0.002 M 8-hydroxyquinoline solution for 6 hr. at 8°C-10°C in the dark (see fon by the author was obtained from a erreicher" (Costa Rica). I thank the Botan taxa and for sricswledgod. Special than care University of Vienna inae making them M for hoe studies. Technical istanc e to the collectors mention Table 1). The fixations were kept under cool condi- tions at approximately 8°C. Chromosome staining was performed with Feulgen reagent, Giemsa, or aceto- tissues investigated, and techniques used for eac species investigated are listed in Table 1. Permanent slides for the counts are deposited in the personal collection of the author. Voucher specimens have been deposited in the herbarium of Vienna cra (WU) and/or in other herbaria as stated in T. The tribal arrangement of the Rubioideae in s this paper follows Robbrecht and Manen (2006). RESULTS AND DISCUSSION Table 1 presents the new chromosome data and, when applicable, also includes references to earlier counts. Data for 91 species and subspecific taxa (130 accessions) of 26 genera are reported. They include the first chromosome number reports for the tribe Perameae, for 11 genera, and for 71 species. Data for 15 species are in accord with earlier reports; five reports deviate from earlier counts. BASAL RUBIOIDEAE SENSU ROBBRECHT AND MANEN (2006) Perameae and Lasiantheae. The monogeneric tribe Perameae was separated from Spermacoceae by This study was partly supported by the ER eae der Stadt e (proj. H-196/99). Logistical support of acional in San José (Costa Rica) and from the “Verein Regenwald M ) for the skilled ——1 of man in some counts by M. Pass is gratefully s Dessein for sharing unpublished wasa. S Bridson, J. H. Kirkbride Jr, C. M. Taylor, and W. Till for determinations, to S. V. T. Helkecll, and an anonymous reviewer for useful molecular studies on Spermacoceae, and to comments. "University of Vie nna, Department of Biogeography, doi: 10.3417/2007115 ANN. Missouni Bor. Garp. 97: 91-105. Pu S. Dessein, E. Robbrecht, Rennweg 14, A-1030 Vienna, Austria. michael.kiehn@univie.ac.at. BLISHED ON 31 Marcu 2010. 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(Z) "ws zuag-up1BoN uoyug 1y2nvds qn 9 Mut H A H M 86 E [3-28 YY “YM 0g = ug uey əiotu 1ou Á|əltutJəp U : S XG or xi 98€ “SEE pud y 7NAQ-U9LIAN MS HOR Y U i = xc 9c — (T) "ws zu4dg-ugigoy 1907) xo uojug 142302 "4 MG DOponiy Se U y ES XG «8d — -12882 19819q5N09 w safropuasyq "unus *y (3ue1dg) viv]joqum 73 snuo2 oq 10] junoo 1s1tj "puq xe pgoq »zndoounu "unos “Y (MYOS Ņ woy xə PIM) vwmado mpoq = H 9t H vy +98 — 1/8-SIZOS6 1ə(muləs1ə] TPUYPS $ ure) opis q "1 Pang SJUQUWILO) PUB SAIBUIOL :s]unoo IQULIO Y IL 1S d Id uc u I9Q9noA UOXB |, "penunuo)) ‘I QPL Missouri Botanical Garden Annals of the T Y *ZU1O-uo18ƏN 01 pajeorunuo) ejep ayi 10991791 Ápareanooe jou op 1nq *1291109 9q p[noo squaurojejs asaup ,, ("uuo "sed “uyary) (endeuy W15) 110407 9 pue “(endeu] jea1o)) 1yInods¡nu q *(ooeqy 19912) pue equ) sz4011] 7] (oouqy 18915) 14909 g Buowe AIBA JOU səop “I — x *requinu eurosouiorqo orsgq aug ***,, sg (pep :9661) &axporg pue zni()-uoigoN ur pue ,, * * '("uruioo "siad *ugary tuong 170140] "3 pu tuong rn2npdspu 73 *stp4or] 75] 19307) xo uontag 242302 71) exei pezrudooo:1 Apuaumo eq Áq pətiqiuxə st T = u *12quinu auiosouro1q9 oreeq aures ət: 7, SE (EQ :966T) ¿MIO -U9BAN Áq parro 919^ Kap "zni-uorday oi pareorunururoo *[rejop ur o1aq pauodoid se *a1oA si[nsar au] *s[o49] Ápro[d oi qsipqeiso o1 o[qrssod Apuo se 1r 10 o2ue1 1oquinu ouiosouroqo [eua]od v po[eaAar aure squnoo 1a [[E *(əspudpl1əuioid ənotru ur umi p '89) sawosoworyo əy) JO azirs ase] au pue suonext] prey eu jo Kupenb aui 0j on(q 'eqny woy s/D40711] ‘g pue seweyeg 3y} woy 142502 papou4;p 10J pa1oalap 9q Auo p[noo szequimu eurosouioiqo jouxe *sarpnis jueseid ai jo esrnoo au UJ z "Dupouxaui ([ ed 1snur ouru j29100 at tjoax10out st snuoS sri jo uoxej ueotioury. [911u97) ot 01 saprours]p Domu£pi oureu oq jo Tuounsirsse Juano ay *('urtuoƏ 'siəd) əəuəio' y q Áq sorpnis peusiqndun o] 2urproooy , *1 xipuaddy ur pajuasaid are ejep zurjoo[oo popreje 'srsojur uoprod ‘od *xade jooys ‘de ‘sdr 1001 *j1 tənssn 1uəug “t tənssn e| A18 *15 treo Sunod ‘Ao ipnq 19^0[J 3unoÁ “[y [99 19yjow ua¡pod *) [pg :se pajeo1pur st sjunoo jo peurojeur ao1nog *esurat^) *) juadeod usd na y “y təuruumooləog “y tourpoumbÁxo1pAy-8 ‘H :4q pereorpur ere spoyiotu Zururejs pue juaurvarjeiq "erep onieron uod uoneriop sojeorput ,, tsaroads ay] 10J junoo jsrtj ou sajeorput , Sururejs ‘Ig tjueurjeaajoad “y tono] Ápropd *]g “1oquinu atwuosoworyo propdip “uz traquinu aurosotuolyo propdey ‘u tenues am 10j junoo jsitj eui quasaldas (,) sistalsy “ansst “11, ‘poyo y y e. gz — 4966-S[ 491008107) U Y a x 96 ji 2981-11 19819q51100 uongognuopt &09 SuirAJsues o] peo[ 10u prp a1nquze1I[ e[qe[reAe 9Nd V — xc -= VI -EZgg4 42819081104) y Jafiopualyy MU ‘ds araooovunads,, "94 (y “umg) saprowkoo muaog = u A H *p 9 — 6I-S8E0I€ XH utəty X uyay "J wung saproukoo 'ç "H A H xc +82 a C/T-SBEOSE NW UYAtTY X uyay u A H “z 87 — — &/I-9880S0-YW “YY P Yyy a]puey psnfuoo `ç [e1qeo m odnpedroeg (we) vDjo0wWas DILALIOg = H A H xc +87 — I/T-S8E09T NW "tory op utgory ‘ABg Y AMY suagunssp 'e (əaoqe oos) pporpnuay Suipn[əxə *(9661) P1qe9 pue odnpesioeg nsuos puauog Surpn[out "| 2202DuLiadg " i eH X E. < “u's 43211540] "aput “ds pypunyory sluəuttuoƏo pug syIguiəir :s]unoo I9ULIO | iL IS d “ld UG u Aayano A UOXE |, *panunuor) ur 2198 L Volume 97, Number 1 2010 Kiehn Chromosomes of Neotropical Rubiaceae Bremekamp (1966), based on earlier observations (Bremekamp, 1952: footnote on pp. 13-14). The first karyological investigations on members of the genus Perama Aubl. revealed x = 9 as the basic number for the genus. The two counted populations of P. hirsuta Aubl. show different ploidy levels (2x and 8x). use this species comprises several varieties (Steyermark, 1974), more counts would be desirable to elucidate potential correlations between subspecific units and ploidy levels. The Lasiantheae were established by Bremer and Manen (2000) and are proposed to comprise the genera Lasianthus Jack, Ronabea Aubl., Saldinia A. Rich. ex DC., and Trichostachys Hook. f. by Robbrecht and Manen (2006). The first count for a species of the genus Ronabea, resurrected by Taylor (2004), reveals the tetraploid level for R. latifolia Aubl. (formerly Psychotria erecta (Aubl.) Standl. & Steyerm.). No other chromosome numbers for Neotropical members of tribe Lasiantheae are known — In the rps16 intron analysis of Andersson and Rova (1999), the genus Perama appears sister to Lasianthus at a basal node of the Rubioideae phylogeny. The Lasiantheae form the third basal clade (after Ophior- thizeae and Urophylleae) in the strict consensus tree for the Rubioideae of Bremer and Manen (2000); this study did not include Perama due to the lack of material. The supertree of Robbrecht and Manen (2006) shows Perama and Lasianthus as one of two clades in a grade at the base of the Coussareeae. Do the cytological results corroborate the relationships of the Perameae and the Lasiantheae suggested by these molecular studies? The present count for Ronabea indicates a basic number of x = 11 or x = 12 on the tetraploid level. Additional data for Lasiantheae are rare: for the genus Lasianthus, there is only one published count of an Old World species (L. acuminatus Wight from India, n = 44; Bir et al., 1984) indicating octoploidy and x = 11 as the basic number. Several attempts made by the author to get additional chromosome data for Lasianthus resulted in only one approximate count (for L. lancilimbus Merr. from China, 2n > 200; Kiehn, unpublished data); this was due to the presence of tannins in the fixations causing dark chromosomes that clumped together. The field fixa- tions of Ronabea (as well as cytological fixations of Saldinia material from Madagascar; Kiehn, unpub- lished data) exhibited the same effects of tannins, while the two investigated Perama field fixations did not show such features. Thus, neither basic number nor chemical compounds interacting with c fixatives support the assumption of a close relati ship between Perama and Lasiantheae. on- How can the cytological results for Perama be interpreted in relation to other Rubioideae? Chromo- mes of Perama St have different staining patterns with acetocarmine (Perama: stains well, with no cytoplasmatic staining; Spermacoceae: contrast of chromosomes against cytoplasma is weak); they are also different in condensation the chromosomes (see Kiehn, 1995: all Spermacoceae exhibit late condensation of telomeric parts of the chromosomes, which is unusual in Rubiaceae and not found in Perama). Thus, a position of Perama near to Spermacoceae is not supported by ch characteristics. Of all groups in closer proximity to Perama in the Rubioideae supertree of Robbrecht and exhibit a bimodal karyotype (Kiehn, 1985, 1995), a situation that could not be documented for the two Perama accessions studied here. Thus, the prese tl known cytological findings give no further indication about relationships of the Perameae. Coussareeae. The tribe Coussareeae as emended by Bremer and Manen (2000) comprises taxa formerly included in several tribes (Coussareeae, Coccocyp- seleae, and Cruckshanksieae) by Robbrecht (1988) and, in the supertree of Robbrecht and Manen (2006), is placed as sister group to the Psychotriidinae and the Rubiidinae. conference abstract). details for the reports of Kiehn (1989) and an additional count for C. hirsutum Bartl. ex DC. are included in Table 1. Based on these data for seven taxa, Coccocypselum exhibits a basic number of x = 10 with taxa on the diploid and tetraploid ploidy level. In C. hirsutum, the occurrence of two cytotypes (diploid and tetraploid) is documented. The first ch me counts for the genera Coussarea Aubl., Cruckshanksia Hook. & Am. Aubl. are presented ere. Cruckshanksia are diploids on x — 11 (one species of each genus). In Faramea, three species (four accessions) were counted; all are diploids. Regarding basic numbers, the obtained picture is not clear. One species (F. glandulosa Poepp. & Endl.) shows x = 11 (counts on mitotic divisions). In F. suerrensis Donn. Sm., all counts on somatic tissues for two accessions also revealed 2n = 22. However, meiotic irregularities were observed, leading to gametes with n = 10 as well as n = ll. In the third investigated species (F. Annals of the Missouri Botanical Garden tetragona Müll. Arg.), the basic number could not be established with certainty. Based on these data, x = tetraploid on either x — 9 or x — number. This result concurs with the pro exclusion of Declieuxia from the Psychotrieae (Bremer discussion below). It also fits with the palynological findings presented by Piesschaert et al. (1999) stating a sein pollen type shared by Coccocypselum, Declieuxia, and . Benth. (the latter not known ejidal yet), with the molecular data (nuclear DNA SES and chloroplast DNA [cpDNA]; Andersson & Rova, 1999; Bremer & Manen, 2000: Robbrecht & Manen, 2006), where Coccocypselum and Declieuxia form parts of a well-supported clade. summary, it can be stated that the tribe Coussareeae of Bremer and Manen (2000) is cytolo- gically heterogeneous. In terms of phylogenetic trends, an ascending dysploid series might be a possible explanation if it is assumed that the relationships expressed by Andersson and Rova (1999) are correct. The tribe then has x — 11 as the original basic number, present in the more basal Cruckshanksia and in the molecularly well-supported clade consisting of Faramea and Coussarea, while the clade formed by Coccocypselum and Declieuxia shows a derived status of x — 10 (or even x — 9). The most probable hypothesis for explaining the observations is that several parallel changes of basic chromosome numbers occurred in the different genera. This would also best explain the situation documented for Faramea. SUPERTRIBE PSYCHOTRIIDINAE Morindeae. Only few chromosome data exist for members of this tribe, and all exhibit x — 11. The statistical data for Morindeae given by Kiehn (1995) need to be adjusted, as the genus Lasianthus, which is responsible for the reports of the high ploidy bsds (8x and 20-22x) in Kiehn (1995), is excluded from the Morindeae (Bremer & Manen, 2000) and transferred to the Lasiantheae. The remaining counted taxa of Morindeae are either diploids or tetraploids. In the Neotropics, only one taxon has been investigated — so far. Morinda royoc L. is diploid (n . 1962; 2n = 22: Fritsch, 1970). For ds OS M. citrifolia L., all counts (revealing one diploid and several tetraploid results) were carried out on accessions from outside the New World (see Kiehn, 1985). The new count for M. panamensis Seem. (2n = 22) fits well into the general cytological picture of the genus. Chromosome struc- ture and staining behavior of Morinda L. are similar to the patterns found in Psychotria L., especially in subgenus Psychotria. embers of Psychotrieae s.l. (Psychotrieae s. str. sensu Robbrecht & Manen, 2006, and Palicoureeae Robbrecht & Manen, 2006) are found in the tropics and subtropics worldwide. In the Neotropics, the tribe is represented by ca. 1000 species (Taylor, 1996). The largest genera in the region are Psychotria s.l. (ca. 600 species), Palicourea Aubl. (ca. 200), and Rudgea Salisb. (ca. 120) (Taylor, 1996). Psychotrieae s.l. Despite the huge number of Psychotrieae s.l. species in the Neotropics, up to now chromosome numbers have been reported for only eight members of the tribe from this region: five for taxa of Psychotria subg. Heteropsychotria Steyerm. and one for a species of Ar subg. Psychotria, Carapichea Aubl., and Palicourea, respectively. These reports all revealed a basic number of x = 11 (the number common for the bulk of the cytologically investigated Psychotrieae species worldwide; see Kiehn, 1995). For seven taxa, the reports are exclusively on the diploid level: Palicourea marcgravii A. St.-Hil. (Pinto-Maglio et al., 1997), Psychotria brachyceras Müll. Arg. (Kiehn & Lorence, 1996), P. brasiliensis Vell. (Fagerlind, 1937, P. nuda hera P. M Schltdl. (Kiehn & Lorence, 1996), hoffmannseggiana (Willd. ex Roem. & RD Mill. Arg. (Pinto-Maglio et al., 1997), P. ligustrifolia (Northr.) Millsp. (Lewis, 1962), and P. nervosa Sw. (Lewis, 1962; Fritsch, 1970, both as P. undata Jacq.). One has diploid and tetraploid reports (Carapichea ipecacuanha (Brot.) L. Andersson = Psychotria ipecacuanha (Brot.) Stokes: Fagerlind, 1937; Janaki-Ammal, 1945). In Palicourea marc- gravii, Pinto-Maglio et al. (1997) observed three additional (B-type) chromosomes. rcumscription of the abun s.l. (see dba 1988; Taylor, 1996) has only ecenily been altered considerably. Several papers (see Robbrecht & Manen, 2006, for a survey) provided evidence that the Psychotrieae s.l. disintegrate into two clades. On the generic level, Nepokroeff et al. (1999) clearly showed that Psychotria in the tradi- tional sense is paraphyletic. One consequence is that the monophyletic Psychotria sect. Notopleura Benth. & Hook. f. was reestablished at genus level (Notopleura (Benth. & Hook. f.) Bremek.) by Taylor (2001). Taylor (2004) excluded Ronabea from Psycho- tria and placed it into the Lasiantheae of Bremer and Manen (2000). Andersson (2002) subdivided the Psychotrieae into two major clades: the Psychotria Volume 97, Number 1 2010 Kiehn 101 Chromosomes of Neotropical Rubiaceae Table 2. Comparision of frequency of ploidy levels in the investigated Neotropical taxa of Psychotria s.l. (including information from literature). 2x 4x 6x 8x 10x 12x(-14x) Psychotria subgen. Heteropsychotria (31 three with two ploidy levels) 12 (35.3%) 18 (52.9% à; í 9%) 1(2.9%) 1(2.9%) 1(2.9%) 1 (2.9% Psychotria subgen. Psychotria (10 taxa) 7 (70.0%) 2 (20.0%) 0 0 0 1 (100%) complex and the Palicourea complex, the latter including Carapichea, Geophila D. Don, Notopleura, ea, and an expanded Palicourea (including Psychotria subg. Heteropsychotria). Both were formally circumscribed by Robbrecht and Manen (2006) as tribes Psychotrieae s. str. (in the Neotropics only comprising members of Psychotria subg. Psycho- tria) and Palicoureeae (with the genera Carapichea, Geophila, Palicourea, Margaritopsis C. Wright, Noto- pleur a, Rudgea, and Psychotria subg. Heteropsychotria occuring in the Neotropics). P. sychotrieae s. str. In the present study, 10 taxa (12 origins) of Psychotria subg. Psychotria are investi- gated, nine of them for the first time. Seven taxa investigated were diploids, two were tetraploids, and only one (P. sylvivaga Standl.) was a high polyploid. This is in marked t to the proportion of diploids - polyploids found in Psychotria subg. Heteropsycho- tria (see Table 2). Palicoureeae. Counts for 63 accessions of 46 taxa out of five genera of the Palicoureeae are presented here, including first generic reports for Notopleura and Rudgea. All investigated genera have x = 11 as the basic Pulbber and show polyploidy. In Geophila, species on diploid and tetraploid levels are reported. The only m for Rudgea is on the 12x level. Palicourea "peces exhibit either 2x, 4x, or 6x. Notopleura species have taxa on 2x, 4x, and 8-10x. In all these genera, different accessions of the same species always have the same ploidy level. No indications se B chromosomes (as reported in Palicourea by Pinto-Maglio et al., 1997) could be found. In Psychotria subg. Heteropsychotria, taxa with 2x, 4x, 6x, 8x, 10x, or 12x are known now. Psychotria subg. Heteropsychotria also comprises all four Neo- tropical Psychotria cases of different ploidy levels reported for different accessions of the same species- For P. capitata Ruiz & Pav., P. hazenii Standl., and P. hoffmannseggiana, both diploidy and tetraploidy are reported, and in the high polyploid P. aubletiana Steyerm. there are counts on 6x (P. aubletiana var. aubletiana) and 10x (P. aubletiana var. Steyerm.). The existence of different ploidy levels can be interpreted in several ways: it could be an indication of shortcomings in identifications (possibly as a result of the high number of Psychotria taxa described in the region). The different ploidy levels could also indicate the presence of two cytologically different units currently treated under one name (possibly the case in P. aubletiana, P. capitata, and P. hoffmannseggiana, as all of these are species with large distribution areas in Central America, the northern part of South America, and the Caribbean, a 3503. oie ej io BE B A mark [1972, 1974]. In these cases, ploidy levels could provide additional arguments and characters for listinguishi 1 nami lly existing taxa. The detected differences in ploidy levels also could be the result of recent polyploidization events forming the basis for separation of new species (possible in P. hazenii, because the two investigated individuals originate from the same geographic region). More collections covering the whole distribution areas the above-mentioned species need to be investigated to get a clearer picture of the implications of the reported differences in ploidy levels. already assumed for Psychotria subg. Psychotria in the Pacific (Kiehn & Lorence, 1996), a predisposi- tion for polyploidization could also be an important ion in the Neotropical Palicoureeae, notably in Psychotria subg. Heteropsychotria. The much higher number of Neo- ed o bi ado ja bane in the Psychotrieae in the Neotropics thus might be the result of a higher polyploidization capacity (as trigger for speciation) in the former tribe. As Table 2 shows, the frequency of ploidy levels differs con- siderably for the subgenera of Psychotria. Although in Neotropical members of Psychotria subg. Psychotria, ar are diploids, Psychotria subg. Heteropsychotria has a very high number of polyploids (nearly 65% of the counted species). The assumption of a relationship between frequency of polyploidization and number of species could even be valid for the whole Palicoureeae, as the percentage of polyploids in this assemblage is more than 60% (Kiehn, unpublished data). Annals of the Missouri Botanical Garden RUBIIDINAE I SENSU ROBBRECHT AND MANEN (2006) Anthospermeae. The only count from this tribe refers to a member of the genus Nertera Banks & Sol. ex Gaertn. The proposed inclusion of this genus into Coprosma J. R. Forst. & G. Forst. (Heads, 1996) is not supported by molecular studies (Anderson et al., 2001; Markey et al., 2004) and i sam result (2n — 44) as all earlier-counted collections of this widespread species (see survey in Kiehn, 1996; Kiehn et al., 2005). Rubieae. Members of two (Didymaea Hook. f. and Gal, gated in the current study. In Didymaea, the first count in the genus (for D. mexicana Hook. f.) revealed 2n = 22. By far the most frequent number in this tribe is x = n = 11, thus the result is not informative with regard to the taxonomic position of the genus. It does not, however, contradict a basal position of the genus within the Rubieae as indicated by molecular studies (Natali et al., 1996). The investigated Galium species is G. hypocarpium (L) Endl. ex Griseb., a species with a large distribution area from Central America to the southern part of South America and a member of the group formerly treated as the genus Relbunium Benth. & Hook. f. (Dempster, 1990). Three species of this Relbunium group have been counted so far: G. araucanum Phil., G. hirsutum Ruiz & Pav., and G. hypocarpium (L..) Endl. ex Griseb. Galium araucanum from southern Chile is diploid (Kiehn et al., 2005). Two ploidy levels are reported for G. hirsutum from Peru: diploidy (Huynh, 1965) and tetraploidy (Diers, 1961). For G. hypocarpium, there are three different ploidy levels known: diploidy (n — 11: Kiehn et al., 2005) from southem Chile, tetraploidy (2n = 44) reported here for a population from Costa Rica, and hexaploidy (n = 33: Huynh, 1965) from Peru. These results support the statement of Dempster (1990) in the context of the Relbunium group of Galium: “...since the counting of chromosomes has been of great taxonomic value with the North American species of Galium...it would almost certainly be valuable for the South American species as well." When comparing the morphology of the investigated collections of G. hypocarpium from Costa Rica and Chile, the Costa Rican plants (4x) are much stouter and more robust than the plants from Chile (2x). Thus, genera of this tribe ium L.) were investi- RUBIIDINAE II SENSU ROBBRECHT AND MANEN (2006) Spermacoceae s.l (including Hedyotideae p.p. and Manettieae). In rece ar circumscribed Hedyotideae (see survey by Robbrecht & Manen, 2006). The correct name for the emended tribe is Spermacoceae (Bremer, 1996; Andersson & Rova, 1999; Bremer & Manen, 2000). This tribe is the sister group to the Paleotropical Knoxieae sl. (Robbrecht & Manen, 2006). The presented new chromosome data further corroborate the predominance of x — 14 in the clade of the Spermacoceae s. str. They include first chromosome number reports for the genera Emmeo- rhiza Pohl ex Endl. and Hemidiodia K. Schum. (a genus included in Borreria G. Mey. or Spermacoce L. by some authors, see, e.g, Bacigalupo & Cabral, 1996), and for species of the genera Diodia L. s. str., Ernodea Sw., and Spermacoce (including Borreria). In the traditionally circumscribed Hedyotideae, new counts could be obtained for species of the genera Arcytophyllum Roem. & Schult., Bouvardia Salisb., and Manettia Mutis ex L. In Arcytophyllum, the new data indicate tetraploidy on x = 9. These results are in accord with the two earlier counts for the genus, both for A. thymifolium (Ruiz & Pav.) Standl., for which Diers (1961) reported 2n = ca. 30 and Lewis (1963: 17) 2n = 36. In Bouvardia, different ploidy levels (4x, 8x, and 12x) on x = 9 are now documented for B. ternifolia (Cav.) Schltdl. (see also Lewis, 1962). Further studies in this species seem worthwhile to investigate potential correlations of geographic or altitudinal distribution pattern of B. ternifolia with the different ploidy levels. In Manettia, x = 11 has been established as the basic number for two species. Also, the existence of the diploid level is clearly documen- ted now (for M. barbata Oerst.). Kiehn (1986, 1995) presented and discussed possible models for the origin of the predominant basic number x — 14 observed in the clade of the Spermacoceae s. str. All these models interpret x — 14 as a paleotetraploid state derived from a basic number existing in Hedyotideae. Chromosome num- bers reported for the Neotropical genus Galianthe Griseb. (2n — 32 and 2n = 30, see Daviña & Cabral, 1991; Kiehn, 1995) could be indicative for such a derivation: a descending dysploidy from a potential tetraploid ancestor exhibiting a basic number of x = 9. Unpublished molecular studies on the Spermaco- ceae s.l. (Dessein, pers. comm.) could be helpful in the context of this discussion. They suggest a position of Galianthe either within or at the base of the Volume 97, Number 1 2010 Kieh Chromosomes of Neotropical Rubiaceae Spermacoceae s. str. and indicate that Manettia and Bousardia often fall in a clade together with the rmacoceae s. str. The presence of taxa with basic numbers higher than x = 7 found in close proximity to or within the Spermacoceae s. str. gives further support for the hypothesis of x — 14 being the result of a descending dysploid series. CONCLUSION The reported data clearly show the significance of chromosome data in defining relationships on the species, genus, or even tribal level, especially when elvis about Neotropical Rubiaceae-Rubioideae in this paper, En are still huge gaps of knowledge remaining. Aside adding data for a not studied yet or E known (e.g.. further studies should be preferably related to taxa such as Bouvardia, where the existing data indicate that new counts, in combination with molecular. morphological, and spatial distribution pattern ana- lyses, can provide valuable contributions to an understanding of speciation and radiation 3 wet Literature Cited Anderson, C. L., J. H. Rova & L. Andersson. 2001. Molecular phylogeny of the tribe Anthospermeae (Rubiaceae): stematic and biogeographic implications. Austral. Syst. Bot. 14: 231-244. —( L. 2002. Relationships a sud en circumscrip- ions in e, Psychotrieae). Syst. & Geogr. Pl. 72: 167-202. & J. H. Rova. 1999. The rpsló intron and the phylogeny of the Rubioideae (Rubiaceae). Pl. Syst. Evol. Eae 161-186. Bacigalupo, N. M. & E. L. Cabral. 1996. Infrageneric si of Borreria ‘Rubiaceae Spermacocea on the basis of American species. Opera Bot. Belg. 7: Bir, S. S., G. Singh & B. S. Gill. — In A. Lóve € OPB chromosome number reports LXXXII. Taxon 33: 128-129. M w. H. Jr. 1968. Revision ea Bouvardia (Rubia- i i Gard. 55: Ned. pur Wetensch., Afd. Natuurk., Sect. 2, 48: 1-297. Remarks on the tion, the delimitation and iMd de of the Rubiaceae. rand n Neerl. 15: 1-33. Bremer, B. 1996. ee studies within Rubiaceae and relationships to other fami ies based on molec pies —J. B logeny y and classification n of the m Rubioideae (Rubiaceae). Pl. Syst. Evol. 225: Daviña, J. R. & E. Cabral. 1991. Recuentos cromosómicos cà (Rubiaceae). Bol. Soc. Argent. Bot. 27: Dempster, L. T. 1990. The genus Galium (Rubiaceae) in America. IV. Allertonia 5: 283-345. Diers, L. 1961. Der Anteil der Polyploiden in den Vegetationsgürteln der Westkordillere Perus. Z. Bot. 49: 437-488. Fagerlind, F. 1937. Embryologische, zytologische und ilie Rubi ceae nebst Bemerkungen über =a: e Polyploidiitspro- bleme. Acta Horti Berg. 11: 1: 55m Fritsch, R. 1970. C Kuba. I. ae adh 18: 189-197. Heads, M. J. 1996. Biogeography, taxonomy and evolution in the Pacific ginis Coprosma (Rubiaceae). Candollea 51: 381-405. tad M., M. Kiehn & A. Weber. 1994. Chromosome numbers of Malayan rain-forest Angiosperms. Beitr. Biol. Pi n 68: 51-71. Huynh, K.-L. 1965. Rubiaceae— Valerianaceae. In Contribu- tion à Pi M. oeste et embryologique E rou. Denkschr. Schweiz. Naturf. Ges. 89: 108-11 Janaki- wat E. K. je ae (Uragoga). P. 237 in arlington & E. Janaki-Ammal (editors), Atlas of cala Plants. George Allen € Unwin Ltd., London. Kiehn, M. 1985. ere mega Untersuchungen an aus Afrika, Madagaskar Messungen Rubiaceae und 1 Systematik dieser Familie. Ph.D. Dissertation, University of TO Vienna. Karyosystematische Unte Size ve nzahlungen in der Gattung Coe- cocypselum. 5. hromosome: Ósterr. Bot.-Treffen. Kurz. Referate u. Poster. Bot. Inst. Univ. Innsbruck. 1991. numbers of and karyological es on Paederia L. L. (Rubiaceae—Paederieae eae). Opera Bot. Belg. 3: 125-132. 1995. Chromosome survey of the Rubiaceae. Ann. Missouri Bo Bot. Gard. 82: . Chromosomes of Rubiaceae occurring in Md. gem Phili New Guinea, and the Pacific. put De "e 7: 249-260. & D. H 1996. Ch pea cultivated at the Botanical Garden, Kauai, Hawaii. Pacific Sci. 317-323. VM Jodl & G. e 2005. Chromosome ecce uan Fernández Islands, the Tristan da Cunha dris an from mainland Chile. eo Sci. 59: A e N E Hellmayr, J. Walter, J. ——— C. Justin A M. Mann. 1991. Beiträge zur Flora Österreich: Chromosomenzählungen. Verh. Zool. he Ges. pape 128: 19-39. Lewis, W. H numbers in North American Rubiaceae Batons 14: 285—. n Documented chromosome numbers of plants. Eie 17: 116-117. . 1966. Chromosome numbers of phanerogams 1. Ann. Missouri Bot. Gard. 53: 100-103. Markey, A. S., J. M. Lord & D. A. Orlovich. 2004. Coprosma tal romosome counts on National Tropical Sci. 50: brockiei: An oddball sheds am on the — P. 6 in SYSTANZ General Mee ng and Plant Species Radiation Workshop. Skotel, a yaken 12-13 Annals of the Missouri Botanical Garden February 2004. Ea WU), Ehren- NR 74922- 2-9 (WU); s, on Itacoatiara Rd., Ceplac Cacao Station, Eten e 2-1 (WU), rencias 74927-1-13 (WU). Bahia n Correntina, bei Veredáozinho (Dona Amelia) | 1 1- 1267 (WU), Gottsberger 13-2267 (WU), Gottsberger 15-2267 (WU), Gaiters 16-2267 (WU). [Rio Paranapiacaba Nat. Res., Ehrendorfer & Got 1312 (WU), Elrendorfer E Gottsberger 73822-602 (WU), Ehrendorfer & Gottsberger 73825-1312 (WU). Ehrendorfer & Gottsberger 73825-1319 (WU), Ehrendorfer & Gottsberger 73825-1324 (WU). RIBBEAN REGION. s. loc., seeds from HB Bonn (1983-1104), € in Ep sub RR 756, Kiehn RR 756 (WU). CHILE. Regi II [Atacama]: Provincia de Huasco, Estación Chuqi 1 Vallenar, Grau 2522 (Herb. Grau, M, WU) COSTA RICA. Alajuela: along rd. down from Poas Volcano, ca. s las outside a E Park, Kiehn et al. MK 920211-2/2 (WU); betw. P. MO von Lá Suiza), Kiehn & K -2/3 , Kiehn & Kiehn MK 2/6 (MO, WU); IL pr :1 CATIE bei urrialba, & Kiehn MK: O, WU), Kiehn & Kiehn MK 270786-1/1 (MO, SJ); kai: des CATIE, Regenwald im Tal des Río Reventazon, Kiehn & Kiehn MK Till s.n. (WU); Haziendá Florida Sur bei Turrialba, —: der Lá Montafia-Versuchsplantage, Kiehn & Kiehn 300786-1/3 (WU), Kiehn & Kiehn MK 300786-1/5 (WU; Km 84.5 on s 2' (Cartago-San Isidro del General, “Interamericana”), near Cerro Zacarales, Kiehn & Kiehn MK AULA (SJ. WU): ua e Turrialbe-Lá Suiza, ca. d Ciencias Agricolas entfernt in Richtung s Suiza. kurz vor der Brücke über den Reventazon, Kiehn & Kiehn MK ae (WU); Tapanti Refugio Nat. de Fauna Silvestre, near to the border ío Grande de Orosi, Kiehn & Kichn MK 880319-1/2 (MO, SJ, WU), Kiehn £ Kiehn MK 880319-1/8 (MO, WU) Yielaiide südl. des letzten Hauses von San Antonio, Kiehn & Kiehn MK 210385-1/9 en Heredia: Braulio Carrillo Natl. Park, Éstacion Carrillo at new rd. an José & Guapiles, -— & Kiehn MK e 1⁄1 (MO, SJ, WU). iehn & Kiehn MK 880309-1/3 (MO, WU), Kiehn & Kiehn Volume 97, Number 1 2010 Kiehn Chromosomes of Neotropical Rubiaceae MK 880309-1⁄4 (SJ, Nae Kiehn & Kiehn MK 880309-1/7 (MO, iehn & Kiehn MK 880309-1/11 (WU); bis Carilo Natl. Park, trail behind MINAREM station, Crex 9907-2 (MO); zwischen Porrosati und Sacramento, ca. 4 km vor Beginn des Natl. Park Braulio Carrillo am Fuß des Vulkan Barva, Kiehn & Kiehn MK 030485-1/1 (DUKE, WU); San Pablo de Heredia, Kiehn & Kiehn MK 160385-1/1 (WU). Limón: Cahuita, — Kiehn & Kiehn MK ide (WU); Tortuguero Natl. Park, base of arawa peak, Crex 9909-2 (WU), Heiselmayer 950212-1/1 (WU). Puntarenas: s Garabito, Ortgebiet von Jaco, Kiehn & Kiehn MK RR-90.21, Frimmel 8-90 (WU), Ta n MK 1/3 (MO, SJ, WU), hn & Kiehn MK 880316-1/4 (MO, WU); Monteverde Cloud Forest Prese ero uboso, Heiselmayer 950217-1/1 (WU), Kia MK 950217- 1/2 (WU); region Golfito, ca. 2 km E of La Gamba (Esquinas), or 950220-2/1 (MO), Huber - Weiflenhofer 9917-1 (MO, WU); region Golfito, ca. 2 k amba, Parque Nac. Pie Blancas, Seccion “Esquinas ue de los Austriacos, Bernhard & Greger HG2607083 ? (WU), Be Kiehn MK 961117-1/4 (INB, WU), Kiehn MK 961117-1/6 (INB), Kiehn MK 961118-2/1 (INB, WU), ate MK 961118- 4/1 (INB, WU), Kiehn MK 961118-4/2 (INB, WU), Kiehn MK 961119-2/1 (INB, WU), Kiehn MK 961119-3/6 (INB, si below entrance of Rincén de la Vieja Natl. Park, Heiselma im 5-3/1 (MO); Rincón de la Vieja Natl. Park, aa — L-] ` * (W Braulio ix Natl. Park, Valle Virgen, Crex 9915-2 (MO): nahe vo o La Palma, bei Lecheria Alto La Palma und Finca S ied Kiehn & Kiehn MK 030485-3/3 mi, Kiehn & Kiehn MK- 030485- 3⁄5 (WU); near Zurqui at nes rd. betw José & G atl Park, Kiehn & Kiehn MK 520909.2/1 (MO, SJ, aa wa & Kiehn MK 880309-2/2 (WU), Kiehn & Kiehn MK 88031 309-2/5 (SJ, T. Kiehn & Kiehn MK 880331-1/1 (SJ). A. s. loc., seeds from HB La Habana (Cuba) 1984- 1051, As in HBV, Kiehn 1984-1051 (WU); s. loc., seeds from HB La Habana (Cuba) 1984-1028, cult. in HBV sub RR 87-21, Kiehn RR-87- DOMINICAN rid IC El Seibo: A I abirmas. 5 km S of Miches to Nisibon hwy., on rd. t o Las me cult. in HBV sub RR-87-81, Zanoni et al. 15980 (WU); Eastern chez & Miches, = n FRENCH GUIANA. Rte. N2, Km 50, cult. in HB Meise sub no. 83-2784, Billiet 1860 (BR). MEXICO. s. loc., cult. in HB Kew sub no. 38-91201, Balls 5465 (K); native in the Botanic Garden UNAM, Mexico City, cult. in UCBG sub No. 75-665, cult. in HBV sub RR-916, Vogel et al. 1984-2-12/2 HB Góttingen 1986-1602, aps in HBV, Kihn 1986-1602 n Gua “Lagunas Lathrop Trail, W & NW of Smithsonian hrendorfer 6400-2502 (DUKE, WU); Canal Zone, Colorado Island: Wheeler-Armour Trail to Big fou. Ehrendorfer 6400- o PUERTO RICO. Ponce: NE of Ponce on rte. 139 at Km na oe e" (DUKE), de r 7087 (DUKE, WU). Punta, Taylor 7076 (DUKE), e erus n 77 (DUKE, WU). Utuado: Taylor 6935 (DUKE), Taylor 6938 oo 5A s. loc., 24 Mar. 1973, cult. in HBV sub RR 87-74, Echos s.n. (WU). VENEZUELA. Aragua: NW of Maracay, Tan Nac. Rancho Grande, ical bo Pass, Ehrendorfer 6400-5409 (DUKE, WU). ar: Km 116 along the rd. from rom Santa Elena de Uairén Ei Dosis nir La Escalera, at Salto El Danto, Till 16058 pd U), Till 16059 (WU); near Canaima, Ehrendorfer 74104-1- 9 (WU); cult. in HBV sub RR- ier 9, Ehrendorfer 74 A 9 (WU U); Quebrada Jaspe (Koko P. ará) along the rd. from Elena de Uairén to El Dorado, Till 16015 (WU); Santa Elena Sa Uairén, near the Ya-Koo hotel, Till 16063 (WU). Méri de las Flores, Ehre fe Me m 4003 —— m Teleferico Pico Espejo above Mérida, e ion II, La Montana, Ehrendorfer 5005 (DUKE, W WU, E A su . loe.: HB ib SA seeds pus HB Basel 1983- 1501, Kiehn 1983- ia (WU); seeds from HB Bonn 1983-1105, Kiehn 1983- 1105 (WU); seeds from HB Hauensis (Copen 1706, cult. in HBV sub RR 663, Kiehn RR 663 (W U): cult. in HB Kew a HB Oxford (No 11-00377), cult. in HBV : sub RR 95-04 RR 95-04 (W RECONCILING TAXONOMY AND Michael S. Mayer? and Lindsay Beseda? PHYLOGENY IN THE STREPTANTHUS GLANDULOSUS COMPLEX (BRASSICACEAE)! ABSTRACT -Previms studios hare postulated that the Streptanthus glandulosus Hook. complex Em LEM through don ates. - Here, w te patterns of interfertility, morphol ology, ITS, and chloroplast DN. A (cpDNA) eens of the phylogeny of this "d As a result, we oe | . single species S. sb with 10 Spiri i to . Populatio constitute the com north of the San Francisco Bay are now divided between two new su ndulosus subsp. a kapti “< through molecular — periamth « color, and fruit ate The name S. peramoen glandulosus subsp. glandulo is further lectotypifi M. S. Mayer ni. subsp. raichei M. S. Mayer, diagnosable us Greene is synonymized to S. words: cea cpDNA, ITS, IUCN Red List, phylogeny, Streptanthus. In the past 50 years, the Streptanthus glandulosus Hook. complex has received attention for a vari ety of reasons: bearing flowers both beautiful and atypical e w (e.g.. sesos, ns fi laments, thre ped and ch i inlal exhihiu Jo AAMC, SCrpentine endemism serving as a model for palas of a: sd divergence and speciation. Moreover, it has bee recognized as a natural group, albeit diverse, since the 1890s at latest (Greene, 1904). The group is mostly restricted to small outcrops of serpentine substrate in the California Coast Ranges, from Tehama County south to San Luis Obispo County, although a new taxon from southern Oregon has recently been described, Streptanthus glandulo- sus subsp. josephinensis Al-Shehbaz & M. S. Mayer (Al-Shehbaz & Mayer, 2008). Members of the complex are annuals with gomorphic perianths featuring a colored, urceolate calyx and petals that 3 and crisped, white margins. The morphological diversity among the populations, mostly in the form of perianth coloring, is bewildering. Past taxonomic schemes have recognized from one to 13 species in the group. The taxonomy currently in use recognizes three species and a number of infraspecific taxa (Table 1; Kruckeberg, 1958; Buck et al. Rollins, 1993). In 1957, Arthur Kruckeberg published the results of a large analysis of interfertility among the populations of the complex (Kruckeberg, 1957). He found a negative correlation between the linear distance separating two populations and the fertility of their hybrids. This classic paper demonstrated that "isolation by distance" could be a potent force in the divergence and speciation of groups of populations. He used these findings to support his revision of the taxonomy of the complex (Table 1; Kruckeberg. 1958), currently used in The a Manual: Higher Plants of California (Buck et al., 1993). hen we examined the ee genetics of the Streptanthus glandulosus complex using enzyme electrophoresis, the same correlation emerged be- tween geographic distance and genetic identities (Mayer et al., 1994). Subsequent phylogenetic studies of the chloroplast DNA (cpDNA) and ITS of 1 nuclear ribosomal RNA genes of the group echoed and refined these patterns (Mayer & Soltis, 1994, 1999). However, we also found the present taxonomic system at odds with the phylogenetic patterns we revealed. The present study was undertaken to reconcile this conflict. 1993; ' We are grateful to Arthur Kruc ckeberg, Ihsan Al-Shehbaz, pr qe C. Hollowell, Roy Buck, Roger Raiche, Robert Preston, Jon Rebman, and Beah Painter for helpful conversations, editori this study. Linda V curators of the following herbaria for hosting our visits and loaning us specimens: CHSC, n supported by a Faculty Research Crant by the ht of San Diego an Diego, San Daya. California 92110, U.S.A. Author for correspondence: diagnoses and the cura RSA, and SD. This project has bee Experience (SURE) grant provided oe of Biology, University of S; det 10.3417/2007010 populations included in and assistanc ce in locating the i ipt. We thank Mike Simpson for the Latin DS, J and a Summer Researc Undergraduate ANN. MISSOURI Bor. Garp. 97: 106-116. PUBLISHED ON 31 Marcu 2010. Volume 97, Number 1 2010 Mayer & Beseda 107 Taxonomy and Phylogeny in Streptanthus glandulosus Table 1. Comparison of taxonomic treatments for the Streptanthus glandulosus complex; the present study depicts S. glandulosus subsp. glandulosus sensu Kruckeberg (1958 distributed among three geographic clades depicted in Figure 1. Kruckeberg, 1958; Buck et al., 1993; I Rollins, 1993 Present classification Š. glandulosus S. glandulosus subsp. ulosus Southern clade subsp. glandulosus Northwestern clade subsp. raichei Northeastern clade subsp. arkii subsp. pulchellus var. secundus subsp. secundus var. sonomensis subsp. sonomensis var. hoffmanii subsp. hoffmanii S. albidus subsp. albidus subsp. albidus subsp. peramoenus syn., subsp. glandulosus S niger subsp. niger We have argued, as did Kruckeberg (1957), that the disjunctions among populations and the divergence among taxa of the complex were caused by vicariance rather than dispersal. The complex consists of the remnants of a widespread ancestral species, fitting the profile of a paleoendemic (Stebbins & Major, 1965). Fortunately for us, the gradual isolation of the regions within the range of the ancestral Streptanthus glandu- losus has been marked by the concomitant accumula- tion of molecular apomorphies, allowing the resolution of well-supported clades in the phylogeny (Fig. 1). Gene flow among populations within even the same variety or subspecies was estimated to be lower than is necessary to offset the effects of genetic drift (Mayer et al., 1994). Genetic variation within, and divergence mom, populations is high, again supporting à vicariant rather than dispersalist history for these widely disjunct populations (Mayer et al., 1994). We Suspect that as the range of the anc fragmented over time, regions and populations were subject to genetic drift and local selection pressures, causing divergence in floral color, plant size, and ence while retaining varying combinations of ancestral traits. Consequently, the ancestral species served as the progenitor of multiple derived lineages out its iti the group of remaining ancestral populations it paraphyletic. Such a paraphyletic progenitor has been termed a plesiospecies and any derived species an apospecies (Olmstead, 1995), because the latter is diagnosable via apomorphies, whereas the progenitor is defined by the sharing of plesiomorphic character states. This terminology seems apt for the Streptanthus glandulosus complex, with its combination of rare, regional taxa and the wide-ranging, highly disjunct S. landulosus subsp. glandulosus. We viewed the current taxonomic structure of the Streptanthus glandulosus complex (Kruckeberg, 1958) as a phylogenetic hypothesis to be tested. This paper will synthesize the available data, report the results of new sequence and morphological analyses, and make taxonomic revisions that recognize the dynamic biology as well as the strong phylogenetic patterns of this species complex. MATERIALS AND METHODS We rely largely on published data in this study. Interfertility data (Kruckeberg, 1957), cpDNA restric- tion site data (Mayer et al., 1994), and ITS sequences (Mayer & Soltis, 1999) are reviewed and, in some cases, regenerated or augmented by the addition of new populations and data. POPULATION SAMPLING The present study refers to populations analyzed by Kruckeberg (1957) and to populations studied in the cpDNA study (Mayer & Soltis, 1994), which attempted to sample, as close as possible, exemplars of the same populations as the Kruckeberg study. If ese populations could not be located or no longer existed, we sampled others that were relatively near. DNA of three to seven plants per population was pooled for the molecular work (Mayer & Soltis, 1994). The 29 populations (Appendix 1) represented here provide a good sample of the taxa and g i regions in the range of the complex (Fig. 1). We used Streptanthus polygaloides A. Gray as the outgroup for the analyses, as it had been successfully used for this purpose in earlier analyses (Mayer & Soltis, 1999). MORPHOLOGICAL STUDY We examined herbarium specimens of wild and greenhouse-grown plants to look for morphological pattems to compare with molecular phylogenetic patterns. Because flower color is not preserved well in herbarium specimens but carries significant weight in the diagnostic keys and species descriptions, we photographed the flowers of plants grown in the greenhouse from wild-collected seed. Nearly all populations are represented in this way. We examined PT PE E cdi b cH LI " visits: CAS, CHSC, DS, JEPS, OBI, RSA, SD, and UC. 108 Annals of the Missouri Botanical Garden v o 2 o Ë 2 s 2.0 2 S. g. gland., 105.4 t z S. g. gland., 561 19 [—— — S. glandulosus 100 S. g. gland., 562.4 subsp. arkii T S. g. gland., 563.4 ° * S. g. gland., 573 Hl o 6 = E S. g. gland., 565.4 š S. g. gland., 569 — S. glandulosus z š S. 9. gland. 79.4 subsp. raichei = 2 S. g. gland., 557.4 pes S. g. sec. hoff., 548.4 — — S. glandulosus S. g. sec. sono., 545.4 subsp. hoffmanii S. g. sec. sono., 546 o S. g. sec. sono., sena | 3 — p. sonomens > Moi wind i š S.g.sec.sec,543.4 | subsp. secundus > e = S. g. pulch., 537.4 S. glandulosus subsp. pulchellus 100 S. g. pulch., 539.4 i 99 2 = 5. niger, 535.4 E. S.glandulosus i subsp. niger 100 S. niger, 536 el 2 S.a.albidus 584.4 | — S. glandulosus = p. albidus S. a. pera., 585.4 - 3 S. a. pera., 303.4 š S. g. gland., 564.4 £ z S. a. pera., 582.4 ó — 5. glandulosus 15 S. g. gland., 583.4 subsp. glandulosus 100 99 S. g. gland., 587.4 uu I S. g. gland., 306 40 miles S. a. pera., 581.4 S. g. gland., 556.4 = ies CO fiha Q did in California, dicte taxonomic treqtrments: Mer hr terminals are identified pa E traditional hondo treatment and t mr 1958) and dis number (Ap; right, which is also related to to geographic origin on 8. or gland., glandulosus; hoff., hoffmanii; pera., the map. offm peramoen. lengths are noted Pe + benches Vaio ete frr restriction ch ues below branch i of 42. MOLECULAR DATA cpDNA restriction site data were generated by the study of Mayer et al. (1994), which assessed variation at 948 sites (ca. 3.6%) of the genome. ITS amplifica- tion and sequencing the present study followed the methods of Mayer and Soltis (1999), with the exception that ITS amplification products were purified using the GFX PCR Purification kit (Amer- sham Biotech, Piscataway, New Jersey, pendix 1) on the left and by the D traditional n e pre cen taxonomic treatment (Table 1) on the 1 zo albi. sono., sonomensis. Branch pomorphies, respective di Bayesian posterior us; pulch., pulchellus; sec. , secundus; site and ITS a es. The tree is rooted by S. polygaloides (not shown), which had a U.S.A.). Purified products were subjected to auto- mated sequencing using ABI 377 technology (Applied Biosystems, Foster City, California, U.S.A.) at the San Diego State University Microchemical Core Facility. Of the 29 ITS sequences of the complex analyzed herein (Appendix 1), 24 are new or have not been previously analyzed (12 of these from populations not analyzed in previous studies) and five were analyz previously (Mayer & Soltis, 1999). The combined data matrix for all 29 populations consists of 35 variable Volume 97, Number 1 2010 Mayer & Beseda Taxonomy and Phylogeny in Streptanthus glandulosus 109 cpDNA Boso sites mS apanerpbian on di to th e alienmen the branch g to th plus the alignment of ITS-1 and ITS-2 kanisha lich provides 62 variable positions within the complex. PHYLOGENETIC ANALYSES Sequences were aligned visually and were sub- jected to maximum parsimony analysis (with a bisection-reconnection [TBR] branch — bootstrap — (1000 replicates) by PAUP* 4 one (Swofford, 2001). Bayesian ig si ed the general time n (GT DNA substitution model option of MrBay s (Huelsenbeck & Ronquist, 2001), the ubi preferred by Modeltest 3.6 (Posada & Crandall, 1998). Four rate categories were set for the gamma distribution. MrBayes ran four simultaneous Monte Carlo chains for 1,000,000 generations, saving trees every 100 generations, but discarding the first 1000 trees (burn-in value) prior to constructing the consensus tree. RESULTS AND DISCUSSION PHYLOGENETIC PATTERNS The combined dun in of pma -— ITS sequence data reveals a among the populations of the Streptanthus glandulosus complex Fi d t (1958) taxonomy for the complex (Fig. 1). Although Kruckeberg’s (1957) patterns of interfertility among Populations of the complex were strongly correlated with geographic distance, the taxonomic structure he used (1958) was not. Consequently, the A E patterns show greater congruence with cl r- ship than with din: (Table 2). "o ced Populations of Kruckeberg's S. glandulosus subsp. &landulosus north of the San Francisco Bay proved to be closer phylogenetically to any population of any other taxon endemic to this region than to populations of subspecies glandulosus east or south of the bay (Fig. a ate wink poem M versus popu Pattern: average interfertilty is boues P " geographic P of populations than by taxonomic ELS (Table 2 de-based — of Kruckeberg's taxa and interferility (Table 2) depicts A of Strep- nthus glandulosus subsp. glandulosus from east and south of the San Francisco Bay on a well- supported of Krucke- berg's S. albidus Greene subsp. albidus and subsp. peramoenus (Greene) Kruckeb. (Fig. 1). Also, popula- Table 2. Mean interfertility among populations of the Streptanthus glandulosus complex.* S. gland. subsp. gland. NE S. gland. subsp. gland. NW S. gland. subsp. gland. S S. gland. S. gland. subsp. sec. var. sec. subsp. sec. var. sono. S. gland. subsp. pulch. S. niger S. albidus 86.3 (12, 16.3) S. albidus no data 17.5 (4, 22.2) S. niger S. glar 0) - 5.0 (2, 7.1) 5.0 (1 10.0 (5, 13.7) »sp. gland. S 87.8 (16, 24.2) 62.1 (7, 44.9) 6.3) - 3.6 (7 51.00 (5, 47.0) 0) 0 (1, 0) 0 (2 5.0 (3, 5.0) < — — d. su e 7? = AM wj g S| £ š ASE q Sj È = S k sa | 2, 133 alse WIE : a E E HE ii^ <| ° p Ë Ia = ec š š easi aN (eee cent. pt Š gait EE I — - Y i933: ta mie — A fool ese esis £33 zu 108 ITA ses s S E K j m. = «OO 5 ÉE Š cmm sse na E c | ° š BES sot Sas 427 es sig c S| E AE cos LER s = s| š 5: eca|25% an ps Š = “18 sË S š — | — Sis. <= < IRSE = £| š 2 É oam ess AMOS aga AT slt TS eoe-.isr . pes E] LLE TZ Y ccc ES š £ > š El + vx» 3 sik =e s ¿[33 š 2 1 TZ . Sw < 4 k | ç Z — . Š 51 5 2 < > > G > ë E : & $ «lg. Q a ag adj 23 3353 85. 22 2/2 3 UU ses sss|áAz-c ~ Å= Å= —7— 2 So Se sol. Ë S A uv zou 110 Annals of the Missouri Botanical Garden tions of Š. glandulosus subsp. glandulosus from northwest of the bay (the Northwestern [NW] clade, Fig. 1) showed higher interfertility with the varieties of S. glandulosus subsp. secundus (Greene) Kruckeb. of that region (variety secundus — 75.096, variety sonomensis Kruckeb. = 93.0%; Table 2) than with subspecies glandulosus from the southern counties (1.9%). Similarly, the two geographically proximate varieties of subspecies secundus (varieties secundus and sonomensis) had relatively low interfertility in the crossing study (68.5%), and in the molecular phylogeny it is ond that they are not sister taxa: variety secundus is sister to S. glandulosus subsp. pulchellus Crees) Kruckeb. (interfertility = 95.8%) and variety sonomensis is sister to subspecies glandulosus of the NW clade (interfertility = 93.0%, Fig. 1). Overall, most of the cases of low or high interfertility that were surprising in the context of the crossing study are not unexpected given the topology of the molecular phylogenies; a simply signify cases of disconnect between taxonomy and phylogeny of the group. — of the patterns of topology, geography, and rphology constitutes compelling evidence for the ubsp. glandulosus is highly paraphyletic and serves as a vivid example of a plesiospecies that has given rise to multiple narrow endemics. Because this taxon is distributed among three robust, geogra- phically structured clades of the molecular phylogeny Be. Ak impe IN, and NE n Fig. = we mark these clades and discuss beni in tum bekis. This shared history of Streptanthus albidus subsp. peramoenus and populations of S. glandulosus subsp. glandulosus east and south of the San Francisco Bay is suggested by morphological as well as molecular data. Flower color of subspecies glandulosus from this region varies from lavender and violet, which it shares with subspecies peramoenus, to dark maroon. The molecular phylogeny depicts both subspecies of S. albidus and all these populations of subspecies glandulosus on the same did clade, which we call the Southern clade (Fig. 1). The molecular divergence among members of this clade is minor, and several populations of the three taxa are indistin- guishable using the ITS and cpDNA data. Examina- tion of specimens, including greenhouse grown, of subspecies glandulosus from north of the bay versus those of the Southern clade (n = 82 and 87, respectively, unpublished data not shown), as well as S. albidus subsp. peramoenus (n = 40, unpublished data not shown) showed a combination of non-perianth features that align the southern subspecies glandulo- sus with S. albidus rather than with northern subspecies glandulosus. There is generally less pubescence in the Southern clade of subspecies glandulosus than in the northern clades, but the clearest distinction is seen in the shape of the mid- to upper-cauline leaves. In both S. albidus and southern subspecies glandulosus, these leaves are narrow, often folded and grasslike, and entire or with few, minute teeth. The northern clades of subspecies glandulosus typically exhibit broader leaves with small to large lobelike teeth. There is a greater similarity in average midcauline leaf length:width ratio of southern sub- species e (16.45, standard deviation dye. = 9.31) to that of subspecies peramoenus (19.7 * TBI uh to that of subspecies glandulosus a of the bay (NW clade: 4.40, SD = 2.51, n = 42; NE clade: 8.32, SD = 11.62, n = 40). Thus, despite perianth color similarity between some of the southern osed morphologically. On the other hand, S. albidus bs albidus, with its white to cream-colored perianth, is easily distinguished from the other taxa of the Southern clade even though it also lacks any observed molecular divergence from these taxa (Fig. 1). The NW and NE clades of Streptanthus glandulosus subsp. glandulosus, which are geographically contig- uous, are clearl resolved by a combination of angan qora md xm apa pios (Fig. 1). pattern of Dorados (Mayer et al., 1994). Kruckeberg (1957) informally recognized similar geographically based groups north of the San Francisco Bay: his North Coast group with rose-colored flowers in Sonoma and Mendocino counties, and his North Interior group with dark purple to blackish flowers found in the inner Coast Range regions to the east. Our molecular analyses indicate that Kruckeberg's North Interior group is actually split between the NW and NE clades we have identified (Fig. 1). Although the nuances of perianth color can be lost in dried specimens, plants of the NW and NE clades can be distinguished by fruit orientation, a feature that not been previously linked to geography or taxonomy within the Streptanthus glandulosus com- plex. Populations of the NW clade bear fruits that are recurved to reflexed at maturity, whereas those of the NE clade are ascending to erect. In both clades, the fruits themselves are qi to slightly curved, so the differences between clades are primarily due to pedicel orientation. Milia morphological patterns that coincide with the molecular-based clades include a modification of REA trends: the perianth colors of the NW clade include not only rose-pink, but deeper shades of magenta to maroon on the sepals and petals. The darker shades can be found following Volume 97, Number 1 2010 Mayer & Beseda 111 Taxonomy and Phylogeny in Streptanthus glandulosus veins of the petals or as solid coloring of the petals and parts of the sepals. Sepal color is most intense basally; the keel and tip of the sepals retain some green color at full anthesis. Flowers of the NE clade, however, exhibit a dark maroon-brown to blackish color on sepals and petals, and there is usually no visible green on the sepals at full anthesis. Identifying the perianth color differences between the NW and NE clades is difficult on dried specimens, which tend to lose the red and green perianth pigments and exhibit just shades of purple, brown, and straw. Finally, the leaves of the NW clade tend to be somewhat shorter and broader on average than those t the NE clade: means of midcauline leaf ength:width are 4.40 (SD = 2.51, n = 42) and 8.32 (SD = 11.62, n = 40), respectively. Tuin NW clade also gave rise to what Kruckeberg ) recognized as two varieties of Streptanthus glandulosus subsp. secundus, as variety sonomensis ma variety hoffmanii Kruckeb. (Fig. 1). This relation- ship is well supported on the molecular phylogeny and entirely consistent with geographical patterns; variety es is found in just a few populations on the " ern edge of the distribution of variety sonomensis. : mentioned ; above, variety sonomensis showed igher interfertility with nearby populations of sub- e glandulosus than it did with the type variety of subspecies secundus (Kruckeberg, 1957; Table 2). Its imi white to yellow perianth color, however, ^ rs it morphologically distinct from both taxa. t LK of the interfertility study, variety hoffmanii not yet been described, so specific interfertility cpDNA, and ITS sequence profiles. Morphologically, . T be similar to subspecies glandulosus of the is with a perianth colored rose to magenta. It is istinct, however, in its secund inflorescences. from each other and exhibit high interfertility E^. Table 2). Streptanthus niger, which consists just two populations on the Tiburon i a San Francisco Bay, is distinguished by eight lecular rphies a few i traits: an often flexuose raceme rachis, a highly constricted corolla throat, and a glabrous throughout. It also exhibits self-pollination and 2 greatly depressed interfertility with the other taxa of the complex. The combination of these eatures Was used as justification for species-level recognition for this taxon in Kruckeberg (1958). 1 "s revision most cro f any taxon with S. niger lead to a sterile Fl, but a few progeny did show fertility up to 10% (variety glandulosus), 20% (variety sonomensis), and 50% (S. albidus; Kruckeberg, 1957). In his study of interfertility, Kruckeberg (1957) set out to quantify the effect fg g phi isolati genetic divergence of populations; he developed legant and sturdy model of vicariance and diversification in the complex. His subsequent revision of taxonomy (1958) was pragr A LO p phyl He taxa We now propose a taxonomic revision in which named taxa are 1 .11 -L L a . Bat k; aul as L REVISED CLASSIFICATION OF THE STREPTANTHUS GLANDULOSUS COMPLEX hoth the glandulosus distinct lineages within it. The complex consists of a single species, S. glandulosus, comprising 10 subspecies. These taxa generally exhibit levels of morphological, geographic, and genetic divergence grealer than those suggested for the rank of variety (Stuessy, 1990), but less than ed for the rank of species. complex as well as the ically and geographically were recently elevated to subspecies, as S. glandulo- sus subsp. sonomensis (Kruckeb.) M.S. Mayer & D. W. Taylor and S. subsp. hoffmanii (Kruckeb.) M. S. Mayer & D. W. Taylor (Al-Shehbaz & Mayer. 2008). The previous taxonomic concept of S. glandu- losus subsp. included the three robust lineages of the Southern, NW, and NE clades in California, all of which merit recognition at the level of subspecies. The type of S. glandulosus was collected in Monterey and exhibits morphology most consistent with that of the Southern clade, and new ific epithets are proposed for the remaining two clades (Table 1). The morphological distinction of the taxon albidus, recognized as Streptanthus albidus Greene (Greene, 1887), is maintained herein, transferred as subspecies albidus within S. glandulosus (Al-Shehbaz & Mayer, 2008). Kruckeberg (1958) reduced another ies peramoenus species of Greene (1887) as subspec (Greene) Kruckeberg. However, this intergrades ogically with subspecies glandulosus and is le in the molecular data set largely indistinguishab 112 Annals of the Missouri Botanical Garden (Fig. 1). m peramoenus is therefore synony- mized u S. glandulosus subsp. glandulosus a o niger was recognized as pecies and transferred to S. glandulosus (AL Shehbaz & Mayer, 2008). It is distinct at the molecular level (Fig. 1) and is largely intersterile (but not entirely) with most other populations of the complex (Table 2). Although these features might constitute a rationale for species-level recognition, similar levels of intersterility and molecular distinc- be found in other populations of the complex (Kruckeberg, 1957; Mayer & Soltis, 1999). Moreover, were very ag ae in number (Table 2), leaving those measures weakly supported. Because human-mediated and possibly natural poo, sana to dione. populations il e emit surviving Rus alions nia even n the narrowest endemic is likely to increase over time. This prediction, san with ven low level of gene flow already present pulations of the complex, suggests that, dE hia complex consists of numerous incipient species. However, we feel that recognition of the 5. #lsmdulatu complex as Me Avena a aei s the paleoendemic S. t dynamic nature of this species iic which understandably might defy adequate representation by a static laxonomic structure. Taxonomic TREATMENT 1. Streptanthus glandulosus Hook., Icon. Pl. 1, pl. 40. 1836. Erysimum glandulosum (Hook.) Kuntze, Rev. Gen. 2: 933. 1891. Pie glandulosa (Hook.) Greene, Leafl. Bot. O| KEY TO THE SUBSPECIES serted and not recurved; Tiburon br Marin Ib. Plants sparsely hairy to hispid: “nto well (> 5 mm) exsert Inflorescences secund or 3a. Sepals white, cream, greenish white, or pale ellow 4a. Perianth cream to light greenish yellow with 5a. Petals 7-8 mm; fruits divaricate- j- 3b. Sepals rose to ik purp! glandulosus s su rachises Erin MUN Crit. 1: 82. 1904, as “Euclisia.” TYPE: U.S.A. California: Monterey Co., Monterey, 1833, D. Douglas s.n. (holotype, K not seen; isotypes, GH not seen, ) Annual; stems erect, 1—12 dm, simple or divari- cately branched just above the basal rosette, glab (and glaucous in some) to sparingly (rarely sl, hispid to the inflorescence, plants densely rosulate at first, basal leaves 5-12 cm, hispid, narrowly lanceo- late, tapering to a short, winged petiole, coarsely and sinuately toothed to MT pinnatifid, the teeth callus-tipped; cauline lea sessile, auriculate, narrowly oblanceolate, Nette dentate to + lobed, gradually reduced upward, becoming sessile, auricu- late, lanceolate-acuminate to linear and conduplicate, entire to + lobed; by anthesis basal and lower cauline leaves becoming deciduous and stems ultimately naked up to 2 or 3 nodes below the inflorescence. Flowers ascending to erect or secund, in single to several open erect racemes, some rachises flexuose; at anthesis flowers on pedicels 1-2 cm, spaced at intervals of 2-4 cm from base to apex. yx urceolate, sepals 4—9 mm, oval, glabrous or sparingly hispid, wholly or partly connivent, and strongly keeled; petals 6-15 mm, Lr and barely to well exserted, the crisped margins usually white, the adaxial pair th broad o! slightly to "ad recurved, longer than the abaxial, less recurved and narrower pair; stamens in 3 pairs, the adaxial with filaments connate to 0.5—0.75 their length, bearing sterile or scarcely polliniferous anthers, the abaxial ascending or divaricate, to arcuate and descending to reflexed; seeds oblong-oval, winged, 2-25 >x 1- 1.5 mm; cotyledons accumbent. OF STREPTANTHUS GLANDULOSUS IN CALIFORNIA AND SOUTHERN OREGON, U.S.A. la. e entirely glabrous; inflorescence rachises ica pedicels longer than the flowers; petals barely (2-3 mm) ubsp. niger (Greene) Al-Shehbaz, M. S. Mayer & D. W. Taylor s. av 1 oae "a L n 1 H rose or lavender-purple on sepal base or petal veins. curved inward; Josephin ne Co., Oregon E Jjosephinensis Al-Shehbaz & M. S. Mayer without purple v . sonomensis raid cun M. S. Mayer & D. W. Y. Taylor 6a. Perianth entirely rose de — fruiting pedicels 5-15 mm; fruits arcuate, spreading to reflexed; Sonoma Co. S. glandulosus subsp. hoffmanii (Kruckeb.) M. S. Mayer € D. W. Taylor . Volume 97, Number 1 Mayer & Beseda 113 2010 Taxonomy and Phylogeny in Streptanthus glandulosus 6b. ening Ma to en purple; fruiting pane 2-5 mm, fruits curved upward, divaricate E d : Marin C, os oreet reir Pda g. S. glandulosus subsp. pulchellus (Greene) Sae 7a. Plants 5-12 dm, euh ] nearly glabrous; perianth t ish white, with le tinge at b of sepals; rare, Santa Clam Crow IL ee iau. . T rs T [ues ctos inde la. S. glandulosus subsp. albidus (Gree ALSheas, M.S. Mayer & D. W. 7b. Plants 2-10 dm, surfaces diis perianth MER s: qin* . a mm 1h. S. idu raichei M. S. Mayer -10 de en oio leaves linear and conduplicate (length usually greater than s^ wi ath, s entire or with few minute teeth; th lilac-lavender to £e violet (rarel maroon); Coast Ranges: Contra Costa Co south to San Luis Obispo Co. ....- se i du DV. ps a eap, UR A EM SSE ti LI 1 } Thy | th. A od al e aa A E AA a posu p la. Streptanthus glandulosus subsp. albidus (Greene) Al-Shehbaz, M. S. Mayer & D. W. Taylor, Novon 18: 280. 2008. pue de Streptanthus 887. Euklisia abe Crit. 1: 83. 1904, as “Euclisia.” Sireptusithas glandulosus var. albidus (Greene) Jeps., Man. Fl. Pl. Calif. 419. 1925. TYPE: U.S.A. California: Santa Clara Co., hillsides 4 mi. S i San Jose, 30 Apr. 1887, Rattan s.n. (holotype, NDG not seen). Distribution and habitat. | Streptanthus glandulo- sus subsp. albidus is rare, possibly limited to serpentine substrate in Metcalf Canyon in the Mount Hamilton range in Santa Clara County, California (Appendix 1). Discussion. Plants of Streptanthus glandulosus subsp. albidus are among the tallest in the complex (5-12 dm) and are glaucous and nearly glabrous. The perianth is cream to cien white, with a purple tinge at the sepal base Ib. Streptanthus glandulosus subsp. arkii M. 5. Mayer, subsp. nov. TYPE: U.S.A. California: Napa Co., SE slope of Mt. St. Helena, 1946, Constance, J. F. Davidson, H. W. Wagner & R. H. Shan 3049 (holotype, UC!). Haec subspecies Streptantho gi Hook. subsp. loso similis, sed eo foli iocaulinis minus quam 5plo longioribus quam prog perianthio atroru- pureo usque nigello, sepalis sub ¡ plerumque non viridibus et siliquis ascendentibus usque erectis distinguitur. Plants 2—7 dm, sparsely hairy to hispid. Midcauline leaves oblanceolate and flat to conduplicate, length less than 5X the width, margins usually wi th small to large lobelike teeth. Inflorescences not secu rachises + + straight, pedicels shorter than the flowers. from dark maroon to blackish a ee ew eee ee ere nent (rarely dark violet), usually with no visible green on the sepals at full anthesis. Fruits are ing to erect. Distribution and habitat. Streptanthus glandulo- sus subsp. arkii has been collected from Colusa, Napa, edge of Sonoma County in California on outcrops of broken and decomposed serpentine, serpentine grass- lands, and roadcuts through serpentine and non- serpentine substrate (Appendix 1). IUCN Red List catego Streptanthus glandulosus subsp. arkii is A (VU C24[i]) according to IUCN Red List criteria (IUCN, 2001). In our assessment, S. glandulosus subsp. arkii is uncommon, exists in isolated populations, and is vulnerable to pressures itat degradation and urbanization. Discussion. Streptanthus e subsp. arkii is similar to S. glandulosus su p. glandulosus except that the length of ae be is less than 5X the width and the margins usually have lobelike teeth. Perianth colors, from maroon to blackish (rarely dark violet), are darker than the range of subspecies raichei, and fruits of subspecies arkii are ascending to erect, whereas those of subspecies raichei are recurved to reflexed. Etymology. The subspecific epithet honors Arthur R. Kruckeberg (1920-). a groundbreaking researc her in the evolution and ecology of serpentine plants : and a rous benefactor of the present project. town jet. on Peters 2333 (UC); Napa Co., burn below Conn . Raven x (UC); below Samuel Springs along Pope Creek on rd. from F. Hoover 4912 (UC); Solano Co., Vaca Mtns., W W. L "A 13410 (JEPS); So 1864, H. N. Bolander 3944 (UC); fias Ci. N of bur am 114 Annals of the Missouri Botanical Garden Colyear Springs Rd., 0.8 mi. W of Lowery Rd., 1991, V. H. Oswald & L. Ahart 4498 (UC). ptanthus k. subsp. glan dulosus, Icon. Pl. 1, pl. 40. p [dae peramoenus Greene, Bull. Teseey Bot. Club 13: 142. 1886, as "peramaenus," syn. nov. Strep- tanthus albidus Greene subsp. peramoenus (Greene) Kruckeb., Madroño 14: 225. 1958. TYPE: U.S.A. California: Contra Costa Co., Oakland Hills, 25 May 1886, E. L. Greene s.n. (lectotype, designated here, NDG not seen; duplicates, CAS not seen, GH not seen) Distribution and habitat. — Streptanthus. glandulo- sus subsp. glandulosus is uncommon, found mostly on serpentine, in grasslands, rocky slopes, and open woodland of the Coast Ranges from Contra Costa County south to San Luis Obispo County in California (Appendix 1). Discussion. Streptanthus glandulosus subsp. glan- dulosus is 2-10 dm tall, depending on site conditions. The midcauline leaves are linear and conduplicate, and the length is usually 10X the width, with margins entire or with few minute teeth. The perianth is lilac-lavender to blackish purple with little to no green on the mature calyx. The fruits are ascending to erect. Kruckeberg failed to locate the specimen cited above and in 1958 lectotypified a specimen collected by H. N. Bolander (H. N. Bolander s. n.) without stating a vues a deposit Later, i in — he examined L £L. type The —À of the bude specimen is currently unknow ec s protologue (1886: 142) mentions two specimens: “Oakland Hills; collected many years ago by Mr. Bolander, and again this year, by the writer.” Of these syntypes, Barbara Hellenthal at NDG (pers. comm.) did confirm Kruckeberg’s later annotation (“Feb. 1970”) as type on NDG 01877. Ihsan Al-Shehbaz (pers. comm.) further considered the Greene s.n. collection and the NDG sheet to represent the lectotype for the name, with isolecto- types seen by him at CAS and GH. Here, we maintain his opinion and designate the NDG speci- men as lectotype. ld. Streptanthus glandulosus s subsp. hoffmanii (Kruckeb.) M. S. Mayer & D. W. Taylor, Novon 18: 280. 2008. Basionym: Streptanthus glandu- losus var. hoffmanii Kruckeb., Madroño 14: 223. 1958. TYPE: U.S.A. California: Sonoma Co., Russian Gulch, 8 mi. S of Ft. Ross, moist soil of steep, rocky, nonserpentinized bank, 400 ft., 24 Apr. 1938, L. Constance 2155 (holotype, UC!; isotypes, GH not seen, MO!). Distribution and habitat. Plants of Streptanthus glandulosus subsp. hoffmanii are rare, known from a few populations on serpentine and non-serpentine substrate in the Russian Gulch and Austin Creek regions north of the Russian River in Sonoma County, California (Appendix 1). Discussion. Streptanthus glandulosus subsp. hoff- manii differs from S. glandulos which also occurs in Sonoma County, by secund inflorescences and a lighter rose to magenta perianth color. Fruiting pedicels are 5-15 mm, and fruits are curved down, spreading to reflexed. us subsp. raichei, le. Streptanthus glandulosus subsp. josephinen- sis Al-Shehbaz & M. S. Mayer, Novon 18: 280. 2008. TYPE: U.S.A. Oregon: Josephine Co., serpentine soil 6.9 mi. N of kp line on Happy Camp-O'Brien rd., 9 July 1 F. W. Hoffman Em 1 (holotype, MO uberi GH not seen, UC!). Distribution and habitat. Streptanthus glandulo- sus subsp. josephinensis has been collected only a few times on serpentine substrate around the type locality in Josephine County, Oregon. Discussion. x glandulosus subsp. jose- phinensis shares w glandulosus subsp. secundus secund cs BA a cream perianth color, but flowers of subspecies josephinensis produce petals 7- 8 mm long and divaricate-ascending fruit, whereas the petals of subspecies secundus are 10-17 mm and the fruit is spreading to reflexed If. Streptanthus glandulosus subsp. niger (Greene) Al-Shehbaz, M. S. Mayer & D. W. Taylor, Novon 18: 280. 2008. Basionym: Strep- tanthus niger Greene, Bull. Torrey Bot. Club 13: 141. 1886. Euklisia nigra S E Leafl. Bot. Observ. Crit. 83. as “Euclisia.” Streptanthus 22 var. E (Greene) Munz, Aliso 4: 91. 1958. TYPE: U.S.A. California: Marin Co., Point Tiburon, Apr. 1886, E. L. Greene s.n. (lectotype, NDG not seen). Distribution and habitat. A rare taxon, Strep- tanthus glandulosus subsp. niger is known to exist only in one area of serpentine grassland on the Tiburon Peninsula, in Marin County, California (Appendix 1). Discussion. Sireptanthus glandulosus subsp. niger is glabrous and produces flexuose racemes with dark Volume 97, Number 1 2010 Mayer & Beseda X 115 Taxonomy and Phylogeny in Streptanthus glandulosus maroon to black sepals; the petals are barely (2-3 mm) exserted and colored the same as the sepals but with erisped white margins; and the pedicels exceed the length of the flowers. lg. Streptanthus glandulosus subsp. pulchellus (Greene) Kruckeb., Madrofio 14: 222. 1958. Basionym: Streptanthus pulchellus Greene, Pitto- nia 2: ee Euklisia pulchella (Greene) Greene, Leaf. . Observ. Crit 904 as “Euclisia.” ee glandulosus var. pulchellus (Greene) Jeps., Man. Fl. PI. Calif. 420. 1925. TYPE: U.S.A. California: Marin Co., dry ridges on the S flank of Mt. Tamalpais, 7 May 1892, M. A. Howe s.n. (holotype, NDG not seen). ` Distribution and habitat. Streptanthus glandulo- sus subsp. pulchellus is rare, found only on serpentine substrate on Mount Tamalpais in Marin County, California (Appendix 1). Discussion. Plants of Streptanthus glandulosus subsp. pulchellus are 1-3 dm, among the shortest in the complex. The subspecies has a crowded, some- times secund inflorescence of red to reddish purple flowers, contrasting sharply with S. glandulosus subsp. secundus, which also occurs in Marin County, but has cream to pale greenish yellow flowers. lh. Streptanthus glandulosus esa raichei M. S. U.S.A. California: , Ukiah, 27 Ns 1905, W. L. Jepson 2508A Clon, JEPS). Haec subspecies Streptantho glanduloso Hook. subsp. glanduloso similis, sed ab eo foliis mediocaulinis minus retinentibus et siliquis recurvis usque reflexis distinguitur- Plants 2-10 dm, sparsely hairy to hispid. Length of midcauline leaves less than 5X the width. Inflores- cence not secund, rachises + straight, pedicels shorter than the flowers. Perianth color ranges from rose-magenta to purple (rarely maroon), either fully or with darker shades following petal veins; sepal color is most intense basally, the keel and tip of the sepals ly retain some green color at full anthesis. Fruits are recurved to reflexed Distribution and habitat. Streptanthus glandulo- California on outcrops of broken and decomposed Serpentine, serpentine grasslands, and roadcuts through serpentine and non-serpentine substrate (Appendix 1). IUCN Red List category. | Streptanthus glandulosus subsp. raichei is Vulnerable (VU C2a[i]) by IUCN Red List (2001) criteria. In our assessment, this taxon is ncommon, exists in isolated populations, and is collie: to pressures from habitat degradation and urbanization. Etymology. The subspecific epithet honors Roger Raiche us an eode field — à ne great asset to our ussion. odes ain subsp. rai- chei is similar to S. glandulosus subsp. glandulosus except that the length of midcauline leaves is less than 5X the width, rather than greater. Subspecies raichei lacks the fully secund inflorescenses typical of subspecies hoffmanii, which is rare but also found in Sonoma County. The fruits are recurved to reflexed, which distinguishes this subspecies from S. glandu- losus subsp. arkii. Paratypes. ges A. California: e Co, Highland reek, 1948, F. Hoffman 2336 Mendocino Co., Ukiah, head of S wis Creek, 1921, W. t len 9223 (JEPS); Sonoma Co., ut along Pine Flat Rd., 12.1 km N of Hwy. 128, 1991, M. Meir 579 (JEPS) li. Streptanthus glandulosus subsp. secundus (Greene) Kruckeb., Madroño 14: 223. 1958. Basionym: Streptanthus secundus Greene, FL 1891. Euklisia secunda (Greene) Greene, Leafl. Bot. Observ. Crit. 1: 83. 1904, as “Euclisia.” TYPE: U.S.A. California: Marin Co., N base, Mt. Tamalpais, 18 May 1886, E. L. Greene s.n. (holotype, NDG not seen). Distribution and habitat. Streptanthus glandulo- sus subsp. secundus is uncommon in Marin County, limited to the north slopes of Mount Tamalpais and adjacent Lucas Valley in California (Appendix 1). Discussion. Inflorescences of Streptanthus glan- dulosus subsp. secundus are secund and perianths are cream to light greenish yellow with rose or lavender- purple on sepal base or petal veins. 1j. Streptanthus glandulosus subsp. sonomensis Lesung M. S. Mayer & D. W. Taylor, Novon 8: 280. 2008. Basionym: Streptanthus glandu- Co., near Guerneville, Great Eastern Quicksilver Mine, serpentine, 8 June 1948, F. W. Hoffman 2323 (holotype, UC!; isotypes, GH not seen, MO!) 116 Annals of th Missouri ned Garden Distribution and habitat. Streptanthus glandulo- sus — sonomensis is uncommon and is found nantly on serpentine soils in Sonoma County, California (Appendix 1). Discussion. fiasco of paie glandu- losus subsp l, sepals are pale yellow, white, or ioni "tile. and petals are white. This subspecies lacks the reddish or purple coloring of the sepal base and veins shown by S. glandulosus subsp. secundus, which occurs in Marin County. Literature Cited Al-Shehbaz, l. A. & M. S. Mayer. 2008. New or noteworthy Streptanthus (Brassicaceae) for the Flora of North America. Novon 18: 279-282. "— = E., D. W. Taylor & A. R. Kru . 1993. 439—448 in J. C. fa Al r), The paa Manual: Higher Plants of California. University of California q rkeley. Greene, E. L. 1904. Certain han American Cruciferae. afl. res Crit. 1: 81-90. Huelsenbeek, J. P. & F. Sur e 2001. MrBayes: Bayesian of phylogenetic trees. 17: Bioinformatics WON: aL IUCN Red List Categories and Criteria, Version 3.1. Pre the IU cies Survival Commission. IUCN, Gland, Switzerland, and Cambridge, United King- dom. Kruckeberg, A. R. 1957. Variation in fertility of hybrids ns of the between isolated populatio serpentine species, Sergius Nat Hook. Evolution 11: 185-211 taxonomy of the species comple, Hook. Madroño zm 217-227. i MS et & P. S. Soltis. 1994. The Eng endemics: A cpDNA phylogeny o! f the Streptanthus glandulosus — D D P Bot. 19: 557-574. s Intraspecific phylogeny analysis usin nces Insights from ies of the Sian Me as co complex (Craciferae) Syst. Bot. 24:4 — dau" D. E. Soltis. 1994. The evolution of the Streptanthus glandulosus E ate EA e 288-1290. Oiti R. G. 1995. =a concepts and plesiomorphic es. Syst. Bot. 20: 0. Posada, D. & K.A. mdi 1998. Modeltest: eme T of DNA substitution. Bioinformatics Z 817-8 Hales, R c 1993. The ' Crucife erae of C. amily oon the Arctic to Panama. Stanford ont Press, Stanford, California. Stebbins, C. L. & J. Major. 1965. i and speciation in the California flora. Ecol. Monogr. 1-35 Stuessy, T. F. 1990. Plant Tax MEN Systematic Evaluation of Comparative Data. Columbia University , New York. Swofford, D. L. 2001. PAUP*. Phylogenetic t: I" Parsimony (*and Other Me thods), Versi . Sinau Associates, Sunderland, Massachusetts APPENDIX AS ene A > specimens used in analysis of ITS phylogeny. All s were collected in sequences dud: analyzed (Mayer & Soltis, 1999). D ep glandulosus subsp. albidus. U.S.A. Califor- : Santa Clara Co., E of Coyote, M. Mayer 584 [584.4, DQ829700 ]. Streptanthus glandulosus subsp. arkii. A. California: Colusa Co., Wilbur Hot Springs, Wilbur ace Rd., R. Raiche 105 [105.4, DQ829797]; Napa Co., Pope Valley Rd., M. Mayer 563 [563.4, Lake osa, Hwy. 128 roadside SE of dam, M. Mayer 573 [513, ITS-1: AF111405*, ITS-2: AF111406*]; Solano Co., Weldon Canyon Rd., M. Mayer 561 js d AF111351*, ITS-2: AF111352*); M. Mayer 562 [562.4, DQ829800]. ia hiis subsp. glandulosus. U.S.A. California: Alameda Co., Sunol Reg. Wilderness, above Alameda Creek, R. Raiche 306 [306, EF208035]; 1 km up creek adj. a Ba parking lot, M. Mayer 582 [582.4, ss oak Co., i Gate Rd., M. "sss 581 [581.4, DQ829792]; San Benito Co., Panoche Rd., 19 km S of Hwy. 25, M. Mayer 564 [564.4, 829796]; San Luis Obispo Co., Santa Rosa Creek Rd., M. Mayer 556 [556.4, DQ829785]; Santa Clara Co., Santa Teresa Hills, Calero Reservoir, R. Raiche 303 [303.4, DQ829784]; Mt. Hamilton, W of Lick Observatory, M. Mayer 583 [583.4, DQ829791]; Em € Glen Ayre Rd., M. Mayer 585 [585.4, DQ829798|; H em State Park, Corral Trail, M. i 587 [587.4, DO829 86]. hus glandulosus subsp. ua U.S.A. Cali- fornia: Tm Co., E ridge of The Cedars Canyon, M. E 548 [548.4, Streptanthus pl sis niger. U.S.A. California: Marin Co., Tiburon Pe SE of end of Mira Flores Ln., M. Mayer = [535.4 83]; Ti Peninsula, slopes beside St Hillary's- Church, M. Mayer 536 [536, ITS-1: AF111393*, ITS-2: AF111394* Streptanthus glandulosus mkin pulchellus. U.S.A. Cali- fornia: . Tamalpais, Bootjack Camp, M. Mayer Mt. Tamalpais, Carson Ridge, Pine Mtn. Trail, `M. Mayer 539 [539.4, DQ8297 188]. Sireptanthus glandulos . U.S.A. Califor- i i SII 101, M. Mayer 557 [557.4, DQ829795]; Feliz Creek Rd., W of Hopland, M. Mayer 565 d 4, DQ829794| Mountain . M. Mayer 569 |569, ITS-1: AF111397*, ITS-2: AFI ee Sonoma Co., Pine Flat Rd., N of Hwy. 128, M. Mayer 579 [579.4, DRUG 3]. Streptanthus us subsp. secundus. U.S.A. Califor- nia: Marin Co., Y km of S; EE. Ridge. : Mayer 542 [542, 1TS-1: AFI11381*, e AF111382*]; E end of Lucas Valley, M. I 543 [543.4, DQ829789]. anthus subsp. sonomensis. U.S.A. Cali- ma Co., irn Hwy., at crossing with Duvoul Creek, M. Mayer 545 [545.4, DQ829803]; rd. to The Cedars, 1 km E i i 546 [546, |; Guerneville, : I psam of Sweet- uu Se Rd., M. Mayer 549 [54 S, ec 1. Streptant polygaloides [AF111419, AF ion. (Mayer & Soltis, 1999). a al EPIPHYTIC GROWTH HABITS OF M. Fernanda Salinas,” Mary T. K. Arroyo,’ and CHILEAN GESNERIACEAE AND Juan J. Armesto* THE EVOLUTION OF EPIPHYTES WITHIN THE TRIBE CORONANTHEREAE! ABSTRACT monotypic and — Fu - PN Gesneriaceae (Gesnerioideae, Coronanthereae) occur in temperate rainforests of southern South Am epiphytic growth habits among these i. ee species were assessed. The Presence or absence of plants on t on the old-growth temperate rainforests of northern Chiloé Island (42°30' ia in Chile. An evolutionary int erpretation based on p wo o species of Chilean Gesneriaceae, Mitraria aon Ë k £ th coccinea Cav. and Asteranthera ovata (Cav. ) Hanst., gin main roots in the lary her emiepiphy tes. The third species, Sarmienta — Ruiz & Pav., "yaq found exclusively « on tree trunks and branches of livi yte. on reported phylogenies and biogeographical, ecological, and M data, the mechanically independent arboreal xe to be the ancestral condition in the Coronanthereae, which in turn gave rise to the climbing habit and finally A ene habit. This may be a common evolutionary pathway toward holoepiphytism within other lineages in Gesneri. Key vnm Asteranthera, Chile, Coronanthereae, Gesneriaceae, holoepiphyte, Mitraria, Sarmienta. Epiphytes are plants that use other plants (phor- Bromeliaceae; and (2) hemiepiphytes, which root on ophytes) as substrates, without drawing water or e ground during some stage of their life cycle nutrients from the living tissues of the phorophyte (Oliver, 1930). The latter can be further distinguished (Oliver, 1930; Barkman, 1958; Liittge, 1989; Benzing, into: (a) primary hemiepiphytes, which germinate n 1995). Among vascular plants, the epiphytic habit is the phorophyte and later send roots down to E e represented in 83 families and some 30, species ground, as in Ficus L. (Moraceae) peas ë -^ (Gentry & Dodson, 1987). Vascular epiphytes have — 1996) and members of the Araceae and — been subdivided based on Son in their life (Sandra ae al., po "e 0 seca — cycles into: (1) holoepiph tes, which never root in the — phytes, ET ground (Barkman, s 1 complete their entire life ^ upward onto dim phorophyte ins, Ls od cycle on the phorophyte, such as most of the epiphytic — Portillo et al., 2000). Some secondary hemiepiphy MEA partially s ia Fondo de Financiamiento de P n Excelencia en €— hag er de Desarrollo Científi ico y Tec co (FONDAP-FONDECYT) 1501 —— s š > Biodiversidad (IEB) Ecologío y Biodiversidad AEN, "Pontif icia pr Católica de Chi Instituto ps Tee mnoVigien (CONICYT). qe ICM, P05-002 ICM); and AT-4050069 Comi Nacional de Investigación Cie je fo lord su n. A F.S. thanks CONICYT, IEB, and "nen de Posgrado y Posto, Universidad de ( Chi e f or fellow: ip ppa grant from Equi We ea enabled M.F.S. — MEL, AK, and NOU € and field sites in Australia, New — and New Caledonia. rm Tomás Abud for field assistance; Katia Velásquez and Innes Hannig for allowing us to — t = rh 2 preserved forests; and Pablo Necochea, — Gaxiola, and Felipe gora we eh nat ci C. podamental literature. Constructiv iiie si — Em da Darwi n Biological Station, Ancud, Chiloé. M.F.S. on, and Mark J. — (MEL) penes X memory of our friend o Farfán. This work is part of Ciencias Universidad de Chile in d Posta u Mayas ua . d de Ci Biológicas, Pontificia enter for Advanced Studies in Ecology and Biodiversity (CASEB), Faculta i hah etus n m n i Católi Alameda 13677, Casilla 114-D, Santiago, Chi x “nso de Beck y a (IEB), Facultad de Ciencias, U sd de Chile, Casilla 653, Ñuñoa, finum doi: 10.3417/2006210 Ann. Missouri Bor. Garp. 97: 117—127. PUBLISHED ON 31 March 2010. 118 Annals of the Missouri Botanical Garden Flowers and fruits of the gu monotypic genera of the var yn inel e present in central- - Sa rmienta Figu ide Chile and adjacent Argentina. —A occinea Cav ovata pas Hanst. —D. Sarmienta repens fiit —E. Mitraria coccinea fruit. LE ln ovata Fit. Scale bars in = ] cm repe are s when young, if no support is available (Moffett, 2000). It is widely accepted that the epiphytic habit evolved independently in different vascular plant lineages (Benzing, 1987; Gentry & Dodson, 1987: Kremer & van Andel, 1995). Colonization of the canopy habitat has occurred repeatedly, as in the Orchidaceae, where obligate twig epiphytism has evolved several times (Gravendeel et al., 2004). In the Bromeliaceae, Pittendrigh (1948) proposed that epiphytism evolved independently within the sub- families Tillandsioideae and Bromelioideae, and Crayn et al. (2004) greatly clarified the origin of the epiphytic habit within Bromeliaceae by conducting a phylogenetic analysis of nucleotide sequences. The epiphytic habit within Bromeliaceae evolved a mini- mum of three times within the family (Crayn et al., 2004). However, the origin of epiphytes should not be considered a labile character (Wilson & Calvin, 2006) because reversals to the terrestrial habit are not common. To our knowledge, only one hypothesis has been proposed to explain the mechanisms associated with the origin of ee by means of hemiepiphytic intermediaries. Bews (1927) recognized the appear- ance of the climbing habit very early in the evolution ns Ru B. Mitra . Asteranthera iz & Pav. of angiosperms, as woody lianas are abundant in many ancient orders and families and in the fossil record. Bews (1927) also suggested that the evolution of holoepiphytes is in many cases connected with the lines of development of lianas. Temperate rainforests of southern South America are characterized by a high peep and biomass of vascular epiphytes (Armesto et al., rroyo et ., 1996; Muñoz et al., 2003). The I history of the biogeographic isolation of the temperate rainforest biota in southern South America is reflected in high levels of local endemism, 8796 of the woody flora (Arroyo et al., ; Villagrán & Hinojosa, 1997), which also characterizes many of the epiphytes (Arroyo et al., 1996). However, no previous study has addressed the origin of the habit in epiphytic lineages represented B. by species in these rainforests. Among the vascular epiphytes of Chilean temperate rainforests, three endemic mono a of pou" frequent components of the canopy. Asteranthera ovata (Cav.) Hanst., Mitraria coccinea Cav., anc Sarmienta repens Ruiz & Pav. (Fig. 1) have memes been considered as tes or climbing shrubs in the scientific lienem Sini further precise defini- Volume 97, Number 1 Salinas et al 119 2010 Evolution of Epiphytes in Coronanthereae Table 1. References to the growth habits described in the li for th demic epiphyti ies of G from southern Chile. Most authors recognize all speci i imbi ila, ipsias di ca ta E in gn pecies as epiphytes (s.l.) or climbing shrubs, ignoring differences in their Habit description Asteranthera ovata Mitraria coccinea Sarmienta repens Climbing shrub rooting in the ground 1 1 Strictly epiphytic shrub 1 Epiphytic shrub 2 2 2 Facultative epiphyte 3,8 Climbing shrub 4, 6 4, 6 4 Epiphytic climbing shrub Epiphyte 6 5, 8, 10, 11, 12 5, 10, 11, 12 5, 8, 10, 11, 12 q 7 7 * Numbers in the table correspond to the following ref i i i t g references: (1) Reiche, 1898; (2) Muñoz, 1959; (3) Rivero & Ramírez, E (4) Muñoz, 1980; (5) Villagrán & Armesto, 1980; (6) Hoffmann, 1982; (7) Wiehler, 1983; (8) Gentry & Dodson, 1987; (9) vero, 1991; (10) Smith-Ramírez, 1993; (11) Smith-Ramírez & Armesto, 1994; (12) Armesto et al., 1996. Climbing vine, epiphyte Subshrub, epiphyte tion (Table 1). No study has quantified variation in the STUDY SITES growth habits or substrate use within or among species. It is possible that epiphytic growth habits an a The percentage of frequency of the occurrence of differ among these species, as noted more t rooting on the ground and on phorophytes was century ago by Reiche (1898). MATERIALS AND METHODS STUDY SPECIES The Gesneriaceae family is mainly tropical and subtropical in distribution, comprising about 120 genera and 2500 species (Cronquist, 1981). Species in the Gesneriaceae include herbs or half shrubs, shrubs or small trees, and lianas or epiphytes (Cronquist, 1981). About 20% of the Gesneriaceae are epiphytic, ranking among the top 10 vascular plant families in terms of absolute number of epiphytic species (Gentry & Dodson, 1987). Gesneriaceae are represented in the Chilean temperate rainforests by Sarmienta repens, Mitraria coccinea, and Asteranthera ovata (Fig. 1, Appendix 1). These three species attach to trees by adventitious roots at the nodes and have reddish tubular flowers pollinated mainly by the hummingbird Sephanoides sephaniodes Lesson (Rivero, 1991; Smith-Ramirez, 1993). At the end of the summer and during the fall, they produce inconspicuous, greenish berries (Fig. ID-F) with numerous small seeds. Sarmienta Ruiz & Pav. (Fig. 1A) frequently grows on the branches of phorophytes. The leaves of Sarmienta are succulent and mainly glabrous, while the leaves of Mitraria Cav. and Asteranthera Hansl. are thinner an have higher trichome density. Mitraria (Fig. 1B) often grows as a twiggy shrub on trees, whereas Asteranthera (Fig. 1C) grows tightly attached to tree trunks, its flowers occur close to the stem, and it is often found creeping on the forest floor and logs. assessed in Sarmienta, Mitraria, and Asteranthera in two old-growth stands of North Patagonian rainforest (sensu Veblen et al., 1995) located in the lowlands of northern Chiloé Island, Chile (Fig. 2): (1) Fundo Los Cisnes, Caulin, and (2) Senda Darwin Biological Station, El Quilar. The prevalent climate is wet- temperate, with a strong oceanic influence (Di Castri & Hajek, 1976). Meteorological records (1996-2004) at Senda Darwin Biological Station indicate a mean annual rainfall of 2124 mm and a mean annual temperature of 8.7°C. The mean maximum monthly summer temperature is 17.5%, and the mean minimum monthly winter temperature is 2.5°C. Evergreen broad-leaved trees and a few narrow- leaved conifers dominate the rainforest canopy in both stands. Nothofagus nitida (Phil.) Krasser (Nothofaga- ceae), Podocarpus nubigenus Lindl. (Podocarpaceae), Saxegothaea conspicua Lindl. (Podocarpaceae), Eu- cryphia cordifolia Cav. (Cunoniaceae), and Weinman- nia trichosperma Cav. (Cunoniaceae) shape the emergent layer over 25 m tall (Table 2). Drimys winteri J. R. Forst. & G. Forst. (Winteraceae) and Legrand Kausel, Tepualia stipularis (Hook. & Arn.) Griseb. (Myrtaceae), and Caldcluvia paniculata (Cav.) D. Don. (Cunoniaceae) are abundant also in the lower canopy and understory of the forest (T. able 2). Other vascular epiphytes in these rainforests included iaga polyphylla (Hook.) J. F. Macbr. (Luzuriagaceae). Fascicularia bicolor (Ruiz & Pav.) Mez (Bromeliaceae). and 12 species of filmy ferns (Hymenophyllaceae) (Salinas, 2008). The ground is 120 Annals of the Missouri Botanical Garden Q, Ew gure Š Geographic location of study sites in northern Chiloé Island. Arrow in the inset box shows Chiloé Island in merica. Narrow lines show Senda Darwin n Biological Station (SD), near El Quilar, Ancud, and Fundo Los — em at the locality of Caulín Table 2. Parameters of 0.1-ha. permanent plots sampled in North Patagoni inf f northern Chiloé Island, Chile. Tree stems measured had more than 5 cm DBH. Stand code SD 1 SD II FCI FC II Total basal area (m? 71.8 804 97 115.1 0.1 ha.~’) Density of trees 334 225 235 277 (individuals 0.1 ha.~') No. of tree species 9 12 11 13 Mean DBH (cm) 12.5 14.1 15.8 16.0 Maximum DBH (cm) 109.4 127 148 129 ain emergent tree Nothofagus nitida, Podocarpus nubigena, “P. nubigena, Saxegothaea N. nitida, species ne W. trichosperma, conspicua, Eucryphia E. cordifolia, richosperma N. nitida cordifolia S. conspicua Main canopy tree Meis stipularis, T. stipularis, D. winteri, Amomyrtus S. conspicua, species imys winteri, D. winteri, luma, A. meli A. luma, Caldcluvia C. paniculata D. winteri paniculata Abbreviations: SD I, Senda Darwin E; SD IL Senda Darwin II; FC I, Fundo Cisnes I; FC H, Fundo Cisnes II. Volume 97, Number 1 2010 Salinas et al E 121 Evolution of Epiphytes in Coronanthereae covered with abundant woodfalls, often covered by a carpet of bryophytes, filmy ferns, and lichens. FIELD SAMPLING Within each forest stand we set up two 50 X 20-m plots (Fundo Cisnes I, Fundo Cisnes II, Senda Darwin I, Senda Darwin II). Each plot was located at least 200 m away from any forest edge and was free of signs of recent human disturbances such as fire or clearcutting. Total basal area per plot was calculated as X (n X [DBHp) / 4 per tree. Sampling plots did not differ statistically in terms of total basal area and density of trees, number of tree species, and mean tree H (3? — 4, df — 3, P > 0.05 for all cases). Within each plot, we conducted two surveys. Coronanthereae on the forest floor. To determine the frequency of each species on the forest floor, within each plot, four equidistant 50-m-long transects were traced. Along each transect, 25 quadrats of 1 m^ were quadrats were sampled within the four 50 X 20- m? plots in two old-growth North Patagonian forests. Frequency and rooted substrate of Coronanthereae o characterize the frequency of eac Gesneriaceae species on trees, their presence or absence on all trees greater than 5 cm DBH within each forest plot was recorded, while the presence of epiphytes on trunks, branches, and on the crowns of trees was checked with Pentax (Tokyo, Japan) 12.5 X 50 DCF SP binoculars. To characterize the rooting substrates, the epiphytic stem toward the base of the tree was carefully followed. If the plant was rooted on the ground, it was recorded as a hemiepiphyte. When the epiphytic stem did not reach the forest floor, the plant was recorded as a holoepiphyte. A total of 1071 trees greater than 5 cm DBH within the four plots of old-growth North Patagonian forests were survey le 2). on trees. DATA ANALYSIS Randomizations of data using RT 2.1 (Otago, New Zealand; Manly, 1997) software were performed because frequencies had non-normal distribution. The the ground and on trees was compared independently. while one-way ANOVAs with 10,000 randomizations of the data were performed. The proportion of each species the forest fl d using the 16 transects eo as replicates. The proportion of trees showing each on la as replicates. Mann-Whitney U tests were performed for post-hoc analysis. BIOGEOGRAPHIC AND PHYLOGENETIC DATA FOR CORONANTHEREAE Available phylogenetic (Smith et al., 1997; Wang et al., 2002; Mayer et al., 2003), systematic, ecological, biogeographical, and morphological information for the species in the Coronanthereae (Bentham, 1869; Reiche, 1898; Petrie, 1903; Guillaumin, 1948; Allan, 1961; Morley, 1978; Morley & Toelken, 1983; Wiehler, 1983; Nicholson & Nicholson, 1991; Walsh & Entwisle, 1999; Friedman et al., 2004) and field observations of Fieldia australis A. Cunn. (Victoria, Australia), Rhabdothamnus solandri A. Cunn. (Auck- land, New Zealand), Coronanthera sericea C. B Clarke (Mont Koghi, New Caledonia), and C. clarkeana Schltr. (Plateau de Dogny, New Caledonia) for generating hypotheses about the evolution of the epiphytic habit within the tribe. RESULTS FREQUENCY DISTRIBUTION AND ROOT SUBSTRATES Coronanthereae on the forest floor. Differences in the frequencies of the three species of Gesneriaceae on the forest floor were found (one-way ANOVA with randomized data, P < 0.001). Mitraria and Asteranthera were found to root on the ground in both forest stands (Fig. 3A). In contrast, Sarmienta was not found on und quadrats in either of the two forest stands (Fig. 3A). Müraria had a mean frequency on the ground adrats of 0.31 per transect and was more frequent than Asteranthera (Mann-Whitney U test, Z — 292, P « 0.005), which had a mean occurrence of 0.15 per transect (Fig. 3A). Both M. coccinea and A. ovata were significantly more frequent than S. repens on the forest oor (Mann-Whitney U test, P < 0.05 in both cases). Growth patterns on the ground differed: Mitraria was able to grow without support for up to 10-20 cm in height on the forest floor, and erect stems were ted 10-50 cm from others and were connected by buried lateral shoots. Instead, Asteranthera had a creeping habit on the ground and was never found growing erect more than 10 cm in height on the ground. Frequency and rooted substrate of Coronanthereae on trees. No statistical diff in the proportions o trees bearing each Gesneriaceae species was found (one-way ANOVA with randomized data, P = 0.0829). Mitraria (n = 297) occurred on a proportion of 0.29 of IXO Stau 122 Annals of the Missouri Botanical Garden B : + i b -" a gi > 2 | H F 1 3 30 32525 4 iii F H - 5S 20 | 5 1 ped 258 2 2 #8 4, y pe 18-3 3- nm" Hs dh 10 ÉS | A È S [E u 5 i a Sarmientarepens Mitraria coccinea ^ Asteranthera ovata Sarmienta repens Mitraria coccinea Asteranthera ovata fq. 1 Figure 3. A Patagonian rainforests, N = 8 transects within each si the forest floor (o). —B. r bsent from the ground (a), while Mitraria cocc ] sh fs Narth ite, ‘N= 25 re aun per transect for a total of 400 e inea Cav. was species on the forest ground (b), and Asteranthera ovata (Cav.) Hanst. was less frequent than M. coccinea on ean percentage of trees with Coronanthereae epi — 2 plots, 0.1 ha. at each forest stand. Sample size, N — 1071 eum Same letter (a) above bars indicates no statistical diffiimoes i in frequenc rando iphytes within two North Patagonian rainforests, ncy on trees among Coronanthereae s pecies (ANOVA with mized data, P > 0.05). — different frequencies between species were found only on ide forest ded Epiphytic M. coccinea and A. ov while epiphytic S. repens was never found. rooted o trees pe th = DRUHU I 1 = 139) occurred on a proportion of 0.14 of trees sampled (Fiz 3B). A (n = 40) had the lowest proportion of 0.04 on trees sampled (Fig. 3B). Differences in the rooted substrates of the epiphytes rowing on trees were revealed. Only Mitraria and Sc root ] and Sarmienta (n epiphytes, germinating and growing on the floor and climbing on trees afterward. In contrast, Sarmienta did not root on the ground, and thus Sarmienta may be classified as holoepiphyte, germinating on trees and not rooting on the ground. BIOGEOGRAPHY AND PHYLOGENY OF CORONANTHEREAE The Ce xonanthereae consists of nine genera and 20 ly, Coronanthereae has received considerable attention in discussions related to the origin of the Gesneriaceae (Weber, 2004). The tribe is resent in the southern South American temperate rainforests of Chile and adjacent Argentina, mainly in the North Island of New Zealand, Lord Howe Island, and in the provinces of Queensland, Victoria, and New South Wales in Australia. monotypic (Table 3). Depanthus ven genera are S oe with two species, and ping Vieill. ex C. B. Clarke, with 11 species, are eta to New Caledonia (Table 3 - Only one species of Cor O- nanthera is present in the Solomon Islands (Wiehler, 1983; Table 3). Present-day distribution patterns and available fossil evidence of Gesneriaceae from south- ound always rooted on the gro und and were classified as secondary hemiepiphytes, n the ground x was classified as holoepiphyte. em South America (Villagrán & Hinojosa, 1997) suggest an ancient clade that precedes the breakup of Gondwana (Dalziel, 1992). The elevated proportion of monotypic genera (78% of the genera) and the endemism of species to isolated and restricted areas (Table 3) support the contention that current Cor- onanthereae represent relictual taxa of a more diversified group in the past (Burtt, 1963, 1998; Wiehler, 1983; Weber, 2004), which was affected by subsequent extinctions (Wiehler, 1983; Weber, 2004) Phylogenetic studies and isocotylous seedlings support the position of the Coronanthereae within the Gesnerioideae (Burtt, 1963; Smith et al., 1997; Wang et al., 2002; Mayer et al., 2003) in a fairly basal position (Wang et al, 2002). Our literature review indicated a diversity of growth habits among living species of Coronanthereae, varying from trees to holoepiphytes. Among genera, the functional stamen number in the flowers varied from two to five, and the fruit type varied from a dehiscent capsule to a fleshy fruit. All species within the Coronanthereae occur in rainforests, ranging from tropical to temperate regions ) (Table 3 Discussion EPIPHYTIC HABITS OF SOUTHERN SOUTH AMERICAN GESNERIACEAE Mitraria and Asteranthera are considered secondary — as they were regularly found as terrestrial plants as well as epiphytic climbers with Volume 97, Number 1 2010 Salinas et al. ; | f 123 Evolution of Epiphytes in Coronanthereae Table 3. Number of species, geographic distribution, habitat, habit, stamen numbers, and fruit characteristics of nine genera in the gesneriad tribe Coronanthereae.* Species Geographic Stamen Genus number distribution Habitat Habit number Fruit type Depanthus 2 w Caledonia montane forest tree 5 capsule Ne, 1 Lord Howe Island montane forest tree 4 iit le Coronanthera 11 New Caledonia, montane forest tree 1 siue Solomon Islands Rhabdothamnus 1 New Zealand, North montane forest shrub 4 capsule an Lenbrassia L Australia, Queensland rainforest 4 berry Fieldia 1 Australia, Victoria and montane rainforest 4 berry ales hemiepi Asteranthera 1 Chile and adjacent temperate rainforest masan berry Müraria 1 ud — — ile and adjacent temperate rainforest berry Argentina hemiepiphyte Sarmienta 1 Chile temperate rainforest E. 2 berry * Modified from Whieler (1983). the main stem rooting on the forest floor. As noted in many other species of Gesneriaceae, both species showed that the development of lateral shoots on the prostrate stem may lead to multiplication and to the patchy habit (Weber, 2004). In contrast, Sarmienta was never found rooted on the ground and hence is not a terrestrial plant, but rather a holoepiphyte. These results support early observations reported by Reiche (1898). EVOLUTION OF Considering stamen number in genera of Coro- nanthereae (Table 3), there appears to have been at least two reductions in number within the tribe. From a putative ancestral number of five functional sta- mens, as present in Depanthus, a first reduction of one stamen to staminoid is present in seven genera within Coronanthereae (Table 3). A second reduction has taken place in the lineage, now present in the flowers of Sarmienta, which have three staminodes, two longer than the third (Reiche, 1898), and only two functional stamens (Table 3), which support two reductions to staminodes in the lineage of Sarmienta. The presence of rudimentary, reduced, or functionless structures has traditionally been used to establish the direction of evolutionary change since de Candolle (1813). The 5-stamen condition present in Depanthus flowers has traditionally been regarded as a secondary acquisition within the lineage (Wiehler, 1983; Weber, 2004), a hypothesis that has never been challenged or demon- strated. However, considering the relative ances position of Coronanthereae in Gesneriaceae (Burtt, 1963; Wiehler, 1983; Smith et al., 1997; Wang et al., 2004; Weber, 2004), five functional stamens could likely represent the ancestral condition for the family. Within the Gesneriaceae, fleshy fruits are consid- ered a derived fruit type with respect to dehiscent capsules (Wiehler, 1983). Within the Beslerieae and Napeantheae, lehi t capsules I b described as ancestral contrasting with the derived state of fleshy fruits (Smith, 20003). The sister family considered ancestral to Gesneriaceae, the Calceolar- iaceae (Soltis et al., 2005), also presents dehiscent capsules, which would support the ancestral character of dehiscent capsules across the entire Gesneriaceae. Within Coronanthereae, genera bearing dehiscent capsules seem to have maintained the ancestral character state (as in Depanthus, Coronanthera, Negria F. Muell., and Rhabdothamnus A. Cunn.). Fleshy fruits, present in the Australian Fieldia A. Cunn. and Lenbrassia G. W. Gillett, and in the South American Asteranthera, Mitraria, an Sarmienta (Table 3), may have originated at least once within the tribe, potentially representing a derived character. Growth habits within the living genera of Coro- nanthereae include trees (Depanthus, Negria, Coro- nanthera, and Lenbrassia), shrubs (Rhabdothamnus), climbers (Fieldia, Mitraria, and Asteranthera), and holoepiphytes (Sarmienta, Table 3). At least three reductions in vegetative size associated with shifts in growth habits seem to have occurred within the Coronanthereae. One trend would have been from the arboreal condition to the shrub habit. Another trend is the reduction in stem thickness from the arboreal to the secondary hemiepiphytic habit. A further reduc- tion in plant size within this lineage would have 124 Annals of the Missouri Botanical Garden accompanied the shift from the secondary hemiepi- phytic to the holoepiphytic habit (Table 3). Coro ra sericea, which occurs in the tropical rainforest of Mont Koghi, New Caledonia (Appendix 1), and is described as a tree iehler, ; Table 3), was also found growing as a secondary hemiepiphyte on the trunk of a tree fern, much as the climber Fieldia australis, which grows on tree-fern trunks in Australian rainforests (Walsh & Entwisle, so wnat h eor: in p "- tree t to seco pply (Bohl tal., 1995), and may present in seed dispersal vectors (Klein- feldt, 1978). Consequently, the hypothesis proposed by Bews (1927), indicating that in many cases the evolutionary line of development of lianas results in the production of epiphytes, seems reasonable. Essen- - m menn ee pa ^ tuong P hy phorophyte) and hesia aliyi in the early ipes of the life cycle. e en c MENS of the Dope habit to have been T in the poth habit of C. sericea an de ——: shift: this unusual secondary hemiepiphy- developed from the climbing habit, ae as seen in ieldia, Mitraria, and Asteranthera. Furthermore, Ty: £T (16090 1 + (^ = ir 3.2 E ES 1 +L genetically from Fieldia and Mitraria in estoica time, thus altering the shape of the reaction norm in the derived lineage (see Pigliucci et al., 2006). Leaves of Coronanthera sericea and C. clarkeana (Appendix 1) in the rainforests of New Caledonia showed variation from early development to adulthood. Such leaves show ontogenetic modification in terms of (1) leaf margin, from toothed or crenated to smooth, and (2) trichome density, from pubescent to glabrous or nearly so. Early developmental stages of an organism can recapitulate early stages found in its ancestors (Stebbins, 1974; Thorne, 1976), making heterochrony a potential mechanism for morphological change (Olson & Rosell, 2006). If the derived organism is neotenic, a common phenomenon in plant evolution (Takhtajan 1959, 1969, 1976; Doyle, 1977, 1978) that has been previously reported in Gesneriaceae (Jong & Burtt, 1975; Nieder & Barthlott, 2001; Mayer et al., 2003), early developmental traits of the ancestor will be shown in mature plants (Gould, 1970; McKinney & McNa- mara, 1991). Hemiepiphytic species in Coronanthereae exhibit toothed or crenated leaf margins and rather pubescent leaves as seen in early stages of previously mentioned arboreal rainforest. Coronanthera leaves. hemiepiphytes in Coronanthereae is heterochronic, and leaf margin and trichome density of secondary hemiepiphytes are neotenic (see Gould, 2002). Epiphytes are more specialized than terrestrial plants with regard to physiological, morphological, and ecological traits (Oliver, 1930; Pittendrigh, 1948; Strong & Ray, 1975; Winter et al., 1983; Nobel & Hartsock, 1990; Lambers et al., 1998; Helbsing et al., 2000), We the increase in Iunii has been considered a common evolutionary trend (Takhtajan, 1991). It is suggested that plants present in micro- itats in the forest canopy receive more and a different quality of sunlight than plants present on the forest ground (Parker, 1995), are subjected to wider taxa are found in the warm, humid, and shaded tropical forests, where a significant number of Gesneriaceae have abandoned the terrestrial habit in search of more light, with a few becoming lianas and the rest evolving into holoepiphytes. OTHER ORIGINS OF THE EPIPHYTIC HABIT WITHIN THE GESNERIACEAE Within the Gesneriaceae there are 598 epiphytic species within 28 genera (Gentry & Dodson, 1987). Epiphytic Gesneriaceae are present in circumglobal tropical — P wing qn Paleotropics, and Aus- tralasia) an long to two different subfamilies i i The distribution of the epiphytic in different phylogenies based on DNA sequences in the Gesnerioideae subfamily has been considered by Smith and n (1994), Smith and Carroll (1997), Smith (2 t al. ( i ) studies is that the epiphytic habit has evolved independently at least four times within the subfamily Gesnerioideae in (1) the Episcieae (Smith & Carroll, 1997; Smith, 2000b); (2) the genus Columnea L., with 160 species that include lianas and epiphytes (Smith & Sytsma, 1994); (3) the Sinningieae (Perret et al., 2003); and (4) the Coronanthereae (present results). Whenever holoepiphytes are present within these analyses in Gesnerioideae, their closest relatives are either terrestrial and/or secondary hemiepiphytic it. Therefore, we suggest that holoepiphytes evolved through the increased use of other plants for structural and mechanical support from terrestrial or = tic habit in Gesnerioideae would involve a potentially terrestrial ancestral condition, considering the terres- trial habit in the closest ancestral relatives to Gesneriaceae, within the Calceolariaceae (Soltis et al., 2005). The derived form would be a climbing herb or shrub, associated with the canopy habitat. For the Volume 97, Number 1 2010 Salinas et al. 125 Evolution of Epiphytes in Coronanthereae climbing habit, specialized physiological, morpholo- gical, and ecological traits associated with the holoepiphytic habit derive. Similar steps leading to the holoepiphytic habit postulated for Sarmienta within the Coronanthereae may have evolved in parallel within the tribes previously mentioned in Gesnerioideae. Future well-supported phylogenies within Gesneriaceae and Coronanthereae and its relative position within the Cesnerioideae will provide a test of these hypotheses. Follow-up articles will explore ecological differ- ences in vertical distribution patterns among Chilean Coronanthereae species, their dynamics and require- ments for germination and seedling survival, and comparative anatomy of their leaves and stems in relation to specialization to the epiphytic habit. Literature Cited Allan, H. H. 1961. Flora of New Zealand. R. E. Owen, Government € Wellington, New Zealand. Armesto, J. J., P. León & M. Arroyo. 1996. Los bosques templados dd sur pa y Argentina: Una isla biogeográfica. n J. J. Armesto, C. Villagrán & M. Arroyo n Ela cel E Ee Nativos de Chile. Editorial Universitaria, S Arroyo, M. P EE Cavia ares, A. Pu En M. Riveros & A. M.F . Relaciones fitogeográficas y patrones Armesto, C. Villagrán & M. de (editors), Ecología de l ues Nativos de Chile. 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Sin. 44: 903—907. ete i m MG ig MM d cte ecd te RS A ODA Volume 97, Number 1 Salinas et al. 127 2010 Evolution of Epiphytes in Coronanthereae Weber, A. 2004. Gesneriaceae. Pp. 63—158 ¿n K. Kubitzki — Wilson, C. A. & C. L. Calvin. 2006. An ori n of aerial i pri Families and Genera of Vascular Plants, branch s eri the eae family, Danaila. VII. Flowering Plants—Dicotyledons. Lamiales Amer. J. Bot. 93: 787—796. Pup Acanthaceae Including Avicenniaceae). Springer, Winter, K., B. J. Wallace, G. C. Stocker & 2 € Berlin 1 Crasenlace an acid Wiehler, H E . A synopsis of the neotropical Gesner- cada epiphytes and some related E dose iaceae. o 6: 1-219. 68: 224—230. APPENDIX 1. Voucher specimens for the two study ld-erowth stands of North Patagonian rainforest located in the owlands of northern Chiloé Island, an (1) Fide Cisnes s 41 1°50'S, a Coulín, and @ —_ Darwin Biological pe (SD, 41°52’S, 73°40’ W), El Quilar. Voucher specimens are g tal t t rainforest of Wenderholm (WE, 36°32’S, 174°42’E), dines: Aucklind; N head of Bunyip Valley Road (BU, 37^54'S, 14541 'E), Gembrook, Eastern MEM Victoria, Australia; and two tropical rainforests in the South Province, New ewe (1) E Koghi (KO, 22^11'S, 166730' E), main trail to Pic Malaoui, 20 km gny (DO, 21737'S, 165°52’E), Dogny. Taxa with epiphytic habit are cq | 4 t th. northeast from Noumea Idfaced. Collector number Species Site (herbarium) Asteranthera ovata (Cav.) Hanst. FC Salinas 823 (CONC) A. ovat SD Salinas 816 (CONC) itn coccinea Cav. FC Salinas 824 ONC) M. coccinea SD Salinas 815 (CONC) Sarmienta repens Ruiz & Pav. FC Salinas 822 (CONC) S. repens SD Salinas 814 (CON Coronanthera sericea C. B. Clarke KO Salinas 776 (AK, CONC, NOU) C. clarkeana Schltr DO Salinas 782 (AK, CONC, NOU) Rhabdothamnus solandri A. Cunn WE Salinas 759 (AK, CONC) BU Salinas 756 (CONC, MEL) Fieldia australis A. Cunn. CHROMOSOME STUDIES IN AMERICAN PANICEAE (POACEAE, PANICOIDEAE)! Silvana Sede,’ Alejandro Escobar,’ Osvaldo Morrone,” and Fernando O. Zuloaga? ABSTRACT Chromosome b d meiotic beh f 60 individuals behavior UL ALLA Y previously uncounted species: Axo species of Echinochloa P. Beauv., Eriochloa Morrone, Paspalum L., and Setaria Key words: America, chromosome nu Kunth, Hymenachne por dom L., Parodio, F. P: ge 37 are confirmations of previous reports. Paniceae, Panicoideae, Poaceae. of American Paniceae, Poaceae, are provided, feng six andinus G. A. Black (2n = 20), A. va (Poepp.) G. A. Black (2n AN Dichanthelium hebotes (Trin.) Zuloaga Qn = 18), Paspalum geminiflorum Steud. (2n — 20), and Setaria tenacissima Schrad. ex Schult. D 36). Of th a. 20), P. heterotrichon Trin. (2n e remaining 54 counts, 17 awaqa to new ploidy levels in iophyllochloa Zuloaga & Chromosome numbers have proved to be of great value in understanding the evolution of vascular plants hes 1975), particularly with regard to polyploid taxa (Davidse et al, 1986). Alth ough n is a common feature in the Poaceae, karyological studies are still lacking in many tropical and subtropical grasses (Honfi et al., 1991), thus limiting our ability to understand the patterns of chromosome change across the family. This paper continues a series focusing on chromosome numbers of Panicoideae (Morrone et al., 1995a, 2006; Hunziker et al., 1998). The purpose of this work is to increase the cytological knowledge of species of Panicoideae collected in different regions of South America. Chromosome numbers were compared with those in previous reports in the Poaceae, included in the following indexes: Ornduff e s 1969), Bolkhovskikh et al. (1969), re (1970, 1971, 1972, 1973, 1974, 1977), baa. (1981, 1984, 1985, 1988), and Goldblatt and Johnson (1990, 1991, 1994, 1996, 1998, 2000, 2006). MarERIALs AND. METHODS One population (with only one individual per population) was analyzed for each species studied, except in Eriochloa punctata (L.) Desv. ex Ham., Paspalum denticulatum Trin., P. pilosum Lam., P. plicatulum Michx., and P. robustum (Hitche. & Chase) S. Denham, for which four, five, two, two, and two populations were sampled, respectively. All chromosome counts were made from slide preparations of microsporocytes and root tip cells. Inflorescences and root tips were fixed with Carnoy's solution (6 parts ethanol:3 chloroform:1 acetic acid) in the field; individual anthers and root tips were squashed in 2% iron propionic hematoxylin (Sáez, 1960; Núñez, 1968), with 2% acetic carmine. Five to 10 pollen mother cells and mitotic metaphases per sample were examined using a standard 18 Zeiss microscope (Zeiss, Jena, Germany) equipped with a photographic camera at SI. A complete list of the species studied including chromosome numbers, meiotic configurations, geo- graphic origin, and voucher specimens is given in Table 1. Voucher specimens and dried herbarium sheets were deposited at the Instituto de Botánica Darwinion (SI, with duplicates at CTES, LPB, MO, and VEN). RESULTS AND DISCUSSION Counts obtained in our study (Table 1) are discussed below alphabetically by genus, except for Paspalum L. species, which are discussed as part of Chase's informal groups Morrone, 2005). Photomicrographs species from five genera (Axonopus P. Beauv., rioc representative in Figure 1. AA A e pea ep cece gs ' We thank the Consejo Nacional de Investi igaciones Científicas y Técnicas d for research gran Promoc Agencia Nacional de Geographic Society for research grant Author for oción Científica y Técnica (ANPCyT) for grants 1 7792-05. t PI 3374, 32664, and 1286; karg "h. iod ? [nstituto de Botánica Darwinion, ——— — Casilla de Correo 22 San Isidro B1642HYD, Buenos Aires, Argentina. corres; doi: 10.3417/2007118 ANN. Missouri Bor. Garp. 97: 128-138. PUBLISHED on 31 MARCH 2010. Volume 97, Number 1 2010 Sede et al. 129 Chromosome Studies in American Paniceae Table 1. Chromosome numbers and chromosome associations in species of American Paniceae. Taxa Axonopus andinus G. A. Black* A. chrysoblepharis (Lag.) Chase A. iridifolius (Poepp.) G. A. Black* A. scoparius (Flüggé) Kuhlm. A. siccus (Nees) Kuhlm. Mame hebotes (Trin.) Zuloag, D. db (Scribn.) Gould Digitaria ciliaris (Retz.) Koeler D. filiformis (L.) Koeler var. laeviglumis (Fernald) Wipff D. sacchariflora (Nees) Henrard Echinochloa Hen i dn Hitche. var. polystachy Eriochloa distachya Kunth E. punctata (L.) Desv. ex Ham.* E. punctata' E. punctata E. punctata Hymenachne donacifolia (Raddi) Chase? Ichnanthus procurrens (Nees ex in e Configurations observed in aki diakinesis of metaphase I and mitotic metaphase Origin and voucher 10 II BOLIVIA. La Paz: Nor Yungas, camino de Yolosa a La Paz, vía carr. antigua Los Yungas Coroico-La Paz, Morrone & Belgrano 4904 (CTES, LPB, MO, S 10 II BOLIVIA. Santa Cruz: Nuflo de Chávez, Rta. Nac. 10, ca. Km 97, camino de San Javier a Concepción, Morrone & Belgrano 4956 (CTES, LPB, MO, 10 II BOLIVIA. La Paz: Nor Yungas, camino de Unduavi a Coroico 10 II BOLIVIA. La Paz: Nor Yungas, camino de Unduavi a T por la carr. nueva Los Yungas, Morrone & Belgrano (CTES, LPB, MO, SI) 10 I BOLIVIA. La Paz: Nor Yungas, camino de Unduavi a Coroico r la carr. nueva Los Yungas, ca. Km 67, Morrone & Belgrano 4841 (CTES, LPB, M , SI) 9 II BOLIVIA. La Paz: Nor Yungas, ca. 10 km de Challá camino a Caranavi, Morrone & Belgrano 4880 (CTES, LPB, MO, SI) 18 II VENEZUELA. Aragua: Colonia Tovar, cerca del Monum. Nat. I camino a Colonia Tovar, Morrone et al. 4674 ‘ab. SL V 18 I BOLIVIA. I Cruz: Nuflo de Chávez, camino de Concepción a San Javier, Rta. = E 13, Morrone & Belgrano 5079 (CTES, LPB, M 27 Il VENEZUELA. Aragua: cits via ada Tovar por La Victoria, sector Loma Briza, Morrone et al. 4666 (MO, SI, 18 II BOLIVIA. Santa Cruz: Florida, camino de la Angostura a Samaipata, rta. 60, Morrone & Belgrano 5091 (CTES, LPB, 27 Il ARGENTINA. Entre Rios: Victoria, Viaducto Rosario— Victoria, 20 km de Rosario, Morrone & Giussani 5176 (MO, S oll BOLIVIA. Santa Cruz: Nuflo de Chavez, 9 km de Concepción amino a S.A. Lomerio, Hda. San Lorenzo, Morrone & Belgrano 4987 (CTES, LPB, MO, S 9 II ARGENTINA. Entre Ríos: Islas del Ibicuy, alrededores de Villa Paranacito, Morrone et al. 5199 (SU) 36 II ARGENTINA. Corrientes: Empedrado, Rta. Nac. 12, Km 958, Ayo. San Lorenzo, Morrone et al. 5328 (MO, SI) 18 Il — La Paz: Nor Yungas, 3 km de Coroico camino a aranavi, camino a Río Coroico, Morrone & Belgrano 4866 E CTES, LPB, MO, SI) 18 ll BOLIVIA. Santa Cruz: Ñuflo de Chávez, camino de Concepción a San Javier, Rta. 10, Km 73, Morrone & Belgrano 5081 (CTES, S, LPB, MO, SI) ca. 10 II BOLIVIA. La Paz: Nor Yungas, alrededores de ok entre Chálla y Coroico, Morrone & Belgrano 4884 (CTE LPB, MO, ca. 10 II —À Santa Cruz: Nuflo de Chavez, 6-8 km de mino a S.A. Lomerio, Morrone & Belgrano Con 4971 ces, LPB, MO, SI) 130 Annals of the Missouri Botanical Garden Table 1. Continued. Configurations observed in diakinesis of metaphase I Taxa and mitotic metaphase Origin and voucher Mesosetum loliiforme (Hochst. ex eud.) Chase Panicum elephantipes Nees ex rin. P. trichanthum Neest Parodiophyllochloa cordovensis (E. Four.) Zuloaga & Morrone' Paspalum alcalinum Mez P. arundinaceum Poir.’ P. arundinellum Mez P. atratum Swallen* P. campylostachyum (Hack.) S. Denham P. commune Lillo P. denticulatum Trin. P. denticulatum P. denticulatum P. denticulatum P. denticulatum' P. geminiflorum Steud.* P. heterotrichon Trin.* P. inconstans Chase P. intermedium Munro ex Morong P. juergensii Hack. mri tenia ge 16 II 15 II 36 II 35 1 +2 1 9 11 20 II ] VII - 1 IV - A HI ca. 25 II 20 Il 20 Il 20 II 20 II 20 II ca. 10 I 10 II 30 II 20 II 20 II VENEZUELA. Bolívar: Gran Sabana, Parque Nac. Canaima, 6-10 km de Kama-Meru camino a Santa Elena, Morrone et al. 4766 (MO, SI, VEN ARGENTINA. Entre Ríos: Islas del Ibicuy, Brazo Largo, R' . 12 y Río Paraná Guazú, Morrone et al. 5191 (MO, ^ BOLIVIA. La Paz: Nor Yungas, 3 km de Coroico camino a Caranavi, Morrone & Belgrano 4863 (CTES, LPB, MO, SI) BOLIVIA. La Paz: Nor Yungas, ca. 10 km de Challá camino a A. Bella Vista camino a Empedrado, Mawes et al. 5322 (MO, VENEZUELA. ados Mata Linda, carr. Chaguara: e 81 km d Morrone et al. 4749 (MO, x VEN) ARGENTINA. Misiones: San Ignacio, Parque Pro Teyucuaré, Peñón del Teyucuaré, Zuloaga et al. pa (MO, BOLIVIA. Santa Cruz: Ñuflo de Chávez, camino de Concepción a San Javier, Rta. 10, Km 73, Morrone & Belgrano 5082 (CTES, LPB, MO, SI) VENEZUELA. Táchira: 31 km de San Cristóbal camino a Las Delicias, alrededores del Control de Guardia Pabellón, a 2 km de Pabellón, Morrone et al. 4702 (MO, SI, VEN) — Salta: La Caldera, Rta. Nac. 9, camino al Abra e Santa Laura, Zuloaga et al. 8480 (MO, SI PUR Jujuy: Dr. M. Belgrano, Sierra de Zapla, Zuloaga et al. 8607 (MO, S ARGENTINA. Jujuy: El Carmen, Abra de Santa Laura a i ) : án, entrada a Ingenio El Tabacal, Zuloaga et al. 8562 (MO, SI) ARGENTINA. Entre Ríos: Victoria, Viaducto Rosario- Victoria, 20 km de Rosario, Morrone & Giussani 5174 (MO, ARGENTINA. Entre Ríos: Islas del Ibicuy, cruce de las rutas Nac. 12 y 14, Morrone et al. 5212 (MO, SI) BOLIVIA. uus Cruz: Nuflo de Chávez, Rta. Nac. 10, ca. Km 97, camino de San — a eu. Morrone & Belgrano 4964 (CTES, LPB, MO, S VENEZUELA. Miranda: Area i. Parque Nac. El Avila, camino a Sabas Nieves, Morrone et al. 4739 (MO, SI, VEN) BOLIVIA. La Paz: Murillo, Valle del Zongo, camino de La Paz a Zongo, ca. 7 km de Zongo, Morrone & Belgrano 4805 (CTES, LPB, MO, SI) ARGENTINA. Corrientes: Em Rta. Nac. 12, Km 958, Ayo. San Lorenzo, Morrone et al. 5327 (MO, SI) ARGENTINA. San Roque, Rta. Nac. 12, Km 870, 31 km de S Roque camino a Goya, Morrone et al. 5336 (MO, S BOLIVIA. La Paz: Nor Yungas, camino de Unduavi a Coroico r la carr. nueva Las Yungas, Morrone & Belgrano 4831 (CTES, LPB, MO, SI) Volume 97, Number 1 2010 Sede et a l. 131 Chromosome Studies in American Paniceae Table 1. Continued. Configurations observed in diakinesis of metaphase I Taxa and mitotic metaphase Origin and voucher P. macrophyllum Kunth? P. maculosum Trin. P. malmeanum Ekman P. microstachyum J. Presl P. multicaule Poir. P. penicillatum Hook. f. P. pilosum Lam.t P. pilosum! P. plenum Chase P. plicatulum Michx. P. plicatulum P. regnellii Mez P. remotum J. Rémy! P. repens P. J. Bergius P oM (Hitche. & Chase) S. ham Denham P. robustum? Pennisetum latifolium Spreng. P. montanum (Griseb.) Hack. P. nervosum (Nees) Trin. Setaria tenacissima Schrad. ex Schult.* S. vulpiseta (Lam.) Roem. & Schult.* 20 II VENEZUELA. Táchira: ca. 2 km del Sector La Honda camino a Las Delicias, a 18 km del control de Guardia Pabellón, € et al. m mo is TM 10 II BOL OLX 6 camino a S.A. Lomerio, Hda. San Lom Morrone & Maece s erm HM x. € 10 II 2, Okm de C as camino a S.A. Lomerio, Hda. San pon Morrone & Belgrano 4991b (CTES, LPB, MO, S. 20 II VENEZUELA. Cojedes: camino de Tinaquillo a Tinaco, carr. Valencia-San Carlos, Km 59, Morrone et al. 4683 (MO, SI, VEN) 2n — 20 VENEZUELA. Portuguesa: carr. Acarigua-Guanare, a 50 km de Acarigua, Morrone et al. 4686 (MO, SI, VEN) 20 II BOLIVIA. La Paz: Murillo, Valle del Zongo, camino de La Paz a Zongo, Morrone & Belgrano 4808 (CTES, LPB, MO, SI) 10 II VENEZUELA. Mérida: Fac. de Cien. Forestales, Morrone et al. 4721 (MO, SI, VEN) 10 II VENEZUELA. Bolívar: Gran Sabana, Parque Nac. Canaima, 16 km de Quebrada Pacheco y a 12 km de Yuruani camino a Santa Elena, Morrone et al. 4778 (MO, SI, VEN) 11 II 4 18I ARGENTINA. Corrientes: Empedrado, Rta. Nac. 12, Km 958, Ayo. San Lore a sn Cil 5330 (MO, SI) 20 II BOLIVIA. Santa Cruz: Nuflo de Chávez, 9 km de Concepción camino a S.A. Lomerio, Hda. x Lorenzo, Morrone Belgrano 4979 (CTES, LPB, M 20 II ARGENTINA. Jujuy: La Caldera, rm Nac. 9, camino a Abra de Santa Laura, Zuloaga et al. 8477 (MO, ca. 10 II ARGENTINA. Entre Ríos: Concordia, camino de Colonia Ayui a la Rta. Nac. 14, 3 km de Co. Ayui, Morrone et al. 5303 (MO, SI) ca. 20 II ARGENTINA. Jujuy: Ledesma, Abra de Cañas, camino a Valle Grande, Zuloaga et al. 8522 (MO, SI) 10 II ARGENTINA. Entre Rios: Islas del Ibicuy, Brazo Largo, Rta. Nac. 12 y Rio Parana pee Morrone et al. 5193 (MO, SD 20 H VENEZUELA. Miranda: Are. tro, Parque Nac. El : Ávila, camino a Sabas Nieves, E et al. 4740 (MO, SI, VEN) 40 II VENEZUELA. Portuguesa: Guanare, predio de la Univer. Nac. Exp. de los Llanos Centrales E. Zamora, Morrone et al. 4694 (MO, SI, VEN) 18 I URUGUAY. Tacuarembó: Rta. 26, Km 208, Cañada del Sauce, Morrone et al. 5278 o SD 2 IV + 12 II BOLIVIA. La Paz: Larecaja, 2 m de Sorata vía el camino por “Altai Oasis,” Morrone & a. 4931 (CTES, LPB, MO, SI) ca. 18 II ARGENTINA. Entre Ríos: La Paz. Rta. Nac. 12 y Río Guayquiraró, Km 593, Morrone et al. 5355 (MO, SI) 18 I BOLIVIA. La Paz: Nor Yungas, desvío a Yanicucho, a 1 km de carr. nueva Los Yungas La Paz-Coroico, Morrone & Belgrano 4860 (CTES, LPB, MO, S 9 BOLIVIA. Santa Cruz: Ñuflo de Chávez, camino de Concepción a San Isidro, ca. 3 km antes de San Isidro, orrone & Belgrano 5023 (CTES, LPB, MO. SD ivalent, IV — quadrivalent, and VIII — octovalent. Chromosome associations at meiosis: E = ogically st umbers that differ from previously published reports. univalent, Il — b 132 Annals Missouri Botanical Garden igure tomi l iotic ch f American Pani riochloa punctata (L.) Desv. ex Ham., 8 II, prometa aan tenacissima Schrad. ex Schult., 18 ut e a inesis. ers Axonopus iridifolius (Poepp.) G. š Black, 10 II, ue —D. Paspalum geminiflorum Steud., 10 Il, prometaphase I 10 diakinesis. . —E. Paspalum atratum iecur um macrophyllum Kunth, 20 II, diakinesis. —G. Paspalum penicillat: k.£,20 : —H. Porodisphsllocklon is (E. nes Zuloaga & Morrone, 9 II, metaphase Í —1. Paspalum Nabi sn Trin., 0 IL, prometaphase I. —J. ar num Eisen. 10 II, early metaphase I. —K. Setaria vulpiseta (Lam.) Roem. & Sd A me m ME Axonopus is a large genus of more than 100 species Black (2n — 20), a species of subseries Scoparii G (Black, 1963) confined to the won, - only Black, and A. iridifolius (Poepp.) G. A. Black A ap pecies in Africa; y of il i egenus 20) (Fig. 1C), of subseries Ancipites G. A. Black are significant components of wii pastures. Key (sensu Black, 1963), represent the first cytological diagnostic morphologies for the genus are spikelets report for both taxa. Counts of 2n = 20 for Axonopus a ee siio sid esa ibi nile chrysoblepharis (Lag.) Chase (section Cabrera (Lag.) rachis. Chromosome numbers of A. andinus G. A. Chase), A. scoparius (Flüggé) Kuhlm., and A. siccus CET Sie iis BE eg cx: Tue oak s SAI M TI ART Volume 97, Number 1 2010 Sede et al ; 133 Chromosome Studies in American Paniceae (Nees) Kuhlm. (subseries Barbigeri G. A. Black) are in agreement with previous reports by Shibata (1962), Pohl and Davidse (1971), Davidse and Pohl (1974), Hickenbick (1975), Norrmann et al. (1994), and Morrone et al. (1995a). Dichanthelium (Hitche. & Chase) Gould is an American genus with approximately 60 species distributed from Canada and the United States to Argentina and Chile in South America (Zuloaga et al., ). The genus includes many species with foliar and floral dimorphism, which are usually present in humid places, such as forest edges or margins of streams and rivers (Gould & Clark, 1978; Crins, 1991; Zuloaga et al., 1993). A high percentage of diploids, ca. 80%, have been reported for North and Central American species of Dichanthelium (Dubcovsky & Zuloaga, 1992). The chromosome count of D. hebotes (Trin.) Zuloaga (2n = 18) is reported here for the first time, while that of D. viscidellum (Scribn.) Gould (2n = 36) is in accordance with a previous report (under Panicum viscidellum Scribn.; Davidse & Pohl, 1974). Both numbers are in agreement with the basic chromosome number proposed for the genus (x — 9) (Brown, 1948; Gould, 1966, 1968; Gould & Soder- strom, 196 The genus y Digitaria Haller includes from 200 to 330 species distributed worldwide in tropical, sub- tropical, and warm temperate regions (Nicora & Rúgolo de Agrasar, 1987; Watson & Dallwitz, 1992). Key diagnostic morphologies for the genus are spikelets with the lower glume small, upper anthe- cium cartilaginous, with the margins of the lemma flat, not inrolled over the palea. The base chromosome number of the genus is x — 9 (Watson & Dallwitz, 1992), and polyploidy is a common feature (Bolkhov- skikh et al., 1969; Gould & Soderstrom, 1974; Mehra & Sharma, 1975). Chromosome counts of D. ciliaris (Retz.) Koeler (2n — 36), D. filiformis (L.) Koeler var. laeviglumis (Fernald) Wipff (2n = sacchariflora (Nees) Henrard (2n = 36 of previous reports (Reeder, 1971; Morrone et al., 1995a; Hunziker et al., 1998 Echinochloa P. Beauv., a pantropical genus of mw 40 species (Clayton & — I as a base chromosome number ES tetraploid, bid: and akaun n (Watson & Dallwitz, 1992). A new hexaploid count, with 2n = 54, is reported here for E. polystachya (Kunth) Hitche. var, polystachya; previous reports for this species are an approximate dodecaploid count of 2n = 108 (Pohl & Davidse, 1971) and subsequently its confirmation as n = 54 (Davidse & Pohl, 1974). The genus is distinguished by its racemose inflor- escences, with spikelets unilaterally arranged; spikelets with lower glume short, upper glume me and lower lemma acute to awned; and upper anthecium indurate, smooth and shiny, with the apex of the palea reflexed. Eriochloa comprises about 30 species of moist grasslands and open woodlands in tropical, subtropi- cal, and warm temperate regions of both hemispheres (Clayton & Renvoize, 1986). The genus is distin- guished by the presence of a basal swelling, which is the fusion of the vesitigial lower glume with the rachilla internode. The basic chromosome number of genus is x = 9, and tetraploid, hexaploid, and octoploid cytotypes have been reported (Watson & Dallwitz, 1992). A chromosome count of 2n = 18 was found in E. distachya Kunth, in agreement with previous diploid reports (Pohl & Davidse, 1971; . 1994) Also, three counts are reported here for E. punctata: 2n = 36 (Fig. 1A), which agree with previous tetraploid reports (Núñez, 1952; Gould, 1966; Gould & Sodestrom, 1967; Quarin, 1977; Hunziker et al., 1998); the other two counts, 2n = 18 and 2n = 72, represent new diploid and octoploid levels for the species. Hymenachne P. Beauv. is a small genus with approximately 10 worldwide distributed species in poze wetlands (Watson & Dallwitz, 1992; Aliscioni , 2003). The genus is distinguished by having cam plants, with inflorescences with racemose branches, spikelets unilaterally disposed, and spike- lets with upper anthecium membranous, the margins of the lemma flat, leaving the apex of the palea exposed. The basic chromosome number for the genus is presumed to be x — 10, although there are previous counts of n = 18 (Sindhe et al., 1975; Sharma et al., 1978) and 2n = 24 (Gould & Soderstrom, 1970). Hymenachne donacifolia (Raddi) Chase is reported herein as a diploid cytotype T — ca. 20); previous counts for the species are 2n = 24 and 2n = 40 (Gould & Soderstrom, 1970; Pohl & Davidse, 1971; Honfi et al., 1991). The genus Ichnanthus P. Beauv. comprises about 33 species mainly distributed in tropical regions of the New World. The genus is distinguished by having a lower glume that is 1/2 to 1X the length of the spikelet and the presence of conspicuous wings, base of the upper lemma. Its basic - or scars, at the e number is x = 10, and aneuploidy, as chromosom well as tetraploid and hexaploid cytotypes, were reported for some species (Gould & — 1967; Pohl & Davidse, 1971; Honfi et al., Hunziker et al., 1998; Watson & Dallwitz, en, Ichnanthus procurrens (Nees ex Trin.) Swallen of section Foveolatus Pilg. (Stieber, 1987) is a diploid cytotype with 2n = 20; this count is in agreement with that of a previous report (Gould & Soderstrom, 1967). Annals of the Missouri Botanical Garden Mesosetum Steud. is a genus with nearly 35 American species, mostly distributed in South America, with a few representatives in the West Indies and Central America (Filgueiras, 1989). The genus is distinguished by the aia being a solitary raceme, with spikelets solitary, the upper anthecium indurate, open at the apex, and the caryopsis with a linear hilum. M eir counts have been reported for the genus (Goul ; Gould & Soderstrom, 1967; Pohl & Davidse, s Davidse & Pohl, 1972), they suggest that the basic chromo- some number of Mesosetum is x — 8. Our chromosome count for M. loliiforme (Hochst. ex Steud.) Chase, 2n = 32, agrees with that of a previous report (Gould & Soderstrom, 1967). Panicum L., s.l., has nearly 450 species worldwide, distributed mainly in tropical and subtropical regions (Webster, 1988). Basic chromosome numbers pro- posed for the genus are x = 7, 9, and 10 (Watson & Dallwitz, 1992), although Panicum, in the strict sense restricted to subgenus Panicum, has a basic chromo- some number of x = 9. The count 2n = 30 for P. elephantipes Nees ex Trin. from subgenus Panicum, section Dichotomiflora (Hitchc. & Chase) Honda (Zuloaga, 1987), is in agreement with previous reports of 2n = 30 (Covas, 1949; Núñez, 1952; Urbani, 1990). Panicum tricha: ees of section Parvifolia Hitchc. €: Chase ex Pilg. (Zuloaga, 1987) showed 36 bivalents (II) and also 35 bivalents (II) plus two univalents (I). This is the first report of an octoploid cytotype for the species. Previous reported counts correspond to tetraploid cytotypes (Pohl & Davidse, 1971; Davidse & Pohl, 1972; Honfi et al., 1991; Norrmann et al., 1994; Morrone et al., 2006). Section PS is — by including annual r peren es, aquatic or from humid areas, ae lets M dn with the lower glume reduced, 1/5 to 1/3 the length of the spikelet. On the other hand, section Parvifolia includes species with open, lax inflorescences, spikelets obovoid to lanceolate, upper glume and lower lemma 5-nerved, and upper anthecium indurate, with bottlelike microhairs and simple papillae all over its surface. The recently established genus Parodiophyllochloa (Morrone et al., 2008) includes six American species of tropical and subtropical regions, usually present in the interior of forests or forest edges. This genus departs from Panicum s. str. because its species grow at the edge of forests and are characterized by membranous ligules, the presence of cleistogamous inflorescences, and upper anthecium mucronate, with simple papillae all over its surface. Parodiophyllo- chloa cordovensis (E. Fourn.) Zuloaga & Morrone is a diploid cytotype with 2n = 18 (Fig. 1H). Previous counts for the species, under Panicum cordovense E Fourn., are 2n = 54 (Pohl & Davidse, 1971) and n = 27 (Davidse & Pohl, 1978). The genus Paspalum — f 310 primarily American species chromosome number of x — 10 eie. pe The genus is distinguished by its racemose inflore with spikelets arranged unilaterally on the racemes, glume absent, occasionally reduced. rescences, with lower Polyploidy, mainly D is frequent within the genus 992; Pagliarini et al., 2001). Within Paspalum, bua tsa (Pers.) Rchb. includes 25 species distributed fro south uth America in Argentina and Uruguay (Denham et al., 2002). This subgenus has been characterized by having inflorescences with one to several racemes, the rachis of the ra winged and hyaline to membranous, and the spikelet is dol pilose, with the upper lemma not enclosing the tip of the upper palea. A diploid cytotype with 2n = 20 (Fig. 11) was observed in P. heterotrichon Trin., representing the first count for the species. Paspalum malmeanum Ekman is a diploid with 2n = 20 (Fig. 1J), which confirms a previous report for this species (Killeen, Mexico to cemes is _ ). Subgenus anions " rin.) S. Denham of aspalum is l by the presence of terminal and: axillary inflorescences in the upper foliar sheaths, solitary racemes, and spikelets with lower glume present; it includes 39 American species (Denham, 2005). Within this subgenus, the count 2n — 40 for P. campylostachyum (Hack.) S. Denham is in agreement with a previous report (under Thrasya campylostachya (Hack.) Chase [Davidse & Pohl, 1972]). The chromo- some number (2n — 20) found in two individuals of P. pilosum is the first report of a diploid cytotype for the species; tetraploid cytotypes were cited by Pohl and Dside (1971) and Davidse and Pohl (1974). A count of 2n = 60 for P. inconstans Chase agrees with the report from Morrone et al. (2006). Two individuals of P. robustum were analyzed; one of them has 2n — while the remaining has 2n — 80, both representing rst. reports of tetraploid and octoploid cytotypes, o It should be mentioned that a previous count, er T. robusta Hitche. & Chase (Pohl & Devidbe, | 1971), corresponds to a hexaploid cytotype. Within subgenus P. um, the group Livida (Chase, ined.) includes caespitose and decumbent perennials with compressed culms, flat blades, and paired, smooth or scabrous spikelets (Chase, 1929; Zuloaga & Morrone, 2005). Three species from Chase’s Livida group were herein investigated, P. alcalinum Mez, P. d and P. remotum J. Rémy. The o 2n = = Mla. sica confirms a m ) and dies ioa that of Parodi (1946), who reported 2n — Volume 97, Number 1 2010 Sede et al. Chromosome Studies in American Paniceae 76. Paspalum denticulatum is a widespread American species with highly variable vegetative and floral characters (cf. Zuloaga & Morrone, 2005). Five different individuals of P. denticulatum were ana- lyzed: four accessions showed 2n = 40, in agreement with the tetraploid vies condi previously reported (Quarín et al., & Burson, 1991; Hunziker et al., 1998), di ni fifth represents a diploid cytotype (2n = 20), which is a novel ploidy level for the taxon. One uc a P. sabens was investigated here and sho = 40), which differed from the report liom Hu cler et al. (1998), who found an octoploid cytotype for this species. The informal group Quadrifaria Barreto of Paspa- lum (Zuloag Morrone, 2005) includes tall caespitose species with a stramineous upper anthe- cium. The examined collection of P. arundinaceum Poir., a diploid with 2n — 20, is reported here for the first time, pes: from the previous reports for this species: n = 30 (Davidse & Pohl, 1974), 2n — 40 (under 2 secans Hitche. & Chase; Snyder, 1953), and 2n — 80 (under P. secans; Gould & Soderstrom, 1967). Meiotic irregularities, such as the presence of four to eight univalents, were observed in several cells; a ege irregular pairing with different umbers of tetravalents and univalents was also ported lens & Pohl, 1974) in this species. An accession of P. arundinellum Mez from Argentina has 2n — ca. 50, which is in agreement with a previous report for this species (Honfi et al., 1991). The count of 2n — 40 for P. intermedium Munro ex Morong & Britton corresponds with the reports published by orrmann et al. (1989, 1994). Paspalum plenum Chase is a tetraploid species lio 40) and shows a meiotic configuration composed of 11 II + 18 I. The chromosome number is in agreement with previous reports (Davidse & Pohl, 1972; Norrmann et al., 1994 ). Paspalum regnellii Mez and P. commune Lillo are members of Chase's informal group Virgata (Chase, ined.; Zuloaga & Morrone, 2005, a detail of Chase groups can be found in the latter paper), which is characterized by including tall species with truncate inflorescences and a dark upper anthecium. One examined accession of P. regnellii is a diploid with 2n = ca. 20 and differs from tetraploid cytotypes of 2n = 40 reported by Norrmann (1981) and Honfi et al. (1991). Paspalum commune is a tetraploid with 2n = 40, in agreement with previous counts recorded by Saura (1941, 1948) and Hunziker et al. (1 998). Three species were examined in Chase’s species group Plicatula (Chase, ined.) of subgenus Paspalum (Chase, 1929; Zuloaga & Morrone, 2005): P. atratum Swallen, P. geminiflorum Steud., and P. plicatulum. Species in this group are perennial or annual, terrestrial, in wet lands, and have inflorescences with numerous stiff racemes, spikelets plano-convex, and € anthecium dark brown. The specimen studied of atum, from Bolivia, is a diploid with 2n — 20 (Fig. 1B. which differs from previous counts pub- lished by Quarín et al. (1997), Takayama et al. (1998), and Adamowski et al. (2005), who reported 2n — 40 for this species. Paspalum geminiflorum is a diploid with 2n = ca. 20 (Fig. 1D), the first count for the es. The examined accession of P. s isa aes with 2n = 40, confirming previous counts by Moraes Fernandez et al. (1974), Davidse a Pohl (1972, 1974), Honfi et al. (1991), and Pozzobon et al. (2000). The informal group Notata (Chase, ined.), which includes 21 American species (Zuloaga et al., 2004), is characterized by inflorescences usually with two conjugate racemes and a solitary, glabrous or pilose spikelet. Paspalum ionanthum Chase is a tetraploid with 2n — 40, confirming this result with previously reported counts (Quarín & Norrmann, 1987; Pozzobo et al., 2000). Paspalum maculosum Trin. is a diploid cytotype with 2n — 20, in accordance with the report of Norrmann et al. (1994) Paspalum macrophyllum Kunth, a member of the up Macrophylla (Chase, ined), is a species characterized by its flat leaves, paired spikelets, and the stramineous upper anthecium; the taxon is found in Andean regions of Venezuela, Colombia, and Ecuador, at forest edges and in disturbed areas. The accession of P. macrophyllum, from Venezuela, is a iac with 2n — 40 (Fig. 1F), a count that differs prev reports for the species of 2n = 60 (Snyder, 1953; Davidse & Pohl, 1974). e p Parvifolia within Paspalum ( (Chase, 1929, ined.; Zul Morrone, 2005), with approximately nine American species, includes spe- cies with inflorescences with delicate racemes and minute, solitary or paired spikelets. Within this group, our count 2n = 20 for P. multicaule Poir. is in agreement with that of previous reports (Davidse & Pohl, 1972; Killeen, 1990). A Venezuelan P. micro- stachyum J. Presl accession is a tetraploid with 2n = 40, a count that differs from other published ones that found individuals with 2n = 20 (Pohl & Davidse, 1971; Davidse & Pohl, 1974). Paspalum penicillatum Hook. f., a member of group Racemosa within subgenus Paspalum (Morrone et al., 1995b), is a tetraploid with 2n. — 40 (Fig. 1G), i accordance with a previous report published bs Morrone et al. (2006) for this species. The group is distinguished by including annual plants; inflores- cences with deciduous racemes at maturity; spikelets solitary, glabrous, and plano-convex, with the upper Annals of the Missouri Botanical Garden glume and lower lemma 3-nerved; and the presence of distinctive Kranz cells. e group Dissecta of subgenus Paspalum (Chase, 1929; Morrone et al., 1996) includes perennial, aquatic or subaquatic taxa, which all have foliaceous rachises of the racemes and solitary spikelets; species of this group are distributed from the United States to Argentina. Paspalum repens P. J. Bergius has 2n = 20, a result that agrees with previous studies made by Davidse and Pohl (1974). Paspalum juergensii Hack., a species of Chase’s group Paniculata (Chase, 1929; Zuloaga & Morrone, 2005), is a diploid with 2n = 20, in agreement with previous results for this species (Moraes Fernandez et al, 1974; Burson & Quarin, 1982; Morrone et al., 2006). This group is characterized by having plants perennial; inflorescences with numerous racemes; paired spikelets, obovoid to ellipsoid, and usually ferrugineous; and upper anthecium pale and shiny. Pennisetum Rich. is a genus with about 80 species worldwide that are distributed in tropical and subtropical regions. The genus is distinguished by having spikelets on contracted axes to paniculate, the spi coord di ced- or partially united, falling together with the e Pansies latifolium Spreng. has 2n = 36, which agrees with previous results published by Parodi (1946) and Núñez (1952). Pennisetum montanum (Griseb.) Hack. is a tetraploid species with 2n = 32. The p cimen exhibits an irregular meiotic confi (2 QV * 12 II), an anomaly already cited by Bs et al. (1998). The count of 2n — ca. 36 for P. nervosum (Nees) Trin. is in accordance with Parodi (1946) and Núñez (1952). Setaria is a genus of ca. 110 species distributed in tropical and warm temperate regions. This genus is distinguished by the presence of one to many bristles, persisting on the axis, below the spikelets, and upper anthecium indurate, usually ru The basic number of the genus is x = 9, and polyploidy is a common feature. Setaria tenacissima hrad. ex Schult. is a tetraploid taxon with 2n = 36 (Fig. 1B); this is the first report for the species. Our count of S. vulpiseta (Lam.) Roem. & Schult. is 2n = 18 (Fig. 1K); this is the first diploid cytoty ported and this differs from tetraploid (Oliveira Freitas Sacchet, 1980) and hexaploid (Norrmann et al., 1994) cytotypes, respectively, from previous reports As a result of this study, new ploidy levels were found in species of Echinochloa, Erioc , Hymen- achne, Panicum, Parodiophyllochloa, Paspalum, and Setaria. Although only one individual per population was analyzed, the results found in this contribution support, as previously published by Quarín (1994) for Paspalum, the Too of heteroploidy as a common feature wit e grasses. We found only two meiotic ab with multivalent chromo- some associations; one is a count of Paspalum inaceum and another of Pennisetum montanum. Tetraploida, with bivalent meiotic pairing, are th most frequent cytotypes within the analyzed polyploid taxa. Literature Cited Adamowski, E. V., M. S. Pagliarini, A. B. M. coser A. R. E a & J. F. e Valls. 2005. Chromosome numbers and otic behavior of some Laila shite accessions. Genet. Mol. Biol. 28: € Aliscioni, S. E L. M. Giussani, F. O. Zuloaga a E = Kellogg A molecular phylogeny of P. Posen Pasce Tests of monophyly and ce po within the Panicoideae. Amer. J. Bot. 90: Black, G. rasses of the genus Axonopus e ixenomie Geamia). Advancing Frontiers Pl. Sci. 5: —186. Bolkhonskikh, Z., V. Grif, T. Matvejeva & O. Zakharyeva. . Chromosome Numbers of Flowering Plants. V. L. i Botanical Institute, Russian Academy of Sciences, St. Petersbu Brown, W. V. 1948. A cytological study in the Gramineae. Amer. J. Bot. 35: 382-3 Burson, B. L. 1975. 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"n S. Natl. I o & 0. M e. neto Sys tematics of Paulum group fa Poaceae: Teka Paniceae). Syst. Bot. Monogr. 71: Acknowledgment of Reviewers The following individuals are thanked for their collegial reviews in 2009. This peer commitment of time and effort is sincerely appreciated by the Annals. Jerry M. Baskins Ilsi Boldrin (L uh Campbell John Clark B onn Miriam Denham John Ebinger Eve Emshwiller Diane Ferguson Estrela Figueiredo as M. Socorro González Elizondo John Herr Walter Judd Kathy Kron Elton M. C. Leme Rita Li Maria Gabriela Lopez Valéry Malécot Eduardo Sahagún Godínez Bruce Sampson John Sawyer Alan Smith Robert Soreng Peter Stevens Ulf Swenson José F. M. Valls Stephen Weller Mark Wetter —MVotis gratias agamus. Volume 97, Number 1, pp. 1—140 of ANNAIS 0F THE Missouri BOTANICAL GARDEN was published on March 31, 2010 Missouri BB H www.mbgpress.org CONTENTS Olaya | on the Floral Morphology of Sassafras randaiense “I... ee Kuo-Fang Chung, Henk van der Werff & Ching-I Peng 1 Estudios en el üo Paspalum (Poaceae, Panicoideae, Paniceae): Paspalum denticulatum y Especies Afines Silvia S. Denham, Osvaldo Morrone & Fernando 0. Zuloaga ll Revision of the Caribbean Genus Ginoria (Lythraceae), Including Haitia from Hispaniola Shirley A. Graham 3⁄4 | i of Néotranidal Rubiaceae. I: Kubiadae e Michael fem 91 yanan aa ylogeny in the Streptanth dulosus C (B ; Michael x Mayer & ias Beseda 106 : Epiphytic Qin Habits d Chilean Canini and the Evolution of Epiphytes Within the Tribe Coronanthereae — M. Fernanda Salinas, Mary T. K. Arroyo : Juan J. Armesto 117 Chromosome Studies in bu: Paniceae (Poaceae, Panicoideae) ^ — Silvana Sede, — Alejandro Escobar, Osvaldo Morroi & Femando O. Zuloaga 128 : Acronis of Reviewers x 139 i Ginoria pulchra (Ekman & O. C. Schmidt) S. A. Graham, drawn by Taciana Cavalcanti. Annals of the Missouri Botanical Garden www.mbgpress.org. Latin Editor, > . Missouri Botanical Garden _ Thsan A. Al-Shehbaz ——^— a Missouri Botanical Garden — Gerrit Davidse l . Missouri Botanical Garden Garden Garden Volume 97 Annals Number 2 of the Y 2 I. BOTANICAL Missouri urs c bDelmeal GARDEN LIBRARY Garden A REVISION OF DESCHAMPSIA, Jorge Chiapella? and Fernando O. Zuloaga? AVENELLA, AND VAHLODEA (POACEAE, POEAE, AIRINAE) IN SOUTH AMERICA! ABSTRACT A revision of the species of Deschampsia P. Beauv., Avenella (Bluff € Fingerh.) Drejer, and Vahlodea Fr. (Poaceae, Poeae, Airinae) present in South America is given. Fifteen species of Deschampsia and two monospecific genera segregated from Deschampsia—Avenella and Vahlodea—are found in the Andes of Argentina and p p of 30°S, typically in humid or damp sites and wetlands. Isolated populations of the cosmopolitan D. cespitosa (L.) P. Beauv. are also found in Bolivia - highlands of southern Brazil. Keys to differentiate among the species of Deschampsia e the allied genera Avenella an Vahlodea are provided. A lectotype is designated for D. berteroana (Kunth) Tri RESUMEN Se presenta una revisión de las especies de Deschampsia P. Beauv., Avenella (Bluff & Fingerh.) Drejer y Vahlodea Fr. de Sudamérica. Se hallaron quince especies de Deschampsia y m dos paea monotipico A nines Vañindbu (segregados de Deschampsia), t PS m aisladas de laes especie cosmopolita D. cespitosa (L) P. Beauv. se encuentran en Bolivia y : las e altas del sur de B dan claves para diferenciar Deschampsia de sus pe aliados Avenella y Vahlodea as especies de A c E "M el lectotipo de D. berteroana (Kunth) Tri Key words: Airinae, Aveneae, Avenella, dación Poaceae, Poeae, Vahlodea. Deschampsia P. Beauv. consists of about 30 species — Clarke, 1980; Clayton & Renvoize, 1986; Beetle, found in cold temperate regions of both hemispheres 1987; Conert, 1987; Rzedowski & Rzedowski, 1990; (Hultén, 1941; Parodi, 1949; Hitchcock et al., 1969; Hickman, 1993). The number of species may increase Bor, 1970; Tzvelev, 1976; Cronquist et al., 1977; if several subspecies of D. cespitosa (L.) P. Beauv. is part of the doctoral thesis of J.C. at the serge ois del Comahue, Bariloche, Argentina. Curators of B, s BAB, BM, CONC, CORD, K, LE, P, SGO, S, SI, helped specimens. C. Ezcurra provided constant support thro t c n of this work. J e acknowledges fiiis from the Universidad Nacional del Comahue n = Osterreichischer Austauschdienst (OAD-Austria), n = : . American Research LX (KLARF), Royal Botan ens, Kew, which = visits to B, BM, K, LE an Comments by P. M. Pet S. Probat and V. 'Hollowell improved the script. Laboratori clar IMBIV, Universidad Nacional de Córdobe, Vélez Sarsfield 1609, X5016GCA Córdoba, Argentina. jchiapella@imbiv.unc.edu.ar. *Instituto de Botánica Darwinion, Labardén 200, B1642HYD San Isidro, Argentina. doi: 10.3417/2008115 Ann. Missourt Bot. Garb. 97: 141-162. PuBLIsHED ON 9 JuLy 2010. 142 Annals of the Missouri Botanical Garden from Asia and the North Pacific are raised to specific status (Chiapella & Probatova, 2003). Some endemics exist in high mountains or islands, most notably D. chapmanii Petrie, D. gracillima Kirk, D. pusilla Petrie, and D. tenella Petrie in New Zealand; D. christophersenii C. E. Hubb., D. mejlandii C. E. Hubb., D. robusta C. E. Hubb., and D. wacei C. E. Hubb. in the Tristan da Cunha Islands; D. klossii Ridl. in the mountains of Indonesia and Papua New Guinea; D. argentea (Lowe) Lowe and D. maderensis (Hack. & Bornm.) Buschm. in the Madeira Islands; D. dom- ingensis Hitche. & Ekman in the Cordillera Central of Hispaniola; D. foliosa Hack. in the Azores Islands; D. koelerioides Regel and D. pamirica Roshev. in the Pamir Mountains; D. liebmanniana (E. Fourn.) Hitche. in the mountains of Central Mexico; D. nubigena Hillebr. in Hawaii; and D. angusta Stapf & C. E. Hubb. in the high mountains of tropical Africa. The species present in South America are restricted to the subcontinent, with the exception of D. danthonioides (Trin. Munro ex Benth. and D. elongata (Hook.) Munro ex Benth., which are also found in western North America; the nearly cosmo- politan D. cespitosa; and D. setacea (Huds.) Hack., which is found in Europe and central Chile. The genus Deschampsia was described by Palisot de Beauvois (1812) to honor J. C. A. Loiseleur Deslong hamps, physician of the rescue expedition of the explorer La Pérouse. Palisot based his new genus on Aira cespitosa L., a species described in the first edition of Species Plantarum (Linnaeus, 1753), and included three other taxa (D. discolor Roem. & Schult., D. juncea P. Beauv., and D. parviflora P. Beauv.). Linnaeus (1753: 64) separated the species of Aira into two groups, one with muticous lemmas and the other with awned lemmas, and included A. cespitosa in the latter group. In addition to this character, Palisot (1812: 91) characterized Deschampsia as having paniculate inflo- rescences; 2- or 3-flowered “glumes” (= spikelets); glumes longer than the spikelets; lemmas with several teeth; and awn straight, inserted in or near the base of the lemmas, and slightly longer than the lemmas. This rather vague combination of characters and the high morphological diversity and abundance of Deschamp- sia, particularly of D. cespitosa in Eurasia (Chiapella, 2000; Chiapella & Probatova, 2003), resulted in a weak generic concept, as the same description applies to several slightly different forms. Avenella flexuosa (L.) Drejer and Vahlodea atropurpurea (Wahlenb.) Fr. ex Hartm. have had an obscure taxonomic history, being neglected in nearly all European, North American, and South American revisions (see Albers, 1972a, b, 1978, 1980a, b, c; Albers & Butzin, 1977; García-Suárez et aL, 1997; Frey, 1999), and instead treated under Deschampsia as D. atropurpurea (Whalenb.) Scheele and D. flexuosa (L.) Trin. A molecular sequence study (Chiapella, 2007) has shown that Deschampsia is monophyletic, and, despite a close relationship with the main core of Deschampsia (where the South A Ë : x3 X A E y y HH, (Dl. ff & Fingerh.) Drejer or Vahlodea Fr. are included and should be considered as separate genera. The first South American descriptions of taxa later treated in Deschampsia and Vahlodea were done by Hooker (1847), who described Aira antarctica Hook. f., A. kingii Hook. f., A. magellanica Hook. f., and A. parvula Hook. f. Hooker also mentioned collections from southern Patagonia (Port Famine, Strait of Magellan) and the Falkland Islands (Islas Malvinas) of another common European grass, Aira flexuosa L. (= Arenella flexuosa (L.) Drejer), asserting that these plants could not be distinguished from the European plants. No molecular study has addressed whether the South American populations of Avenella flexuosa, Deschampsia cespitosa, and Vahlodea atropurpurea are introduced or native to the region (collection dates in additional specimens studied indicate localities where collecting took place before significant human influence could be considered the likely cause of introduction). Desvaux (1854) made three new combinations: hampsia antarctica (Hook. f.) E. Desv., D. kingii (Hook. f.) E. Desv., and D. parvula (Hook. f.) E. Desv. Other species mentioned by Desvaux (1854) for southern Patagonia and the Andes of central Chile were D. flexuosa (= Avenella flexuosa (L.) Drejer), D. discolor (= D. setacea (Huds.) Hack.), and D. pulchra Nees & Meyen (= D. cespitosa var. pulchra (Nees & Meyen) Nicora); another species, Aira magellanica, was reduced to the synonymy of D. atropurpurea (Whalenb.) Scheele (= Vahlodea atropurpurea (Wah- lenb.) Fr. ex Hartm.). The new genus Monandraira E. Desv., also described by Desvaux (1854) on the basis of plants with single staminate flowers, comprised two taxa from the Andes of central Chile: Monandraira berteroana (Kunth) E. Desv. (= D. berteroana (Kunth) Trin.) and M. glauca E. Desv. (= D. danthonioides (Trin.) Munro ex Benth.). The prolific German-born Chilean botanist, R. A. Philippi, described Deschampsia latifolia Phil. (non D. latifolia Hoechst. ex A. Rich.) and D. laxa Phil. in 1858; D. lasiantha Phil. (= Trisetum preslei (Kunth) E. Desv.) in 1864; D. andina Phil. (= D. cespitosa (L.) P. Beauv.) and Monandraira patula Phil. (= D. patula D. martinii Phil. (= Avenella flexuosa (L.) Drejer), and D. mi Phil. (see Excluded or Uncertain Taxa) in 1896. The beginning of the century brought the first PU de aite Volume 97, Number 2 2010 Chiapella & Zuloaga Revision of Deschampsia, Avenella, and Vahlodea assessments of the genus, as the expeditions to Patagonia by Dusén (1900) and Macloskie (1904) produced the first general assessments of Deschampsia in the region, recognizing five and 12 species, respectively. Hauman (1918) described D. cordiller- arum Hauman, pointing out its resemblance to D. flexuosa (= A. flexuosa) but noting that it differs by xerophilous characters (dense tufts of short, rigid leaves), longer ligules, and smaller spikelets. Valencia (1941) transferred four species of Trise- tum Pers. to Deschampsia and made the new combinations D. juergensii (Hack.) Valencia (= T. combinations, arguing that the structure of the lemmas with awns derived from the middle nerve, as displayed by these taxa, corresponds more to Trisetum; Parodi also updated Deschampsia in South America, accept- ing 17 species, including three new species and two varieties (D. looseriana Parodi, D. looseriana var. triandra Parodi, D. mendocina Parodi, D. venustula Parodi, D. berteroana var. parvispicula Parodi) and three new combinations (D. glauca (E. Desv.) Parodi, D. elegantula (Steud.) Parodi, D. elegantula var. patula (Phil.) Parodi). MATERIALS AND METHODS This study is based on herbarium specimens of B, BA, BAA, BAB, BM, CONC, CORD, K, LE, P, S, SGO, SI, US, and W (Holmgren et al., 1990), including nearly all types. In our study, we used the phylogenetic species concept (Cracraft, 1983), whose main assumptions are: a species is the smallest diagnosable unit of (sexual) populations possessing at least one diagnostic character that is present in all considered diagnostic, although it was not always possible to find clear gaps in quantitative characters. In the descriptions of leaves, the first measurement range is the blade length (expressed in centimeters) and the second measurement range is the blade width (expressed in millimeters). Key ron cine: AVENELLA, DESCHAMPSIA, AND. VAHLODEA IN SOUTH la. PM ovoid to oblong, 3.5-5 mm; en ovate to obtuse, blunt, never acute, 2.5-5 mm; plants always perennial. 2a. Leaf blades filiform, ee convolute, folded or bristlelike, ca. 1 mm e venei 2b. Leaf blades flat, never condupliate or or — up to 6 mm wide; X. Vahlodea lb. ice lanceolate, 2-4 mm; ligules acute, 5-10(12) ants annual or perenni HL TAXONOMIC TREATMENT I. Avenella (Bluff & Fingerh.) Drejer, Fl. Excurs. Hafn. 32. 1837. TYPE: Avenella flexuosa (L.) Drejer. jae I Rep. Fl. Mt. Daisetsu 12: 73. 1930. TYPE: tus flexuosus Honda ex Nakai. Plants perennial, caespitose, sometimes with short rhizomes, flowering culms slender; bud initiation — or extravaginal. Leaf sheaths glabrous ranous margins; blades filiform, pointed; psi obtuse, membranous. Inflorescences paniculate, open; capillary branches dichotomously spreading, with higher order pedicels, minutely scabrous upward. Spikelets oblong, 2-flowered, purplish to silvery; glumes slightly unequal, lower glumes lanceolate, l-nerved, upper glumes lanceolate, 3-nerved, often scaberulose on the midnerve and near apex; oblong, membranous, back rounded, 4(5)-toothed, pert aiam. uiua teeth p PM the lateral, ; rough; awn in the lower 1/3 of lemma; hes 2-keeled, shorter than the lemma, hyaline or sometimes membranous, scaberulose on the keels, apically erose; anthers 3. Caryopses ovoid, purplish; hilum punctiform. 1. Avenella flexuosa (L.) Drejer, Fl. Excurs. Hafn. 32. 1838. Basionym: Aira flexuosa L., Sp. Pl. 1: 65. 1753. Deschampsia flexuosa (L.) Trin., Mém. Acad. Imp. Sci. Saint-Pétersbourg, Sér. 6, Sci. Math., Seconde Pt. Sci. Nat. 2(1): 9. 1836, non rm. (L) P badedddi. flexuosa a Schur, Enum. PL Transsilv. 753. 1866. Podianapus flexuosa (L.) Dulac, Fl. Hautes-Pyrénées. 83. 1867. Salmasia flexuosa (L.) Bubani, Fl. Pyrene (Bubani): 4. 319. er : Europe. "in petris, rupibus" (lect , designated by Clayton in Milne- pni & Polhill [1970: 94], LINN 85.11 not seen, photo S!). Aira versicolor Roe | € Veg., ed. 15 bis [Roemer & Schultes T 679. Meo: Argentina. Islas Mahi [Falkland sn Portu oe: 1789, L. n. (holotype, MA not seen; isotype, BAA!). —À tenella Phil., Anales Univ. Chile 94: 25. 1896, . hom., non Deschampsia tenella Petrie, Tram. & Proc. New Zealand Inst. 23: 402. 1891. ia philippii Mee. Rep. Princeton Univ. Exp. Botany 8: 961. 1906, as “philippi.” "A Chile. Tess ibn Palena," Jan. 1887, F. IM s.n. (holoty seen; isotype, BAA ex SGO!). Aira vestita atta Steud. Syn. Pl. Glumac. 1: 424, tab. 49b. 1854. Desc ia vestita ge Hauman, i 1 Hauman & ::391. Parodi, Physis (Buenos Aires) 929. TYPE: Chile. — Point, s.d., w. tedio 1193 ME pt isotypes, BAA ex P!, BAA ex S!, GOET not seen, fragm. US 02695871 se seen uen martinii Phil., Anales Univ. Chile 94: 24. 1896. TYPE: d “insulis a nis,” Dec. 1884. n. (ho Martin s.n. not seen; isotype, BAA ex macloviana Gand., Bull. Soc. Bot. Fra 28. 1913. TYPE: "e aer Islands, i a F. Port Harriet," seen; isotype, BAAL m ex eT g 124 (holotype, S not Perennial, caespitose grass, new protruding through the base of the cs: ac branching) sometimes rhizomatous; culms 35—70 cm tall, 2- or 3-noded, erect or bent, sheaths glabrous with — margins. Leaf blades 5.5-10 cm X 0.5— mm, sondia i to filiform, stiff, pointed, glabrous nd somewhat papillate abaxially; ligules 2.5— 3 mm, obtuse, s. Panicles 7.5-12.5 X 2- 5 em, open and loose, with 5 to 7 verticils, branches spreading from the main fertile axis, dichotomously spreading, with higher-order pedicels, minutely sca- brous upward. Spikelets oblong, 2-flowered, purplish to silvery; lower glumes 3.5-5 mm, lanceolate, l-nerved, upper glu S mm soils, 3-nerved, often apex; lemmas ser 5 mm, oblong, membranous, adaxially rounded, in the upper 1/3, 4(5)-toothed, teeth minute, central teeth larger than lateral teeth, rough; awn 5.5-7 mm, bent and twisted, inserted at the base or from the lower 13 of lemma; palea 3-5 "Td — S or sometimes membranous, pahe the apex; anthers l .5-2.5 mm. Caryopsis 12, mm, ovoid, brownish purple. Chromosome number. 2n = 28 (Hubbard, 1984, as Deschampsia flexuosa). Illustration. Nicora (1978: 230). Distribution, habitat, and phenology. Avenella flexuosa is a common species that is distributed throughout Europe, eastern North America, northeast- em Asia (Kamchatka to Japan), New Zealand, high mountains in west-central Africa (Kilimanjaro Moun- forests, from sea level to 1000 m elevation. Flowering occurs from December to M Annals of the Missouri Botanical Garden Discussion. Avenella flexuosa has been cited as introduced for Costa Rica (Davidse, 1994) in altitudes of ca. 3000 m m. » presence bis ep pis outside the normal d Aira flexuosa var. ondis Brongn. (in Duperrey, Voy. Monde, Phan. 2: 23. 1829, nom. illeg. hom.) is a later homonym. Specimens from the Falkland Islands (Islas Malvinas) do not differ from continental specimens. Specimens examined. ARGENTINA. Chubut: Dpto. Futaleufú, región del Río Corcovado, Cholila, 43°S, 71°W, N. Ilin s.n. E — La Plata, A. Soriano 3137 (BAA); Dpto. Río Se ontana, » Castellanos 5946 (BA, S); Lomada del € ee de valle, R. León 2364 (BAA). Santa Güer Aike, 3 km NW de Villa Minera Río Turbio, S. iere & S. Arroyo 3667 (BAB); 26 km S of Rio Gallegos, W. J. Eyerdam et al. 24084 (SI); Dpto. Lago Argentino, Lago —— P. James 40 (SI); Parque Nac. Los Glaciares, camping Arroyo entoso, 50729'14”S, 12*51'30"W, A. Cocucci E A. Sérsic 2493 (CORD); Dpto. Río Chico, ES Río Blanco, R. N. Luti 3749 (CORD); pee o Deseado, E. Ancibor & A. Vizinis (BAA). add p uego: P o. Ushuaia, Ushuaia, R. » Luti 1645 (CORD); Lapataia, S. Crespo s.n. (SI); Archipel d'Ushuaia, 25 Feb. 1896, N. Alboff s.n. (CORD); Ushuaia, 7 me 1896, N. Alboff s.n. (CORD); Dpto. Río Grande, near o Grande, ca. 1 m from ocean, Y. Mexía 7911 (S); San ipi P. Dusén 304 (CORD); Rt. Nac. 3, San Sebastián, A. T. Hunziker 8266, 8275 (CORD); Islas Malvinas, Port Stanley, E. A. Ulibarri et al. 1073 (SI); q Malouines, D. Sellow s.n., Voyage i 1825 (P) CHILE. Aisén Region: Lago Buenos s, Valle León, I. von d 6280 (SD. Biobío me po Quebrada H onda, K. Behn 20267 (CONC). Los on: Llanquihue, Cerro Vichadero, Casa Pangue, A. Pp 13568 (US). Magallanes and Antartica Chilena n: Ülti Cord. Paine, M. T. K. Arroyo et eG 92-316 (CONC); Parque Nac. Torres del Paine, Cerro Diente, M. T. K. Arroyo & F. Squeo 85-0891 (CONC); Cerro Donoso, sect. Río Las Chinas, M. T. K. Arroyo et al. 87-0219 oe Punta Arenas, C. Montero 6206 (CONC); 78 km NW of Punta Arenas, rd. to Puerto Natales, W. J. E ero et al. 24165 (SI); Isla Navarino, Puerto Williams, Caro ra, F. Schlegel 8119 (CONC); Ile Navarin, Sierres nd 25 Feb. 1896, N. Alboff s.n. (CORD); Punta Arenas, Chabunco, p & Ricardi 11 ae (BAA); Cerros del Club de Ski Punta Arenas, Pfister Ricardi 11720 (BAA); Detroit de Magellan, Port Lait Voyage de l'Astrolabe et de la Zeléc, 1838-1840, M. Jacquinot Hombron s.n. (BAA) Il. Vahlodea Fr., Bot. Not. 141, 178. 1842. TYPE: Vahlodea atropurpurea (Wahlenb.) Fr. ex Hartm. Caespitose perennials; bud initiation often extra- vaginal. d sheaths glabrous to rather scabrous, margins membranous or more rarely scarious; blades flat, pilose, middle nerve prominent with varying number of secondary nerves, pointed; ligules ovate to obtuse, membranous. Inflorescences paniculate, erect, open; branches lax, slender, nodding, scabrous. Spikelets ovoid, 2-flowered, mostly violaceous, pedi- ; rachilla pilose, hairs about half the ee eee te ee SS Volume 97, Number 2 2010 Chiapella & Zuloaga Revision of Deschampsia, Avenella, and Vahlodea length of the lemma; glumes equal or slightly unequal, lower glumes broadly lanceolate, 1-nerved, keeled, upper glumes lanceolate, longer, 3-nerved, usually only the midnerve scabrous; lemmas 4(6)-toothed, membranous; awns straight or geniculate, twisted, slightly exserted, stout, scabrous, inserted in the upper half of the lemma, rarely in the middle or lower; paleae hyaline, shorter than the lemma, 2-keeled; keels scabrous, sometimes slightly us between the keels; anthers 3, purplish. i fusiform. teeth minute, equal, 1. Vahlodea atropurpurea (Wahlenb.) Fr. ex Hartm., Handb. Skand. Fl. (ed. 4): 30. 1843. Basionym: Aira atropurpurea Wahlenb., Fl. Lapp. (Wahlenberg) 37. 1812. Holcus atropurpureus (Wahlenb.) Wahlenb., Svensk Bot. Tidskr. pl. 687. 1826. Avena atropurpurea (Wahlenb.) Link, Hort. Berol. 1: 119. 1827. Deschampsia atropur- purea ye ahlenb.) Scheele, Flora 27: 56. 1844 TYPE: Finland. “Hab. in fruticetis campis et Rp subuliginosis per partem subsylvati- cam totius Lapponiae passim copiose. . . in Enare juxta Jvalojoki et Sotajoki," 22 Aug. 1802, C. Wahlenberg s.n. (lectotype, designated by Mo- berg & Nilsson [1991: 293], UPS not seen, photo ex UPS!; duplicates, LE-TRIN 1856.01*!, BAA!). Aira magellanica Hook. f., Fl. Antarct. 2: 376, t. 134. 1846. Aira atropurpurea var. magellanica (Hook. f.) I Svenska Vetensk.-Akad. Handl. 56(5): 174. Chile. Port Famine, s.d., James Anderson ee K!; isotypes, BAA fragm. ex K!, photo US 867650 ex K!). epee r bractophyla Phil., Anales Univ. Chile 94 PE: Chile. “Habitat i in valle fluminis > 180; xe s.n. (holot 37212 not seen; isotype; BAA fragm. ex SGO!). Perennial, tufts loose, extravaginal or intravaginal abaxially glabrous to sparsely pilose, adaxially pilose, trichomes soft, white, ca. 1 mm, sometimes i missing in very old specimens, middle nerve promi- nent with 4 to 6 nerves on each side, pointed; ligules 3.5-5 mm, ovate to obtuse, membranous. Panicles 5— 8.5 X 1.54 em, lax, open, branches slender, nodding, scabrous, more densely scabrous close to the spikelets Spikelets 2-flowered, ovoid, + clustered t branch apices, n to violaceous, or gold, ca scabrous, rachilla villose, hairs reaching about half the length of the lemma; lower glumes 4— 5 mm, broadly lanceolate, 1-nerved, keeled, upper glumes 4.5-5.5 mm, lanceolate, 3-nerved, usually only the midnerve scabrous; lemmas 4(6)-toothed, teeth minute, equal mm ranous, awns 2— mm, usually geniculate or weas straight, e slightly exserted, stout, scabrous, inserted in he upper half, dis d 2-keeled, keels scabrous, sometimes slightly scabrous between the keels; anthers 0.8-1.5 mm, purplish. Caryopsis 0.5-1 mm, narrowly fusiform, rown to brownish red. — rarely in the lower; paleae 23.5 mm, Chromosome number. 2n = 14 (Albers, 1972a, b). Illustration. Hitchcock et al. (1969: 548) (as Deschampsia atropurpurea Distribution, habitat, and phenology. Vahlodea atropurpurea has a primarily Northern Hemisphere, circumpolar, amphi-Atlantic distribution; in southern South America it is distributed from 32°S to 54°S (Strait of Magellan region), where it is found on rocky, humid slopes, between 400 and 2300 m elevation. Flowering occurs between January and March. Discussion. those in the Northern Hemisphere) have been treated as a different subspecies by Hultén (1941, 1968) and Haraldsen et al. (1991); the latter authors found that low genetic variation among Canadian and Norwegian populations was correlated with fewer morphological differences, thus giving little support for treatment as separate taxa molecular studies have been performed on South American populations. morphological similarity of Northern and t Hemisphere plants is supported by characters report- ed in Haraldsen et al. (1991: 316, table 5): leaf length is slightly longer in South American plants; spikelet length and awn length are slightly shorter in South American plants. Treatment of the southern popula- tions as a separate taxon is not warranted, and we think more detailed comparative morphological and molecular studies are needed to address this question. The populations in South America (vs. The hern pecimens examined. ARGENTINA. Chubut: Dpto. Futaleufá, P. arque Alerces, Lago DER orilla Este, A. E uice 4169 (BAA). Bekins: Dpto. S Rafael, yrs del río Atuel, mina de azufre, 80 km W de El Sosneado, O. Boelcke et al. 10213 (SI). Neuquén: Dpto. inas, an de la Laguna Varvarco Campos, O. Boelcke et al. 14217 (SD; Dpto. Huiliches, Volcán Lanín, M. N. ); Dpto. Lácar, Parque Nac. Lanín, Lácar, Cerro Malo, R. León & C. E. (BAA) Dpto. Los a A Laguna Las Millaqueo, J. m (SI); Cerro Colorado, J. Diem 253 (BAA); Parque Nac. Nahuel Huapi, Portal Pantojo, L. Cusato (BAA); SETA Arroyo Minero, O. Boelcke £ M. N. Correa 7216 (BAA); Cerro e Mol. 0. Boelcke & M. N. Correa 7129 (BAA). Río Negro: Dpto. Bariloche, Cerro L. R. Parodi 11506 "a A. Burkart 6150 (BAB); I. Annals of the Missouri Botanical Garden von Rentzell 14661 (Sl); Cerro Catedral, U. Eskuche 328 (BAA); Laguna Frías, camino a Cerro Riggi, R. Pérez Moreau sn- (BA-34986, BAA); — > Rigi, 4 L Cabrera 6055 ridi nes o San Martín, desemboca- dura del Río Fósiles, 19 Jan. 1918, A. Bonarelli s.n. (BA dim h : o. Ushuaia, Sierra Valdi- Dpto. U Río - Skottsberg 240 (S); Cerca de Castillo, bo bosque de la Matanza, 31 Jan. 1942, A. Castella. s.n. (BA 45566). CHILE Region: Lago O'Higgins, Florida, 4. Donat 527 (BAA); V. Thénmayer?, - rs A Donat s.n. (BAA). Magallanes Region: El P. arrillar, E. re V. 2519 CoNo; Cordillera del Paine, Jan. 1931, Donat s.n. (BAA Península Brunswick, A. Donat 455 t A). HI. Deschampsia P. Beauv., Ess. Agrostogr. 91-92, pl. T 3. 1812. TYPE: Deschampsia cespitosa (L.) P. Monandraira E. Desv., Fl. Chil. e 6: x 1854. TYPE: aira a leiioon M th) E Sy n os i: 423. m TYPE: Aristavena E Albers & bro ¿FAA 8(1): 83. 1 ristavena setacea (Huds.) F. Albers & iie Plants perennial or annual, often forming tussocks; culms erect, usually < 150 cm tall, sometimes slightly bent at the base, slender to stout. Leaf blades flat, folded, or convolute, =r or pubescent; ligules membranous. Inflorescences paniculate, open to con- tracted. Spikelets 2- flowered (rarely 1 or 3), usually perfect, sometimes cleistogamous, somewhat com- pressed, typically purple or violaceous to pale green, disarticulating above the glumes; rachillas prolonged beyond the upper floret, pubescent; glumes approxi- mately as long as the spikelets, usually 1- to 3-nerved, keeled to rounded, usually cis € florets, roughly equal t o I l in size apex acute; lemma 3- to 5-nerved, the central nerve u dll continuing as the awn, awn dorsal, straight to bent, sometimes twisted below its lower half, inserted from the top to the base of the lemma, sometimes reduced to a minute appendage, lemma apex (2)4-toothed, thin; paleae generally as long as the lemma, 2-keeled, hyaline; lodicules 2, lanceolate to acute or lobed, frequently wider above the mod ovary glabrate, with a few apical ee eS 3. Caryopsis ovoid to fusiform, when ith tl lea: hil elliptic; embryo small; se hard to soft. Discussion. Cheeseman (1906) noted that the awns of species of Deschampsia from New Zealand were extremely reduced and sometimes inserted close to the top of the lemma; this is a unique feature in the genus, which generally has awns that are developed inserted on the lower 1/3 or near the base of the lemma. Parodi (1949) provided a qme of the genus and considered this variation. The preliminary molecular data, available from nuclear ITS ien plastid trnL sequences, support the inclusion of the New Zealand taxa in the genus. The two species D. chapmanii and D. tenella were included in the main clade of Deschampsia (Chiapella, 2007). KEY TO THE SPECIES AND VARIETIES OF DESCHAMPSIA IN SOUTH AMERICA la. Plants up to 50 cm. Plants annual. 4a. Glumes rves acib P as ae fo hee (ales o Ere ii Tie dU de Rer c E D. berteroana 4b. Gl with only the dorsal midnerve sc j F = TA ipa mm, inserted at the base of the imik mma; panicles 5-25 cm ...... 6. D. danthonioides 2b. Plaut s ue -10 mm, inserted in the middle of the lemma; panicles 412 IE ka 10. D. loose: 6a. Panicles 2-7.5 cm, us contracted t t ree Ce o TN V appearance; branches adpressed. APA Tb. in indi er Nauta, qawapi CR WC GC Ned wd me. > n stout, strongly bent or curved; spikelets 2- or 3-flowered .............. 12. D. parvula 9a. Callus hairs 6b. Panicles 3-18 cm, 10a. pale y. ered weak, straight, m or barely bent; e 2-flowered. ing the middle of lemma 2.0 9b. Callus hairs bin the middle of the L. D. antarctica (Antarctic specimens) ksi surpassing the middle . 13. D. patula mu "MEO € e nd ds ME eee Ne Bele aes eye are disci (continental specimens) Ma. Lemmas IM "dx uei d. RR E 14. D. setac: lb. M) iet cm Marcus z ; cepto "i f 2 Suas usati eene E UE 15.1: Soca Panicles contracted, spikelike | beh Kiss ou Do P prem en E oin elo : X NA A a E A ma a ngata Peri lower glume 1- s (exce ptionally 3-nerved in D. cespitosa), upper aad: 3-nerved. Leaf blades with prominent adaxial ribs; nerves glabrous or slightly scabrid to sparsely scabrous. Volume 97, Number 2 2010 Chiapella & Zu loaga Revision of Deschampsia, Avenella, and Vahlodea 15a. Awns present in all florets, the awn inserted at the base or in the lower 1/3 of the lemma ... 15b. A Se i ath coe thao | n l4b. Leaf "im uen ria ut tribe, nerves densely scabrous on both surfaces 5: 13b. i sa 5-9. s stout, fae caespitose; ligules acuminate x Pd delicate, slender, not caespitose; ligules truncate The 15 species of Deschampsia described here are found mainly in the Andes of Argentina and Chile, from ca. 30°S to Tierra del Fuego, in a wide altitudinal range (300-4000 m), but mainly restricted to wet places near lakes, rivers, creeks, bogs, etc localities outside this main distribution area with collections of D. cespitosa (in Bolivia and Brazil, see Specimens Examined) require further studies in order to determine whether introduced. No . Two they conservation threat has been detected for de species, although the high mountain habitats where some of them are found are particularly fragile. 1. Deschampsia airiformis (Steud.) Benth. & Hook. f., Gen. Pl. 3: 1158. 1883. Bas Trisetum airiforme Steud., Syn. Pl. Glumac. 1: 229. 1854. TYPE: Chile. “Arique, in asionym: pratis isotypes, fragm. BAA GOET ey seen, K!, US 91466 not seen). Agrostis desvauxii Phil., Linnaea 33(3—4): 288. 1864. TYPE: Chile. “In andibus prov. Santi A. Philippi s.n. (holotype iso A tag. = ex SGO!, K ex SGO photo!, SGO 37491!, US 556317 fragm. ex SGO PHIL-140 not seen). Annual with slender, delicate culms 4—15 cm tall, l- or 2-noded, slightly bent at the base, sheaths glabrous wit margins. Leaf blades linear or narrowly linear to bristlelike, stiff, 1-6 cm X 0.8-1.5 mm, adaxial side with the nerves moderately to densely scabrous, less dense abaxially; igule elongate, 1.5—5.5 mm, scarious. Panicles contracted 1.5—5.5 X 0.5-2 cm, with 4 to 8 verticils, branches scabrous to densely hirsute. Spikelets (1)2- flowered, green; rachilla with abundant pubescence in the upper half, glabrate or minutely pubescent below; lower glume narrowly lanceolate, 3—6 mm, (1 or 2)3- arrowly lanceolate to lanceo- minutely scabrous on the central nerve and distal 1/3, sparsely scaberulose between the nerves distally, argins scarious; lemma with apex 4(5)-toothed, lateral teeth acute and larger than the central ones; awn stout, bent, rarely straight and basally twisted, 3— 8 mm, inserted at the base or in the lower 1/3; palea hyaline, 1.5-3 mm, 2-keeled or rarely flattened, keels . D. cespitosa var. pulchra * ^e c» e & 9s e sc o...o.n......... + scabrous; anthers 1-2 mm, brownish red. Caryopsis 1-2 mn, ellipsoid, light brown. Illustration. Nicora (1978: 242). Distribution, habitat, and phenology. Deschampsia airiformis is found in the Andes of Argentina and Chile, from 40°S to 50°S latitude, between sea level and 800 m elevation. Flowering occurs in January and February Discussion. _ Deschampsia airiformis was observed as often tized e the rust Tilletia cerebrina Ellis & Everh. Pk 10 78). This rust fungus (Ustilagi- nomycetes, Tilletiales) infects mostly pooid grasses as hosts (Castlebury et al., 2005). The distribution range of D. airiformis overlaps with that of D. berteroana, another annual of similar habit from central Chile, from which it differs in the shorter leaves and more contracted panicles with densely scabrous panicle ranches. The overlapping and extended range of the annual species of Deschampsia agrees with Arroyo et . (2002), who suggested that many elements of the high Andes flora might have used the high mountain corridor to faciliate migrations. Specimens examined. ARGENTINA. Chubut: Dpto. Tehuelches, — Cuatro, E. Nicora 9340 (SI); Río Pico, , A. Soriano 4626 (BAB); Apeleg, Est. 3 a pi Soriano 5802 i E : Dpto. Minas, Laguna Varv Cam nfermera, 36"17'S, 70°39'W, O. Boelcke ira 14056. DAE. Dpto. Los Lagos, Est. Fortín Chacabuco, O. Boelcke 3201 (BAA); camino a Traful, L. R. Parodi 15358 E CHILE. Arauc Region: Malleco, Lumaco, Santa Clara, G. Kunkel p (CONC). 2. Deschampsia antarctica E. Desv. Fl. Chil. eplaced name: Aira ab. 150. 1838 Aira antarctica G. Forst., 1786. TYPE: Antarctica. New South Shetland Islands, s.d., Eights s.n. (holotype, K!). Airidium elegantulum Steud., Syn. Pl. Glumac. 1: 423. 1854 schampsia elegantula (Steud. ) TS e 8: 452. 1949. TYPE: Chile. “ as,” Feb. 1853, W. Lechler 1220 (holotype, a as "BAA! Ki, US-76314 fragm. not seen Deschampsia fuegina Phil., re Univ. Chile 94: 23. 1896. TYPE: Chile. Tierra del Fuego, Hab. Fuegia Orientalis, Feb. 1879, s. coll. (holotype, SGO PHIL-208 not seen, Annals of the Missouri Botanical Garden photo!; isotypes, BAA ex SG0!, US 556482 fragm. ex SGO PHIL-208 not seen). Deschampsia antarctica f. breviaris à Dusén, Wiss. Ergebn. Schwed. Exped. Magellansl. 1895-1897 pt. 5: 221. 1900, nom. nud. Perennial, forming dense caespitose tufts of basal leaves; culms slender, 10-25 cm tall, 1- or 2-noded, sheaths glabrous with margins membranous, more rarely scarious. Leaf blades conduplicate to filiform, 1.5-5.5 em X 1-1.5 mm, adaxial nerves scabrous, abaxially glabrous to minutely scabrous; ligules acuminate to acute, 2-9 mm, scarious. Panicles pyramidal, loose to contracted, when contracted partially included in the uppermost sheath, 4.5—15 x 1.5-6 cm, with 3 to 7 verticils; branches spreading, filiform, scabrous to densely hirsute at the distal 2/3. Spikelets 2(3)-flowered, green to violaceous, or varie- gated with both colors; lower glume narrowly lanceo- late, 3-5.5 mm, 1-nerved, upper glume narrowly lanceolate to lanceolate, 4-6 mm, 3-nerved, both glumes ciliate on the central nerve and sometimes also scabrous between the nerves, basally glabrous, margins scarious; callus pilose, hairs short, not reaching mid- lemma in the non-antarctic specimens, even shorter in the antarctic specimens; rachilla pilose in the upper half; lemma bilobate, 4-toothed, lateral teeth longer than the central, scabrous to hirsute at the apex; awn straight, rarely geniculate, somewhat twisted at the base, 3—7 mm, weak, inserted in the lower 1/3, rarely at the middle, sometimes exserted, scabrous; palea hyaline, 2-3 mm, 2-keeled, keels moderately to densely scabrous; anthers 0.5-1.5 mm, pale yellow. Caryopsis 0.5-1.5 mm, ovoid, brown. Illustration. Hooker (1847: t. 133). Distribution, habitat, and pheno, Deschampsia antarctica is one of only two vascular plant species known to be native to Antarctica. The taxon is also found in several adjacent southern islands (Falkland Islands [Islas Malvinas], South Georgia, ney, South Shetlands, Palmer Archipelago, Bouvet, Crozet, Kerguelen) and in the southern part of the merican continent. Flowering occurs from November to February. Discussion. Deschampsia antarctica is a species similar to the Andean D. venustula and can be distinguished from this taxon by the longer awns that exceed the glumes and the spikelets, which are broadly lanceolate and purplish along the keels in D. venustula versus the spikelets being lanceolate and not colored in D. antarctica. The panicles in Deschampsia antarctica show clear dimorphism between the Antarctic and continental specimens, being closed, contracted, and often with the lower part included in the uppermost sheaths in the plants of Antarctica and some subantarctic islands, but typically open and exserted in continental individuals. It is possible, however, to find contracted panicles in Antarctic forms on the continent and plants with open, larger panicles in the subantarctic islands (the type specimen collected in the South Shetland Islands is a plant with an open, pyramidal panicle). The subtle morphological differences of both forms correspond to almost completely nonoverlap- ping areas of geographic distribution, making possible their differentiation as subspecies sensu Du Rietz (1930). The florets of the Antarctic plants are commonly cleistogamous, while plants with both hk d ls oe t oan hoa £ A in Tierra del Fuego. The molecular evidence available is limited, however, and has focused mai y on Antarctic and subantarctic island populations (Hol- deregger et al., 2003; Van de Vouw et al., 2007). A formal proposal of division in subspecies would require support of a study including several conti- nental populations. Buschmann (1949) cited Deschampsia antarctica as introduced to Holland in 1936. The growth period of this species is particularly well suited for the rigorous conditions of Antarctica; the plants begin to grow during November, the flowering starts in the first week of January, and by the end of the month it is already possible to observe mature spikelets. The quantity of fertile seeds produced, however, is smaller than those produc by plants growing outside Antarctica, e.g., in the Kerguelen Islands, Falkland Islands (Islas Malvinas), and Tierra del Fuego (Corte, 1961). Dusén (1900) published the name Deschampsia antarctica f. breviaristata, mentioning the specimen 0. Nordenskjöld s.n. (Argentina, Patagonia australis: in valle superiore fluminis Gallegos), ause neither a valid description nor illustration is provided, it is considered a nomen nudum according to the International C of Botanical Nomenclature (McNeill et al., 2006: Art. 32d). The search for the specimen collected by O. Nordenskjöld was not successful in the herbaria W (Hackel collection), S, and UPS. Specimens examined. ARGENTINA. Chubut: Dpto. Tehuelches, Lago Vintter, E. Nicora 10231 (SI); Est. Caridad, 43°40’S, 71°20'W, costa del Rio Carrenleufá, A. Soriano 2554 (BAA, BAB); Valle Laguna Blanca, 71°15’ W, 45°52'S, J. Koslowsky 224 (BAA); Valle Huenuleo, 45°55 A. Blanche, A. Soriano 2245 (BAB) Río Negro: Dpto. Pilcaniyeu, Est. Rayhuau, O. Boelcke 4486 (BAB). Santa Cruz: Dpto. Lago Argentino, El Calafate, M. N. Correa et al. cede usas E E aie ar re EM AE deed eai Volume 97, Number 2 2010 bro 2 Zuloaga 149 Revision of Deschampsia, Avenella, and 3082 (BAB); DM Lago Buenos Aires, meseta del Buenos Aires, Est. La Vizcaína, E. G. Nicora 26417 (BAA); Río Coyle, Eval. Las Vegas, L. Dauber 168, 196 (BAB); Dpto. Giier Aike, Est. La Verdadera Argentina, 50^51'S, 72*14'W, s.d., S. Arroyo et al. s.n., TBPA 2139 (BAB); Laguna Céndor, 51°46’S, 71°40’ W, o. Boelcke et al. 12446 (BAB); prox. Puesto 2 Antonios, 51737'S, 72^11'W, J. A. Ambrosetti & E. ae 206 (BAB); Dpto. Rio eh Lago Burmeister, Parque Nac. Perito Moreno, M. J. Dimitri & H. Correa Luna 8243 (BA). Tierra del Puig: Dpto » Us huaia, Ushuaia, N. Alboff 1027 (CORD), M. 8. dirai agp P (CORD); “ile = Canal Beagle, próx. base naval, e= Moreau 1923 (BAB); Est. roget D. M. Moore 1349 (BAB, K); Dpto. Río rande, “Fuegia An — Río e 14 Jan. T E Dusén 405 (CORD); Est. Los Flame 46 km W of Río Grande, D. M. nn P. Goodall 276 chat E. Rt. 3, Río Grande, A. T. Hunziker 8225 (CORD); Golfo San 0 (BAA); Valle de Tierra Mayor, n Ruiz Leal & s o Fagnano, Cast dic 7572 (BAA); Laguna Grande, Sección Mirnski J. H. — 6763 (BAB); Antártida Argentina, Base Primavera, s.d., M. Lauría s.n. (BCRU); A. Corte 1 (BAA); -e dac Tierra de Graham, F. Behn d E S); Puerto Paraíso, Cerro La Cruz .Z Popovici n. (BA 67264); Islas Malvinas Isla Soledad, Puesto Stanley, Port Stephens, Cape Meredith, D. M. hier sof = Ps Sy Archipiélago Melchior: Isla Sobral, es, costa SO, A. T. Hunziker 10190, 10196 (BAA, CORD ‘Isla “ar Panta NO, R. N. Luti 1485 (BAA, CORD); A. Martínez T ae Georgia Island: Stromness Bay, S. W. a 58 (S, SI); Cumberland a 15 May 1902, C. oe (S). Palmer Archipelago: Pointe Maia: de l'ile Anvers, 64^50'S, 63^50'W, 10 Nov. 1905, Dr. Turquets s.n., wy oia ntarctique Frangaise (BAA, P); Île Anvers, baie p Biscue, 10 Feb. 1905, Dr. Turquets s.n. (CORD); Lysted Island, "OF 19S, 62^53'W, P. Siple 336 (BAA, P); Isla Sobral, = NE, sobre el canal Murature, frente a Isla Piedrabuena, A. T. Hunziker 10200 Island, Marlet Inlet, Admiralty Bay STA Potter, A. T. Hunziker 10147, 10150, 10152, 10153 (BAA, nziker CORD); Isla Media Luna, peñasco meridional, A. T. Hu 10112 (CORD), promontorio rocoso al SO de la Isla, A. T. Hunziker 10121, 10205 (CORD): Isla 25 de Mayo, Base Jubany, s. coll, (CORD 1172). South m Islands: Can delmas Island, N ü wait em lagon Longton 601 (BM). CHILE. Mag Isla Riesco, seno Skyring, Estancia Tin A. yo» & £. Ricardi 11938 (BAA); 15 km S of Punta Arenas, moist sandy loam, W. J. Eyerdam et al. 24115 (K, S); xm. 1903, M. S. apo 187 (CORD); Ültima Esperanza, Lago Balma- ceda, 51%53'S, 72^15'W, M. C. Latour et al. s.n., TBPA 1912 (BAB); Laguna Blanca, Feb. 1927, 2 ÉL 183 (BAA); Cajon de ird s, 3000 m, , F. Laffuel 1903 n inmediaciones de Punta ps y vé de La Mina, 1 1917, A. Bonarelli 96 (BAA); Curicó, Baños de Azufre dd Planchún, 2700 m, Jan. 1933, G. Grandjot : ed Lo Cautín, A. Burkart 9507 (BAA). Kerguelen Isla Procter 16 (BM); oy ire a. der fous, 39 nd 1903, E. Werth s.n. (B); L re Australe, Lote 40, s.d., E. A. De La Rüe s.n. (B); 19081 1909, M. Bossieu s.n. (BAA). YT 3. Deschampsia berteroana (Kunth) Trin., Mém. Acad. Imp. Sci. Saint-Pétersbourg, Sér. 6, Sci. Math., Seconde Pt. Sci. Nat. 4,2(1): 10. 1836. et : i na berteroana (Kunth) E. Desv., Fl. Chil. (Gay )6 6: 343. 1854. Aira berteroniana (Kunth) Steud., Syn. Pl. Glumac. 1: 220. 1854. TYPE: Chile. Rancagua, Oct. 1828, C. L. G. Botes ero 30 (lectotype, designated here, P!; duplicates, S!, SI ex P!, MO not seen, photo!). E ence berteroana var. parvispicula Parodi, Darwiniana 466. 1949. TYPE: Chile. V sans; Limache, Cerro faa A. Garaventa 1667% (holotype, BAA!). Annual, slender, delicate, culms up to 45 cm tall, 1- to 3-noded, erect, sheaths glabrous with scarious margins. Leaf blades flat to rather conduplicate, folded, 4-11 cm X 0.6-1.5 mm, nerves abaxially glabrous or with isolated un scabrous adaxially; poses acute, 3-7 mm, hyaline. Panicles loosely tracted, 5-20 um 5 cm, with 5 to 7 verticils, kasha ascending, somewhat adpressed, scabrous to shortly pilose. Spikelets 2-flowered, erect and as- cending, purplish green or purple variegated with green; lower glume narrowly lanceolate, 3.5-6 mm l- to 3-nerved, upper glume narrowly lanceolate to lanceolate, 4—6 mm, both glumes scabrous on all the nerves, rarely only the midnerve scabrous, glabrous or abrous between the nerves, margins scarious; callus and rachilla pilose, trichomes of the callus short, not reaching the lower 1/3 of the lemma; ma membranous, m, 4-toothed, lateral teeth longer than the central, Diered awn bent and twisted in the lower half, 6-9 mm, inserted at or near the lemma base, brown or dark brown in the lower part of the lemma, pale in the terminal portion; palea hyaline, 2— 3 mm, glabrous, bi-keeled, keels scabrous; anthers 1 to 3, 1.5-2 mm, pale yellow. Caryopsis 1-1.5 mm, fusiform, brownish red. Illustration. Parodi (1949: 465). Distribution and habitat. Deschampsia berteroana is endemic to the Andean region in central Chile and adjacent Argentina; it is found in open, humid soils, tween 400 and 2800 m elevation. Although its presence has been recorded in several places in central Chile, it is considered vulnerable (Arancio et al., 2001) Discussion. Deschampsia berteroana belongs to a small group of four annual species with glumes with well-marked nerves, which also includes D. airiformis, D. looseriana, and D. danthonioides. The latter is shared with western North America, while the former are exclusive of the Andes between 30°S and 37°S. The high Andes of central Chile is a region with numerous us species and a Mediterranean-type Annals of the Missouri Botanical Garden climate, consisting of wet winters followed by hot, dry summers (Arroyo et al, 1981). These conditions mostly favor short life cycles and the ability to seed before the winter. The species form an interesting group because of the annual habit, which might have developed as an adaptation to ecological constraints. Carlo Luigi Giuseppe Bertero (1789-1831) was an Italian botanist who drowned in a shipwreck while en route from Tahiti to Valparaíso; he made collections in Chile and the Juan Fernández Islands, and most of his specimens were lost with him. Among the specimens left (found in P, S, SGO, and 70), the specimen Bertero 30 is a good example of Deschampsia oana and is therefore chosen as lectotype. imens examined. ARGENTINA. Heras, cerca de Polvaredas, 2210 m, J. A. Ambrosetti & E. Méndez 7713 (MERL); pasando Polvaredas, cerca ugar de camping, 2200 m, J. A. Ambrosetti 1202 (MERL). CHILE. Temuco, termas de Araucanía Region: Kunkel 2004 (BAA). Biobío i nario, ). Coquimbo Region: La Serena, E. Barros 1655 (CONC); ee E. Barros 9913 (BAA); Fray Jorge, G. Martinez 52495 thei & E 1167 (CONC); Curicó, Cerro Condell, E. Barros 976 ). Santiago Me Region: Santiago, s.d., R. x ge s.n. (B); Apoquindo, C. Looser 1384 (BAA); Melipilla, H. i 20285 (CONC); Quebrada de Peñalo- lén, H. Cunckel 25067 (CONC); Batuco, H. Gunckel —— (CONC), H. Gunckel 18244 (S; Lo Prado, E. Barros (BAA). R. oncagua, Jahuel, Ln Filomena, R. De Giorgio 452 (CONC); Limache, Cerro Cruz, A. Garaventa 1667 (BAA); El Sauzal, A. Garaventa 2838 (BA A). 4. Deschampsia cespitosa (L.) P. Beauv., Ess. Agrostogr. 91, 149, 160, pl. 18, fig. 3. 1812. Basionym: Aira caespitosa L., Sp. Pl.: 64. 1753, as “cespitosus.” Agrostis caespitosa (L.) Salisb., Prodr. Stirp. Chap. Allerton 25. 1796. Campella caespitosa (L.) Link, Hort. Berol. 1: 122. 1827. Avena caespitosa (L.) Kuntze, Taschen-Fl. Leip- zig 45. 1867. Podionapus caespitosus (L.) Dulac, Fl. Hautes-Pyrénées 82. 1867. Aira major Syme subsp. caespitosa (L.) Syme ex Sowerby, Engl. Bot., ed. 3b: 11: 64. 1873. TYPE: “Habitat in Europae partis cultis & fertilibus” (lectotype, ated by Clayton, in Milne-Redhead Polhill [1970: 92], LINN 85.8 not seen, photo!). 4a. Deschampsia cespitosa var. cespitosa. andina Phil., Anales Univ. Chile 43: 564. hampsia 1873. TYPE: Chile. Santiago, Valle del Yeso, Jan. 1866, R. A. Philippi s.n. (holotype, SCO PHIL-201 not SGO photo!; isotypes, BAA ex SGO!, BAA fragm. ex ex Kl BAA 869 fragm. ex B!, SGO 37213 not seen, photo!, US 556497 ex SGO PHIL-201 not seen). Perennial, densely tufted grass with extremely variable habit, culms erect, 25-100(-120) cm tall, leafy at the base, sheaths glabrous with margins membranous to scarious. Leaf blades elongated, linear, flat or conduplicate, 8-20 cm X 1.5-4(5) mm, adaxially scabrous, abaxially glabrous, with 6 to 8 prominent ribs, rough to the touch, margins often scarious; ligules obtuse to acute, 2-12 mm, membra- nous or scarious. Panicles lax, open, frequently nodding, 8-30 X 1.5-7 cm, rarely slightly contracted, peduncles glabrous or minutely scabrous. Spikelets (1)2(3)-flowered, compressed, purple with green and/ or gold (or a mix); rachilla usually with abundant iriness, callus hairs short, about 1/3 the length of the lemma; glumes usually covering the florets, lower glume lanceolate, 3—4.5 m ranous to scarious, acute, entire, 1- to 3-nerved, upper glume narrowly elliptic, 3.5-5.5 oe aes 3-nerved, midnerve abrous emma narrowly ong. 2.5-3.5 mm, ep irepl to erose-toothed, lateral teeth larger, most rarely all equal or the central larger, (1)3- to 5-nerved, membranous; awn straight or slightly curved, weak, commonly not twisted, 1.5— 5.5 mm, inserted usually at the basal or median portions of the lemma and rarely exceeding the umes, scabrous; palea hyaline, 2—3 mm, 2-keeled, keels scabrous. Anthers 1-2 mm, yellow or purple. Caryopsis 0.5-1 mm, ovoid, light brown. 2n = 26 (Albers, 1980b). Illustration. Nicora (1978: 230). Chromosome number. Distribution, habitat, and phenology. This taxon has ca. 18 subspecies in Europe and Asia (Chiapella, 2000; Chiapella & Probatova, 2003) and six in North America (Chiapella et al., in prep.), which have an extensive synonymy and are not listed here. In South America, Deschampsia cespitosa can be found in wet meadows (called “mallines” in Patagonia), bogs, and along streams and creeks in the Andes from Bolivia to Tierra del Fuego. Isolated populations can also be found in high places of southeastern Brazil, at about 1000 m elevation. Flowering occurs between Decem- ber and May. Discussion. Individual specimens of Deschampsia cespitosa from South America are similar in plant aspect, panicle, and spikelet size to those from Europe, although they are sometimes allas: Al- though no specific study has addressed the origin of the South American populations, the limited molec- ular evidence available suggests differences between populations from both hemispheres, since northern (omissis N At ea Meurs o zo eth LM a Me eto gh om eu aM MT LEE LN cU Volume 97, Number 2 2010 Chiapella & Zuloaga 151 Revision of Deschampsia, Avenella, and Vahlodea d southern accessions were joined in separate clades (Chiapella, s species is similar in aspect to D. dindi i which it differs by having awns generally included in the P se spikelets, less densely scabrous lea and a extensive g phic distribution iid slit range. While forms adjoined to D. cespitosa range from 300 to 4000 m, D. ad as is found only above 1800 m. Specimens examined. ra DR _ Dpto. Futaleufá, región del Rí rcovado, entre n y la Colonia 16 de Octubre, N. m 226 och ene Rio Senguerr, Lago Fontana, Estancia Pepita, A. Soriano 1511 (SD); Valle de Gaia € G. F. Gehrling 109 (SI); Lago Musters, . 1939, E. Feruglio s.n. (BA 34811). La Rioja: Dpto. vega del Refugio Barrancas Blancas, F. Biurrun et al. 5280 (SD. Mendoza: Dpto. San Rafael, Valle del Río — mina de azufre, W de El Sosneado, O. Boelcke et al. 10213 (SI); Dpto. San Carlos, Río Diamante, ipn 22 a Dpto. we Valle €— J. R. Figueroa 3094 (CORD); F km Leñas, camino a Valle H E rmoso, G. Seij (BA); ela Rio gel con Arroyo Malalhue, A. Án Tromen, Renee Mills 3864 (BA hito, R. A. Pérez Moreau s.n. ay 3770) i Pino Hachado, Feb. 1920, L. Hauman s.n. (BA 39287). Rio Negro: Dpto. EM pedreros del Tronador, M. J Dimitri & H. Correa na 2843 (BA); Estancia s or, e: ow . Fag, on 78632); Lago Guillelmo, 12 Feb. 1938, A. Castellanos s.n. (BA 21879); Dpto. Fica pr del Pilcañiú, camino Pilcaniyeu a Baril , E. Nicora 3768 (Sl); Río Ñirihua ont Bariloche, A. Burka 6211 pine — Mar. 1942, R. A. Pérez Mo oreau s.n. (BA 48435). San Juan: . Laguna Corani z Río — acis N. Ritter & G. Crow 2199 (ST). BRAZIL. Carneiro, 20 km N of Iratim, L. Smith et al. ee 5713 (SL US. Río Grande do Sul: Cambará do Itaimbezinho, J. F. M. Valls 2394 (SI). Santa Catarina Cacador, Río Verde, 26°45’S, roi W, L. Smith & R. Klein == di CHILE. Aisén Region: Coihaique Alto, M. Paz 7 (SGO); Pac Bids, cerca de Lago Maule, M. E Dimitri et al. 4455 (BA). Antofagasta IT Vallenar, vic. of Laguna Chica, 28°48’S, 69°52’W, I. M. Johnston I m e Maule Pr Curicó, Cordiliera ese E. Werdermann I 2 . Santiago Metro he: Sentings, Berg aipo tal bei San Cabriel, CE & G. Grandjot 3486* (BAA): Y Valk del Yeso, F. Schlegel 2590 (SGO). 4b. Deschampsia cespitosa var. pulchra (Nees & Meyen) Nicora, Darwiniana 18: 101. 1973. Basionym: Deschampsia pulchra Nees & Meyen, in Nees, Gramineae 24-25. 1841. Aira pulchra (Nees & Meyen) — Syn. Pl. Glumac. 1: 220. 1854. TYPE: Chile. Cordillera de San Fernando, ad Río e 4000 m, Feb. 1831, F. J. F. Meyen s.n. (holotype, B!; isotypes, BAA fragm. ex P!, US 865601 fragm., photo ex B!). Plants 20-150 em, panicles open. Leaf blades flat to folded, 10-30 cm; ligules acuminate, 5-10 mm Spikelets 2-flowered, glumes equal, 3.5-5.5 mm, lower glume 1-nerved, upper glume 3-nerved; lemma 2.54 mm; awn straight, 0.5-2 mm, very weak, inserted in the superior 1/3 or near the apex, often lacking in the lower floret. Distribution and habitat. Deschampsia cespitosa ar. pulchra is found in the Andes of Argentina and Chile, from San Juan Province to northern Neuquén Province, in humid mountain valleys. Discussion. This form is part of the extreme morphological variation of Deschampsia cespitosa and includes the plants rather smaller in height with uced awns inserted in the upper 1/3 of the lemma. Some plants present normal 2-flowered spikelets, while others have the upper floret extremely reduced or absent, or have muticous florets. ns examined. ARGENTINA. pae boni del Río Atuel, O. Boelcke 4172 (BAB). N Norquín, — de be asa A. L. Cabrera 6169 (BAA). Dpto. Mina e Los ln 36728'S, 70748'W, O. Boelcke et al m (BAB). - aguelito, F. Kurtz 9495" (CORD). CHILE. egion: Colchagua, Cordillera San Fernando, Río neat s. coll. (BAA). 5. Deschampsia cordillerarum Hauman, Anales Soc. Ci. ie 86: 231, 3l. pl. 4. 1918. TYPE: Argentina. Mendoza: au bord de la riviere, a Las Cuevas, Mar. 1918, M. S. Pennington 22 E BA 39306!; isotypes, BAA ex BA!, 7 ex BA not seen). Perennial, densely caespitose, culms 35-60 cm tall, 1- or 2-noded, sheaths glabrous with membranous margins. Leaf blades folded, 5.5-12 cm X 1-2 mm, acuminate, densely scabrous on the nerves on both sides, midrib not Sens: ed ligules acute, 5-11 mm, membranous, sometimes lacerate. Panicles loose, 8-13 X 2—6 cm, with 6 to 9 verticils, branches glabrous. Spikelets 2-flowered, violaceous to purplish, sometimes variegated with gold; lower glume narrowly lanceolate to lanceolate, 3—5 mm, l-nerved, upper e lanceolate, 4—5 mm, 3-nerved, scabrou both glumes with margins membranous; lemma pe mm, scarious to membranous, 4(5)- toothed, lateral teeth longer than central tooth, 4(5)- nerved, nerves glabrous; awn slightly bent and twisted in the lower half of the lemma, 5—6 mm, slender, Annals of the Missouri Botanical Garden inserted in the lower 1/3 or at the base, exceeding the glumes; palea narrow, 2-3 mm, 2-keeled, keels glabrous. Anthers 1-1.5 mm, yellowish to reddish. Caryopsis 0.3-0.8 mm, ovoid, brown. Illustration. Parodi (1949: 435). Distribution and habitat. Deschampsia cordiller- arum is restricted to the Andes of central Argentina and neighboring areas of Chile, between 32°S and 35°S latitudes, at altitudes of 1800-3300 m, where it grows by small watercourses. Discussion. Deschampsia cordillerarum is similar to D. cespitosa in plant size and aspect, but differs in its slightly longer awns that exceed the glumes (vs. awns V exceeding the glumes in D. cespitosa), the id leaves, and the darker color of the spike varying between violaceous and purplish. Darker spikelets have been also noted for high- altitude forms of D. cespitosa in Europe (Vigo i Bonada, 1983). Specimens examined. ARGENTINA. Mendoza: Dpto. Las Heras, Las Cuevas, valle del rio Las Cuevas, arroyo egion: Oval iguel, 30°50’S, 10735 W, C. Jiles 3623 (C ea Val- d Aconcagua, Laguna tro, Zöllner 46212 (CONC). 6. Deschampsia danthonioides (Trin.) Munro, Pl. Hartw. 342. 1857. Basionym: Aira danthonioides Trin., Mém. Acad. Imp. Sci. St St.-Pétersbourg, Sér. 6, Sci. Math. 1(1): 57. 1830. TYPE: “America Borealis Occidentalis,” 1829, Lindley s.n. (holo- type, LE TRIN 1873.01"). Deschampsia calycina ]. Presl, Reliq. Haenk. 1: 251. 1830. Aira calycina (J. Presl) peg , Syn. PI. Glumac. 1: 220 n montani D ae — “H anis — s. E Haenke MA hos n; isotypes, TRIN i3 or, LE TRIN 1873. "me US 865608 photo ex Monandraira glauca E. Desv., Fl. Chil. Pan 342. tab. 79, fig. 1. 1854. Deschampsia glauca (E. Desv v.) P. Darwiniana 8: 467 , non hampsia glauca Hartm., 1820. TYPE: Chile. “En lugares montañosos de la dehesa de Santiago,” s.d., C. Gay s.n. (holotype, P eq 70!; isotypes, Pt, US fugi ex P DESV 70 not seen gracilis Vasey, Bot. Gaz. 10: 224. 1885. TYPE: U.S.A. California: San Diego Co., 28 June 1884, C. R. Orcutt 1072 (holotype, PH not seen, photo!; isotypes, US rud not seen, photo!, GH not seen, photo!, MO seen Annual, slender, culms 15-35 cm tall, 1- to 2-noded, sheaths glabrous with me Leaf blades margins. flat to rather inrolled, narrowly lanceolate, 3.5—10 cm X 0.8-1.5 mm, abaxial ides ligules acute, 3.5-7 mm, scarious. Panicles open, 5-25 X 4—8 cm, rather contracted in young plants, nodding ee more — when — 6 or » watak branches LE r the ids ppal nad the distal portion. Spikelets distal; clustered toward the end of ranches; callus and rachilla pilose; lower glume narrowly lanceolate to lanceolate, 4—5 mm, 3-nerved, upper glume lanceolate, 4.5—6 mm, 3-nerved, glumes with the ma dip scarious rang the nerves evident, b n all the nerves, and nidum scaberulose been. nerves; lemma 3.5-4.5 mm, 4-toothed, lateral teeth larger than central tooth, 4-nerved, sparsely scabrous on and between nerves, scarious; awn bent, twisted, 5-8 mm, scabrous, inserted at the base of the lemma. Anthers 0.5-1 mm, pale yellow to reddish. Caryopsis 1—-1.5 mm, fusiform, brown. Illustration. Holmgren and Holmgren (1977: ) Distribution and habitat. Deschampsia dantho- nioides is an American species with a disjunct continental distribution. In western North America, it is found from Alaska to Baja California in wet or drying meadows, stream banks, or vernal pools; in h erica, it occurs in north-central Chile from 29°S to 35°S latitudes in similar habitats. This species was introduced into England and Germany with seeds of Poa pratensis L. from the United States (Conert, 1987). ussion. Deschampsia danthonioides differs Deschampsia species in the narrowly s. The species is usually infected by the rust fungus cerebrina (Ustilaginomycetes, Tille- tiales) (Castlebury et al., 2005). Spee examined. CANADA. British Columbia: od Island, near Isabelle Point S of Fulford Harbour, common in wet crevices of rock cliffs, J. A. Calder & K. T. MacKay 29623 (BM). U.S.A. California: San Gabriel Mtns., pap Flats, V. Durán 3507 (P); ME u d A. LR rd., R. F. Hoover 6789 (B ua Lake Cos A. s Beetle Me BAA). Nevada: Elko Co., Pinon Range, oothill area of Cissillini Canyon, A. Tiehm & J. Nahin 14258 pitos Utah: Farmington, M. E. Jones al N de Mantos Matthei 228 ao erm dace de Buenos Aires, sane S, 7114'W, 500 m ; beeen - e UNO: e ana Termas nes, 34^15'S, 70°34'W. lx Pío] 13102 (SL, cà Volume 97, Number 2 2010 Chiapella & Zuloaga Revision of Deschampsia, Avenella, and Vahlodea 7. Deschampsia elongata (Hook.) Munro, PI. of the River Columbia, s.d., D. Do (holotype, K!; isotypes, BAA fragm. ex K!, US 76303 fragm. ex K photo!). Aira 3 Franch., Miss. Sc rn, Bot. 5 1889 Deschumpióà xad d). Speg. Es Ad Mus. Nae Buenos Aires 5: 89. 1896. TYPE: Chile. n Bein 1877, L. pe 161 (holotype, P!; isotype 6296 fragm. ex P photo!). Aira cia var. ee Pinch, Miss. Sci. Cape Horn, . 5: 384. 1889. TYPE: Chile. Patagonie, Punta Aras. 5 "E 1879, L. Savatier 196 AM a Pt isotypes, BAA fragm. ex P!, US 76297 f. x. P photo!). Perennial, caespitose, slender, culms densely tufted, 15-80 cm tall, 1- to 4-noded, with abundant innovations, sheaths glabrous with membranous margins. Leaf blades flat to rather folded, condupli- cate, 4-12 cm X 0.5-1.5 mm, glabrous abaxially, scabrous to densely scabrous adaxially, basal leaves often filiform, forming a dense cover; ligules acute, 10 mm, scarious. Panicles contracted, spikelike, 8—30 X 0.5-2 cm, with 6 to 9 verticils, erect or slightly nodding, branches narrow, adpressed to the culm axis, sparsely scabrous. Spikelets 2-flowered; rachilla and callus pilose, with few ee hairs ca. half the length of > narrowly lanceolate, 3.5- ume had , 3.5-5 mm, both glumes 3-nerved, violaceous or rati green, shiny, scabrous on all nerves, most rarely between them, more ben scabrous in the distal portion of the ; lemma scarious, 2-3 mm, apex 4-toothed, lateral teeth larger than the central tooth; awn straight or nearly so, twisted, 2-5 mm, inserted between the middle and the base of the lemma, more often in the lower 1/3; palea hyaline, 1.5-2 mm, 2-keeled, scaberulose on the keels. Anthers 0.5-1.5 mm, reddish. Caryopsis 1-1.5 mm, fusiform, brown. Illustration. Holmgren and Holmgren (1977: Distribution and habitat. Deschampsia elongata is a species with a disjunct distribution between western North America and South America. In North America, it is found along lake shores and timberline meadows from Alaska to California, whereas in South America it is commonly found in bogs, wetlands, and along small water courses in the Patagonian Andes of Argentina and Chile, from 30°S to 50°S latitudes. Discussion. Deschampsia airiformis and D. elon- gata are similar in appearance with their contracted, narrow panicles less than 2 cm wide. Deschampsia airiformis is distinguished as a small, slender annual no higher than 15-20 cm, with panicle branches more scabrous to densely hirsute and stout awns to 8 mm long; D. elongata plants are perennial and range from cm high, with shorter awns not exceeding 5 mm, and the panicle branches are sparsely scabrous. mens examined. CANADA. British Queen Charlotte Islands, Moresby Island, Gray Bay, commoi on sandy beach in clearings of woods near mouth of creek, 1. A. Calder & R. Taylor 35255 (P). U.S.A. California: San Bernardino Co., cienaga betw. Bear Valley € Bluff Lake, L. Abrams 2833 (P); Truckee, A. S. Hitchcock 1417 (P). Idaho: Lake Waha, A. & E. Heller 3289 "€ T Bozeman, J. W. — 599 (BM). Oregon: Co., Rogue zum 4 mi. E of Gold Bea b us D a P Gas "Mts. A. Elmer 1664 (P); Cascade Mtns., valley of the Nesqually, O. D. Allen 38 (BM). MEXICO. Sierra de las Cruces, C. G. Pringle 4743 (P); Federal Distr., siint C. E mba 13244 (K). Jalisco: 15 mi. S of Autlán, ns. below El Cuartón, R. McVaugh 10323 aw eese tm 23 km SE de Capillas, F. J. Santana uzmán 3411 (US); Hidalgo, i near w Parque Nac. El Chico, H. E. Moo ARGENTI Chubut: Cushamen, Cholila, Martínez ma 3028 (SI); NC Patata, Río DW 71°W, 43°S, N. Illin 167 (CORD); región del Río Corcovado, entre El Bolsón x Colonia 16 de Octubre, N. Illin 224 . Faggi s.n. Mn 19182); Bariloche, L. R. Parodi 11425 (S). Santa Cruz Lago Argentino, 49°4’S, 72°12’W, s. coll. (SI 15053). CHILE. Aisén Region: — Barros 5867 (K); Aisen, Km 49 del camino de Puerto Aisen a Coihaique, R. Maldonado 129 ania Region: Looquisuy, "Cordillera Las Raíces, A. Burkan 9529 (SI); camino de Icalma a Liucura, en la estepa cerca de Marimenuco, cerca de la ribera de Bio Bío, A. A. Per 7383 (CONC). Antártica Pu Leña Dura, E. Barros oan ee eri Australis sd Punta Arenas, P. Dusén 549 (CORD); Río El Ganso, seno Otway, R. Barrientos 220 (CONC); Ültima Esperanza, Cueva del Sladen, A. Ricardi & O. Matthei 375 (B, doce Puerto Natales, 11 Feb. 1936, E. Jara s.n. (CONC 71822); Lago Balmaceda, A. Kalela 2022 E Sin del Fuego, Río Condor, Forestal Trillium, Río era, E. Pisano et al. 8191 (CONC). . Deschampsia kingii (Hook. f.) E. Desv., Fl. Chil. (Gay) 6: 335. 1854. Basionym: Aira kingii Hook. f., Fl. Antarct. 2: 376. tab. 135. 1846. TYPE: [Chile.] “South part of Tierra del Fuego, Strait of ore Port Famine," Jan. or Feb. k n 546 (lectotype. designated by D. M. abr [1986: 30], K!; isotype, CGE not seen, photo!). 154 Annals of the Missouri Botanical Garden Aira elatior Steud., Syn. Pl. Glumac. 1: 423. 1854 58 km south of Punta Arenas at 5836'S, 70°55'W Trisetum dozei Franch., Miss. Sci. Cape Horn, Bot. 5: 384, pl. 9 & f. a—e. 1889, = - m TYPE: Chile. Sandy Point, y. Lec 222 (holotype, P!; ae BAA fragm. ex P!, S!, ea P, photo!). Perennial, caespitose, sometimes rhizomatous, culms 25-125 cm tall, stout, erect, 1- to 3-noded, nodes glabrous, dark, sheaths striate with membranous margins, rarely scarious. Leaf blades flat to condupli- cate, blades 4-15 cm X 2-4.5 mm, acute, with scarious margins, nerves glabrous on the abaxial side, scabrous on the adaxial side to shortly pilose; ligules acuminate, 3.5-7 mm, membranous, sometimes lacerate. Panicles wide, open, pyramidal, 17-35 X 3-10 cm, with 5 to 10 verticils, branches scabrous. Spikelets 2(3)-flowered, purple to variegated with green or gold; callus and rachilla hairy, rarely glabrous; lower glume narrowly lanceolate, 4.5-9 man; ici glume lanceolate, » gl 9.5 mm. both pre = — at ani = E an or scarious; pcm irregularly db ap teeth all similar, rarely the lateral or the central tooth e awn straight, strong, and short, Peeter el, 1- mm, insert per e lemma, 2 frequently in the bw 113; palea hyaline, becomi s when larger, 2-5 mm, 2-keeled, rarely flattened and scabrous between the keels, keels scabrous to densely hirsute; anthers 1 .5-2.55 mm, reddish. Caryopsis fusiform, 1.5-2 mm, brown. Mlustration. Hooker (1847: pl. 135). Distribution, habitat, and phenology. Deschampsia kingii is abundant in the understory of Nothofagus umilio (Poepp. & Endl.) Reiche foresis ; in southern Tierra del Fuego, where it also forms patches growing in water in swamps. It becomes less frequent to the north of Patagonia, where it is gradually replaced by D. cespitosa. The northern limit of its distribution is — found at ca. 45°S. It can be found from sea evel to 600 m elevation. Flow occurs January and March. = s Discussion. Deschampsia kingii is a stout plant similar to D. cespitosa, from which it differs by the larger spikelets with stronger awns and the denser pubescence on the leaves. The stands in Tierra del Fuego represent the typical form, while the differenc- es with D. cespitosa blurred in northern populations. The type locality mentioned in the protologue (Port Famine) is the name given by the English corsair Thomas Cavendish in 1587 to the settlement Rey Don Felipe, founded on 25 January 1584 by s" pene Captain Pedro Sarmiento de Gamboa on side of the central punt cf Sd el MA s species Trin., and Geranium patagon collected in this locality, diiron was visited by many explorers, including Charles Darw imens examined. ARGENTINA. Chubut: Dpto. Tehuelches, Valle Laguna Blanca, 45 52'S, I '15'"W, 4 Koslowsky 142 (SI); Río Pico, Estancia Tromencó, A. Soriano 5368 (BAB); Río Aisen?, 1900, Cafiadón de o. Lago Buenos Aires, entre Lago Buenos Aires N y Cabo Río t. F. Kurtz 32 (CORD); us Cer Aike, Estancia Stag River, afluente W del Río meseta Lat LR sl ntino, Lago San Martin, brazo sy Mar. 1933, L. R. int s.n. (BAA). Tierra del F : Monte Olivia, M. Awschalom s.n., Herb. Parodi 9550. (K. S: cerros - T. Hunziker 8218 (C ORD); Lago Fagnano. Pete 6709 (BAB); Estancia Moat, W Bank, HD. M. 1688 (K); Ushuaia, M. S. Pennington 267 qs 1 Martiales, Feb. ee L A. Tortorelli s.n. (BAB); Tierra Mayor Valley, R. N. P. Goodall 4700 (BAB); Isla de Los Estados, Caleta Brent, A. Castellanos 12846 (BA). C —— Punt ta Are ne Brazos, F., Pastore 72 (sh Patagonia , Australis ad Punta cd P. Dusén 548 (CORD); Istmo de Ofqui, expedición “Hicken-Reichert” El 10985); Última Esperanza, puerto eo Bella Vista, 51703'S, 73 15'W, F. Roig et al. s.n. o 5472 (BAB); Lago Balmaceda, A. Kalela 2021 (S: 5 km S of T Arenas, W. J. Eyerdam et al. 24132 (S); Isla Na varino, C. Skottsberg s.n. (S); mina Loretto, Y. Mexía (K); Pestassla Taitao, des Rafael, M. Gusinde 474 (S); Isla Otaries, Surgidero Romanche, 55°37'S, 67°32’ W, E. Pisano 5089 (SI) 9. Deschampsia laxa Phil., Linnaea 29: 92. 1858. TYPE: Chile. Chonos, en las playas de Guayte- cas, R. Fonck 53 (holotype, SGO PHIL 199 not seen; isotypes, BAA ex SGO!, K photo ex SGO!, US 556490 fragm. ex SGO not seen). is hirthii Phil., Anales Univ. Chile 94: 22. 1896. TYPE: Chile. “In ami fluminis mec Jan. 1885, A Hirth s. € SGO PHIL 133 not seen; isoty BAA fragm. ex SGO!, SI photo ex SGO!, US 1939357 x SGO seen). Perennial, delicate, culms 50-90 cm tall, 1- to 4- noded, sheaths glabrous with margins membranous to scarious. Leaf blades linear, conduplicate, 6-12 em X 1-4 mm, nerves glabrous on the abaxial side, rarely scabrous, on the adaxial side scabrous; ligules truncate, 4—10 mm, scarious, when larger membra- nous, basally dilated and prolonged on both sides of the leaf blade. Panicles loose, open, 15-25 x 3- 15 em, with 6 to 11 verticils, panicle branches up to 12 em, grouped in the base of the panicles forming edd of 3 to 5 branches, base slightly swollen. Spikelets 2-flowered, green to whitish, (Ortiz-Troncoso, 1976). Type specimens of several Poa scaberula Hook. . O. Boelcke et T TBPA 328 3284 (BAB; 3 i. eto dr M sun ci A d Volume 97, Number 2 2010 Chiapella & Zuloaga Revision of Deschampsia, Avenella, and Vahlodea sometimes variegated with gold; callus and rachilla hairy, hairiness less dense toward the distal end; glumes linear-lanceolate, lower glume 3.5-8 mm, I-nerved, scarious on margins and toward the apex, upper glume 4—9 mm, "iet normally only the midnerve kakuq margins membranous; lemma 2— 4 mm, membranous, 4(5)-toothed, lateral teeth slightly larger (rarely smaller) than the central tooth, 4(5 or 6)- nerved, the nerves glabrous or sparsely scabrous in the distal portion; awn slightly bent, somewhat twisted in the base of the lemma, 3—7 mm, inserted adaxially in the lower to middle 1/3 of die lemma; palea 2-keeled or rarely rounded, 2-3 mm, hyaline to membranous, keels scabrous. Anthers 1.5-2 mm, ish. Caryopsis narrowly fusiform, 1-1.5 mm, brown to reddish. Illustration. Nicora (1978: 230). Distribution. Deschampsia laxa occurs in the uthern Andes of Argentina and Chile, from 43°S (Rio Palena) to Tierra del Fuego; it occupies roughly the same areas as D. kingii, although it is much less abundant than that species. Deschampsia laxa differs from D. are glabrous on the adaxial side; the ligules, which are truncate and prolonged into the sides of the leaf blade; the smaller spikelets; and the point of insertion of the awns into the lemmas (nearly basal in D. laxa vs. inserted in the middle of the lemma in D. kin, are also Discussion. kingii in the leaves, whic ii). The branches of the panicle flexuous and curved; otherwise, the two species are similar in aspect, and the identity of D. laxa has yet to be confirmed with more collections and molecular studies. Specimens examined. ARGENTINA. Chubut: Cushamen, Lake, UR A. E: = 586 (SD; Dpto. E Parque Lago éndez, ez Moreau s.n. BA Daa Eu A. Soriano 3493 Patagonia," s. loc., A. Bonarelli 78, Plantae baie (SI). CHILE. Magallanes and Antár- tica Chilena Region: Última Es; speranza, Puerto Bella Vista, 51°30’S, 73^15'W, F. Roig et al. TBPA 5103 (BAB); Isla Hoste, caleta Awaiakirrh, E. Pisano 5474 (SI) 10. Deschampsia looseriana Parodi, Darwiniana 8: 460. 1949. TYPE: Chile. Santiago, Batuco, 500 m, 17 Sep. 1936, G. Looser 3439 (holotype, BAA). Deschampsia looseriana var. triandra Parodi, Darwiniana 8: 464. 1949. TYPE: Chile. a Batuco, 26 Sep. 1931, G. Looser 2049 (holotype, BAA!). Annual, delicate, slender, culms 15—40 cm tall, 2- to 3-noded, branched from the base, sheaths striate, glabrous, with margins membranous or less commonly scarious. Leaf blades flat or folded, 2.5-1 1 cm X 0.5- 1.5 mm, nerves glabrous and somewhat papillate on the abaxial side, — on the adaxial side; ligules acuminate, 3—7 mm, membranous. Panicles open to slightly neh ds 4-12 X 1-4 cm, erect or nodding, with 4 to 7 verticils, lower branches adpressed and grouped in clusters of (2)3, moderately to densely c Spikelets 2-flowered, pedicels scabrous; rachilla and callus of florets with white hairiness; glumes narrowly lanceolate, lower glume 5.5-7 mm, upper glume 6-7.5 mm, both 3-nerved, commonly with only the midnerve scabrous, with margins hyaline and lateral nerves vanishing toward the apex; lemma contracted in the upper half, 4-6 mm, minutely lateral nerves, central teeth minute, rudimentary; awn bent, twisted in the lower half, 7-10 mm, inserted in the middle of the lemma; palea 2-keeled, hyaline, scaberulose on the keels. Anthers 1 to 3, 0.5-2 mm, pale yellow. Caryopsis 0.5-1.5 mm, ovoidal to fusiform, brown to reddish. Illustration. Parodi (1949: 462). Distribution, habitat, and phenology. Deschamp found in central — ae 6. It grows n 300 and 1200 m elevation. Flowering occurs Mon Septem- ber and November. so and Curicó Discussion. Deschampsia looseriana and the other annuals of central Chile and adjacent regions of Argentina (D. berteroana and D. danthonioides) are poorly known species that have been evaluated as vulnerable aoe et al., 2001). Deschampsia looser- iana var. tri as established by Parodi (1949) based on the presence of flowers with three stamens, differing from the typical form with commonly one or two stamens. Modifi nationes in stamen number, anther size, and other rep in lodicule and awn size, filament EM are typical features of cleistogamy (Campbell et al., 1983) and therefore are not considered as valid for separating a variety. Careful examination of the type of variety triandra (G. Looser 2049, BAA) shows the existence of flowers with one stamen with very reduced anthers, a fact already noted by Parodi (1949: 464). uctions Specimens examined. CHILE. Biobío Region: Concep- ción, E. Barros 11 (CONC). Coquimbo Region: Coqu imb, Combarbalá, Cuesta de Punitaqui, C. Dee | € 0. Matthei 387 (CONC). Maule Region: € E. Barros 1637 (CONC); Constitución, Los Molinos, A. Barnier 232 (CONC). Santiago Metropolitan nes Batuco, Montero 2366 (BAA); Batuco, G. Looser 3438 (CONC); ta Reina, E. Navas 8123 (CONC); Quebrada de Peñalolén, Y. Bravo 23 (CONC); Maipá, Cerro El Águila, 32^54'66'S, 88'14"W, A. Tomé s.n. (CORD 1133). Valparaíso Annals of the Missouri Botanical Garden Region: Valparaíso, Marga Marga, A. Laffuel & B. Pirión 1838 (BAA); La Rinconada, U. Levi 2674 (CONC); Limache, Pangal, G. Looser 3718 (BAA). 11. Deschampsia mendocina Parodi, Darwiniana 8: 447. 1949. TYPE: Argentina. Mendoza: Sierra de la Medialuna, valle, 1700 m, 15 Feb. 1922, C. Rigal s.n. (holotype, BAA 4685!). Perennial, rhizomatous, culms erect, slightly bent at the base, 20-25 cm tall, 2- to 3-noded, sheaths glabrous with margins scarious. Leaf blades folded, conduplicate, 6-8 cm X 0.5-1 mm, nerves glabrous on the abaxial side, scabrous on the adaxial side, prickles and very short hairs mostly on the nerves; ligules acute, 4-6 mm, scarious. Panicles slightly contracted, subspiciform, 67.5 X 1-1.5 cm, pedun- cles scabrous, short. Spikelets 2- to 3-flowered, purplish, callus densely pubescent, trichomes white, reaching the top of the florets, rachilla pilose; lower glume 3.5-3.8 mm, I-nerved, upper glume 3.5-4 mm, 3-nerved, both glumes with nerves glabrous and margins membranous, sometimes the middle nerve with isolated prickles; lemma 4-toothed, teeth similar or the central tooth slightly longer, 2-3 mm, 4- to S-nerved, nerves glabrous; awn straight, not twisted, 1.5-3 mm, scabrous, inserted in the lower half or at the base of the lemma, not exceeding the glumes; palea 2-keeled, 2-3 mm, keels scabrous, hyaline. Anthers 0.5-1 mm, reddish orange. Caryopsis not seen Hlustration. — Parodi (1949: 448-449). is a rare species known only from the type in the Andes of central Argentina. Discussion. |! on. Deschampsia ina is similar to D. cespitosa, but differs by its more c aspect (culms only to 25 cm vs. to 100(120) cm in D. cespitosa), its smaller and more contracted panicles {only to 7.5 em vs. lax, open panicles up to 30 em in D. cespitosa), and by the presence of rhizomes (vs. issa). Chil. (Gay) 6: 339. 1854. Basionym: Aira Hook. f. Fl. Antaret. 2: 377. 1846. Trisetum parvulum (Hook. f.) Speg., Anales Mus. Nac. Hist. Deschampsia 12. Deschampsia parvula (Hook. f.) E. Desv., FI. parvula Nat. Buenos Aires 5: 89. 1896. parvula (Hook. f.) Macloskie, Rep. Princeton Univ. p. Patagonia, Botany, Volume viii 1 [2]. Botany 8(1,5,1): 202-203. 1904, nom. illeg. TYPE: Chile. Cape Horn, Hermitte Island, J. D. Hooker 12 (holotype, K!; isotype, BAA fragm. ex K!). x Densely caespitose perennial, culms 5-25 cm tall, - 1-noded, sheaths glabrous, widened at the base, with ` S or scarious margins. Leaf blades linear to | filiform, abundant, forming dense clumps, blades 1.5- 6 cm X 0.5-1 mm, nerves glabrous on the abaxial side, sparsely scabrous on the adaxial side; ligules - slightly exserted, 3-7 X 1-2 cm, with 4 to 9 verticils, b h lly ad d to th l axis, densely scabrous. Spikelets 2(3)-flowered, erect, violaceous, often variegated with gold or green; callus and rachilla pilose, trichomes short and scarce; lower glume * narrowly lanceolate to lanceolate, 3—7 mm, 1-nerved, upper glume 3.5-7.5 mm, 3-nerved, both glumes glabrous, normally scabrous only along the midnerve in the distal portion, with margins membranous or scarious; lemma 4-toothed, lateral teeth acute, larger than the central tooth, (3)4(5)-nerved, nerves gla- brous; awns stout, exserted, strongly bent or curved, 3—6.5 mm, twisted in the lower half, inserted in the lower 1/3 of the lemma; palea hyaline, 2-3 mm, bi- keeled, scabrous along the keels. Anthers 0.5-1 mm, reddish to pale orange. Caryopsis 0.5—1 mm, fusiform. Illustration. Nicora (1978: 234). Distribution, habitat, and phenology. | Deschampsia parvula ranges from the Andes of southern Argentina and Chile, from Lago Argentino to Tierra del Fuego, occurring in wet bogs to rocky soils from sea level to 1800 m. Flowering occurs in January and February. Discussion. The contracted panicles of Deschamp- sia parvula are similar to the inflorescences of Trisetum, but the species clearly differs from the latter genus by the 4-toothed lemmas. ia parvula is similar to D. patula in the small plant size and the short leaves, but it differs from D. patula in its panicles, which are more contracted and with the branches close to the axis. ARGENTINA, Ambrosetti & E. Mendez, TBPA oreno, F. Reichert et al. : Castellanos 12831 (BA); Basket Island, k , CHILE. and Antártica Chilena Region: Ultima Esperanza, Península Roca, Seno Resi, TBPA 2916 (SI); Punta Arenas, O. Zollner 9623 (CONC); Tierra del Fuego, Sector Vicuña, Forestal | | Volume 97, Number 2 2010 Chiapella & Zuloaga 157 Revision of Deschampsia, Avenella, and Vahlodea Trillium, E. Pisano et Mo 7577 (CONC); Parque Nac. Torres del Paine, Cerro Agudo, M. T .K. Arroyo & F. Squeo 87-0007 (CONC) 13. Deschampsia patula (Phil.) Pilg. ex Skottsb., Kongl. Svenska Vetensk. Acad. Handl. 56: 175 1916. Basionym: Monandra ee. Phil. Anales Univ. Chile 43: 565. 1873. Deschampsia elegantula var. patula (Phil.) Parodi, Darwiniana 8: 454. 1949. TYPE: Chile. Magallanes, Punta Arenas, 1869, s. coll. (holotype, SGO-PHIL 244 not seen, photo!; isotypes, SGO 37214 photo!, US 867651 fragm. ex SGO not seen, K photo ex SGO!) Perennial, caespitose, erect, culms 8-20 cm tall, 4- to 6-noded, sheaths glabrous with membranous margins. Leaf blades folded, 1.5-3.5 cm X 0.5- .5 mm, abaxial side sparse to densely scabrous, prickles mainly on nerves, on the adaxial side prickles less abundant; ligules acute, sometimes lacerate, 2— 5 mm, scarious. Panicles open to contracted, 2.5— 6(10) X 2-6 cm, with 4 to 6 verticils, branches moderately to densely scabrous. Spikelets 2-flowered, purple to gold, sometimes variegated with green; lower glume lanceolate, rarely narrowly lanceolate, 2.5— 6 mm, 1(3)-nerved, upper glume lanceolate, 2.5—7 mm, 1(3)-nerved, both glumes scabrous along the midnerve with margins scarious; callus pilose, hairs reaching the middle of the lemma, sometimes few hairs exceeding the middle; lemma 2-4 mm, 4-toothed, lateral teeth larger, rarely all similar, 1- to 4-nerved, nerves glabrous; awns weak, bent and normally twisted and not exceeding the glumes, inserted in the middle or lower 1/3 of the lemma, 1. mm, palea 2-keeled or flattened, 1.5—4 mm, 1 mm. dark reddish to violaceous. Caryopsis 0.5—1 mm, ovoid. Illustration. Nicora (1978: 234). Distribution and habitat. found in the Andes of Argentina and Chile, from Santiago to Tierra del Fuego and also in the southern Patagonian steppe, primarily in wet bogs. It is found ween 900 and 1500 m elevation. Deschampsia patula is Discussion. Deschampsia patula is similar to D. antarctica, Írom which it differs mainly by its shorter, twisted awns, the awns not exceeding the glumes, the more contracted panicles, and the longer hairs of the callus. The existence of intermediate individuals between both taxa was noted by Parodi (1949), who described D. elegantula var. patula, probably trying to accommodate individuals of D. elegantula (= D antarctica) approaching D. pat Specimens examined. ARGENTINA. Chubut: Dpto. Río Senguerr, Laguna Blanca, C. Burmeister s.n. (SI 15043); Dpto. Río Senguerr, El Coyte, con Festuca argentina o F. pallesc ens, R. León 2400 (BAA). Santa Cruz: Dpto. Güer Aike, Laguna Cóndor, O. Boelcke 12446 (BAB); RN 3, 10 km W de Río E a orillas del río Gallegos, O. Boelcke 12358 (BAB); sección San Antonio, 51°24’S, ore. W, F. Roig et al. 77 SD. diss del Pope Dpto. Río Grande, bastián, Estancia José Menéndez, Se Vallerini 3900 RP); Río Grande, Estancia M. Behety, M. Collantes 2107 a Ora nge Harbor, U.S. South Pacific bales Expedi- ber US 867656 (US). ona Magallanes and kates artica ci e Ultima qu on Sierra de los Baguales, ucía, 50 50%44'S, 7 20'W, M. T. K. Arroyo 85- iS cones Isla seri Caleta Lientur, 55°44’S, 67°19'W, E. Pisano 5123 (SI). 14. Deschampsia setacea em ) Hack., Cat. Rais. Gramin. Portugal 33. . Basionym: Aira setacea Huds., Fl. Angl. secat 30. 1762. Aira montana var. setacea (Huds.) Huds., Fl. Angl., ed. 2: 35. 1718. Aristavena setacea (Huds.) F. Albers & Butzin, Willdenowia 8: 83. 1977. TYPE: United Kingdom. Litcham Common, 18 July 1883, F. J. Hanbury s.n. (neotype, designated by Chiapella [2009: 242], BM not seen, photo!). Perennial, caespitose, with vegetative shoots densely packed, erect, culms 12-45 cm tall, 2- to 3-noded, Leaf cim ths glabrous with membran blades festis blades a cm X 1-1.5 mm, inrolled, sharply pointed, glabrous to sparsely scabrous on the abaxial side, margin of blade scabrous, with abundant prickles, adaxial side scabrous, prickles more abundant on nerves; ligules narrowly lanceolate, 4.5-11 mm, hyaline, acuminate. Panicles loose, — 8-18 X 1.5-5 cm, with 5 to 7 verticils, s gl s to scaberulose, lower branches Fe branches sparsely scabrous, brown to purplish, darker toward the tips. Spikelets 2-flowered, purplish, often clustered at the end of branches; lower glume narrowly lanceolate, (3—)4—5 mm, l-nerved, upper glumes lanceolate (3.5—)4.5-6 mm, 3-nerved, both glumes membranous, glabrous to sparsely sca- brous in the nerves; dlls pilose, hairs short, A ^ the ese lemma td mm, paver teral | mm, nad in the inferior 1/3 or at the bise; leoni in the abaxial half, purple in the adaxial half, scabrous; actin narrow, 2-keeled, 2.5-3.5 mm, keels rough, hyaline. Anthers 1-1.5 mm, pale orange to reddish. s 0.5-1 mm, fusiform, brown. Illustration. Parodi (1949: 446). Chromosome number. 2n = 14 (Hubbard, 1984). Distribution, habitat, and ae. ee setacea is known from and wet pla in western Europe, from bino to the Iberian Annals of the Missouri Botanical Garden Peninsula. In South America, it is found in central Chile in similar habitats; it has also been cited for southern Chile (Parodi, 1949), but no material from this region has been found. It grows between 900 and 3500 m elevation. Flowering occurs in January and February. Discussion. Deschampsia setacea is similar to Avenella flexuosa in the bristlelike leaves, but the two differ in the longer and pointed ligules of D. setacea (vs. obtuse in Avenella) and in the more purple-colored spikelets of A. flexuosa. Specimens examined. CHILE. Coquimbo Region: Ovalle, Quebrada Larga, C. Jiles 4143 (CONC); Illapel, Río Ojotas, J. Morrison & R. W. knecht 17424 (BAA, SI). Santiago : Las Condes, cordillera al oriente de Santiago, Mina isputada, G. Looser 1111 (BAA, CONC); A. Garaventa 544 (BAA); Cordillera de las Arañas, Jan. 1861, G. Land s.n. (SGO 045880). 15. Deschampsia venustula Parodi, Darwiniana 8: 450. 1949. TYPE: Chile. Cordillera de Santiago, Valle Largo, Feb. 1892, F. Philippi s.n. (holo- type, SCO not seen; isotypes, BAA ex SGO!, US ex SGO not seen, photo!). Perennial, caespitose, densely tufted, erect, culms 5-27 cm tall, 1-noded, sheaths glabrous, with membranous margins. Leaf blades setaceous, ]— 45 cm X 0.5-1 mm, nerves on both sides usually glabrous, sometimes with prickles on the adaxial side; ligules acute, 3-7 mm, scarious, margins of the ligule prolonged into the upper part of the sheaths. Panicles slightly contracted, 3-14 X 1.54.5 em, with 5 to 7 verticils, branches scabrous, purplish. Spikelets 2-flowered, erect; callus and rachilla pilose, callus trichomes short, barely reaching the middle of the lemma; lower gl ly | late to lanceolate, 3-4 mm, l-nerved, upper glume lanceolate, 3.5- 4.5 mm, obscurely 3-nerved, both glumes normally scabrous and purplish only along the keels, pale gold toward the margins, scarious; lemma 4-toothed, lateral teeth larger than the central tooth, 2.5-3 mm, 4(5)- * r r - Anthers 0.5-1 mm, brownish red. Caryopsis 0.5-1 mm, fusiform. lllustration. — Nicora (1978: 234). venustula occurs in the Andes of Argentina and Chile. from 32°S to ca. 38°S, in humid and open places at altitudes between 200 and 3300 m. Flowering occurs between January and March. Discussion. Deschampsia venustula and D. patula are similar in having glumes that are violaceous along the keels and hyaline or light green toward the margins. Deschampsia venustula differs from D. patula in its longer, slightly more contracted panicles (up to | 14 X 4.5 cm vs. wider, less contracted panicles up to ` 10 X 6 cm in D. patula) and in the awns, which exceed the glumes in D. venustula and are includedin D. patula. Specimens examined. ARGENTINA. Mendoza: . San Carlos, Cordillera del Portillo de La Llareta (entre El Paso del Portillo y la Laguna del Diamante), F. Kurtz 10991 (CORD [sheets A, B]; Laguna Diamante, G. Covas 1047 (BAB, SI, US); próximo a la laguna, O. Boelcke 4122 (BAA, BAB); J. Hueck 18191 (SI). Neuquén: Dpto. Chos Malal, cajón del Arroyo del Cruce, 36^43'S, 70723'W, O. Boelcke et al. 11272 (BAB). CHILE. Santiago Metropolitan Region: tiago, Estero del Plomo, La Disputada, 33°07’S, 70°21' W, M. T. K. Arroyo 83-1340 (CONC). COoNCLUSIONS Deschampsia in South America comprises 15 species, some of which show a high degree of morphological similarity, requiring additional studies to clarify their true relationships. In all cases, the species can be recognized, but the existence of specific status (i.e., some taxa reduced to subspecies or varieties). Groups of species with difficult circum- scription are: D. kingii and D. laxa; D. antarctica, D. parvula, D. patula, and D. venustula; and D. cespitosa, D. cordillerarum, and D. mendocina. Two monotypic genera formerly included in Deschampsia are also found in the region: Avenella flexuosa and Vahlodea atropurpurea. The placement of Deschampsia is conflictive because molecular-based analyses (Soreng & Davis, 2000; Quintanar et al., 2007; Davis & Soreng, 2007; Soreng et al., 2007) did not support its placement inside the “true” Aveneae, but in a closely related clade called “former Aveneae lineages related to the traditional Poeae” (Quintanar et al., 2007: 1563). The fact that molecular results often collide with tradi- tional morphological classifications is well known emai 2006; Middleton, 2006). The differing data nu xdi P c. ] 1 1 Eoi I g suggest two possible placements for Deschampsia: (1) including Deschampsia in the traditional Aveneae, based on morphological data, or (2) including them in the Poeae, on ular data. A classificatory system that reconciles morphological and molecular data is still lacking, but at this point it seems that the inclusion of ia and allies in the Aveneae as ee MESE ORE Yr artis P CNE RUT BERES T MERE AER TIERE ERE RU T II ERIT CS PII RENI PETENTE PIT EOS RD GUN O O O AS Volume 97, Number 2 Chiapella & Zuloaga Revision of Deschampsia, Avenella, and h M. defined is no longer possible. The more ropriate placement—at the moment—is tribe Pasar subtribe Airinae Fr., as advocated by Soreng et al. (2007). Concerning the of Deschampsia, Raven and Axelrod (1974) id " Gtebhins (1975) suggested a northern origin for all the pooid tribes (including the Aveneae s.l. and former Aveneae). Kawano (1963, 1966) hypothesized on the basis of cytological data the most common species (D. cespitosa) might have covered the area of Pleistocene glaciation in the Northern Hemisphere almost completely, and tions into the glaciated lands m several times. Long-distance dispersal events have probably been involved in the nant of ancestors to the south, where a center of secondary differen- A (Tateoka, 1962; Hartley - 1913) developed as a result of the existence of temperate climatic m similar to those of the north. The limited molecular data available (Chiapella, 2007) suggest that althou mpsia is monophyletic, some differences exist D northern and southern populations of the widespread D. cespitosa. Based on biogeographical evidence, Hartley (1973) found the Aveneae s.l. to be more diverse and abundant in the Northern Hemisphere, but, based on the present distribution of the species, Deschampsia has flour- ished in the Southern Hemisphere, where it has developed an important center of diversity in South America. EXCLUDED OR UNCERTAIN TAXA Deschampsia brasiliensis (Louis-Marie) YValansia, ps Arge ionym: Trise nt. Agron. 8: 128. 1941. brasiliense Louis-Mari arie, Rhodora 30: 242. 1928 [1929] tufts in peaty soils among rocks, ve ti rline, 1 Jan. 1925, 2200-2400 m, ab Chase pa IM US ragm. ex US!, MO 924156 not seen, photo!). The fragment conserved at BAA presents isolated spikelets, mostly 1-flowered, with the florets with stout awns that are not typical of Deschampsia. It is not possible to clearly observe the lemmas with the 4-toothed apex, which is one of the few extremely constant characters in the genus. The species was excluded from Trisetum (Finot et al., 2005: 535), so its generic placement remains unclear. Deschampsia 2 (Pilg.) Valencia, Revista Argent. Agron. 1941. Basionym: Trisetum confertum Pilg., e kik Syst. 25(5): 714. T a ps a Finot, Ta ns Natl. H. or. bell y dd e ca cari EN m, 1 Feb. 1871, A. Stiibel 152 (holotype, B not seen, photo!; isotype, US 81771 not seen, photo!). This taxon is excluded from Deschampsia because of the lemmas, which are awnless or awned with bilobed apex, in opposition to Deschampsia, which has awned lemmas with 4-toothed apex. The plant has inflorescences in narrow, contracted panicles as described for Peyritschia E. Fourn. by Finot et al. (2004). The specimen cited by Jorgensen and Ulloa Ulloa (1994), E. Asplund 6976 (S!), collected in Pichincha, Ecuador, agrees well with Peyritschia. e O Phil., Linnaea 29: 91. 1858, nom. illeg. E: Chile. Andes de Linares, s.d., Germain 197 lae SGO PHIL 197 not seen, SGO photo!; isotypes, BAA fragm. ex SGO PHIL 197. US 556494 fragm. ex sees PHIL 197 not seen, photo!). e fragment conserved in BAA consists of a few spikelets with glumes ca. 7 mm long, and the lemmas ave no awn or teeth. The leaf blades are ca. 10 mm wide, while leaf blades are usually no more than 5 mm wide in South American Deschampsia. = a get Phil, Anales Univ. Chile 94: 24. : Chile. Coquimbo, Entrada de Tilito, 7 e a - MP s.n. oat y = 37497 not seen, photo!; isotypes, SGO 6 not seen, photo!, SGO 63067 not seen, ae is n fragm ex SGO not seen, photo!). The specimen conserved in BAA is a complete plant, ca. 42 cm high, with a basal compact tuft of "wi goin almost filiform leaf pem no longer than anicle ca. 5 em, and Pasai das. The lemmas are similar to Deschampsia, but are erose at the apex rather than 4-toothed. The ligular zone presents triangle-shaped thickenings similar to the lateral pulvini described by Rúgolo (1986) for Deyeuxia Clarion ex P. Beauv. Literature Cited Albers, F. 1972a. Cytotaxonomie und B-Chromosomen bei ampsia caespitosa (L.) P.B. und verwandten Arten. Beitr. on Pflanzen 48: 1-62. 972b. Cytosystematische M S in der Il. Die En Vahlodea Fr. und m i E Deutsch. B 79-285. 1978. Karyologische und genomatische Veründer n Aristaveninae iod 97. 9808, Systematik, variation nid Entwicklungsten- ddnde r Subtriben Aristaveninae und Airinae (Gra- mineae—Aveneae). Poio (Horn) 20: 95-116. 1980b. Vergleichende I rüser- Suberibén pon » EM wie sd mie suec aint eal der Grüser-Subtriben dicen has Airinae iam Flora 1 150-167. Annals of the Missouri Botanical Garden ——— € F. Butzin. 1977. Taxonomie und klatur der Subtriben Aristaveninae und Airinae (Gramineae—Ave- neae). Willdenowia 8: 81-84. Arancio, G., M. Muñoz & F. A. Squeo. 2001. Descripcién de Arroyo, M. T. K, sh J. Armesto & C. Villapan. 1981. Plant erns in the High Andean Cordillera of central . "a Ecol. 69: ———, M. Marticorena, 0. Matthei, M. Muñoz & P. Pliscoff. 2002. Analysis of the contributi t flora (Metropolitan and x regions of Chile). korita Chil. Hist. Nat. 75: 792. 767- Beetle, A. A. 1987. Las Gramíneas de México, Vol. 2. Secretaría de Agricultura y Recursos Hidráulicos, Comi- i ico Consultiva de Coeficientes de Agostadero (comcooy, México D.F. Bor, N. L. 1970. Gramineae. In K. E e Saee i Hoc Umrahmend: Gebirge, Persien, Afghanistan, e von hee Pia raq, Azerbaidjan, — Akademische Druck- und Verlagsanstalt, Graz. Brummit, R. K. 2006. a VIE Buschmann, A. 1949. Zwei für -Arten. Phyton (Horn) 1: 190-193, Campbell, C. S., J. A. Quinn, G. P. Cheplick & T. J. Bell. 1983 963. Cleistoguny in n grasses. Ann. Rev. Ecol. Syst. 14: 411-441. — L. A, L Carris € K. Vánky. 2005. Phylogenetic analysis E Tilletia and Sore genera in = Tilletiales (Usti cetes; Exobasidiomyceti- ae) based on large subunit nuclear rDNA . "tdeo 97: 888-900. C man, T. F. 1906, Manual of the New Zealand Fl John Ma Mackay; RE t PA J. 2000. ks nns ml cespitosa CRM in rope: A morphological anal ha J. Linn. Soe. mee 495.512. — 2007. A molecular ph a Aira oo Hudson Ped Watsonia 27. m va. 2003. Deschampsia complex (Poaceae: Avene) = special reference to Russia. Bot. J. Li nn. Soc. 142: 213-228. Clarke, G. C. S. 1980. beai 225-: Tutin, V. H. Heywood, N. A. E eae (part 1 IU. R. M. Polhill "n a. Crown Agents for Ov Sia ions, London. A. Renvoize. 1986. Grami Bull. Addit. $e. XIII. Genera Granimum. Key CR H. J. - Deschampsia. Pp. 302-317 ¿n Gustav cA Hisoniede Flora von Mitteleuropa, Band 1 s 3. Parey Buchverlag, Berlin. x e A. 1961. — de las semillas en fanerógamas crec Cabo Primavera (costa de Danco), ` Península earum Contr. Inst. Antarc. Argent. 65: ` -16. indue J. 1983. Species concept and speciation analysis. | Curr. Ornithol. 1: 159-187. — eae A. H. Holmgren, N. H. Holmgren, J. L. Ree 4 P. K. Holmgren. 1977. Intermountain Flora, 2 PA University Press, New York. Davis, J. I. & R. J. Soreng. 2007. A preliminary phylogenetic analysis of the grass subfamily Pooideae (Poaceae), with attention to structural features of the plastid and nuclear ` genomes, including an intron loss in GBSSI. Aliso 23: 335-348. Davidse, G. 1994. Deschampsia. Pp. 888-999 in G. Davidse, . Sousa S. & A. O. Chater (editors), Flora Mond Vol. 6: Alismataceae a K Universidad Nacional ; Missouri Botanical Du Rietz, G. 1930. The bd. units of biological taxonomy. Svensk. Bot. Tidskr. 24: 333-428. P Die pedem der Magellanslánder: Ostkiiste von ri Noni Exped. Magelansándema 3 3: 77-264. Finot, V. L., P. M. Pete . Soreng & F. O. Zuloaga. . A revision of Triserum m, PFeyisselin, n nd Sphenopho- lis (Poaceae: S nd in Mexico and Central America. Ann. Misso =0. a R. J. Seen: & O. Matthei. 2005, A revision of Trisetum (Poaceae: Pooideae Aveni- nae) in South America. Ann. Missouri Bot. Gard. 533-568. Frey, L. 1999. Avenella —A genus of Aveneae (Poaceae) worthy of recognition. Fragm. Florist. Geobot. 7(Suppl.): 27-32. Garcia-Suarez, R nso-Blanco, M. C. Fernandez- n J. A. ess Pray A. Roca $ R. Giraldez. jj et id from karyotypes, protein Ped sis, total genomic DNA vin and chloroplast DNA analysis. Pl. Syst. Evol. 205: 99— H araldsen, K. B., M. Odegaard & I. Ad — Variation in the amphi-Atlantic plant Vahlodea opurpurea (Poaceae). J. Biogeogr. 18: 311-320. Hartley, W. 1 ies on the origin, evolution. , and distribution of the cll V. The subfamily Festu- coideae. Aust. J. Bot. 21: 201-234. Hauman, L. 1918. La végétation des Hautes € de ifornia. University of amer Press, Berk Hitchcock, C. L, A. Cronquist, M. T 1 1969. Nona Pan : Un d Northwest Part 1: Vascular cC s and cotyledons. University of Was kaa ko Press. Sem tle. patna a R.L i AM R. L L. Smith & R. J. Abbott. rgrass (Deschampsia uc show D y domin cas An Arctic Alpine Res. 35: 229-235. Holmgren, A. H. & N. H. A Fon eae. In A H. Holmgren, J. L. Reveal Pue sea Flora, Vol. 6. ripe ew Yak o Garden, Bronx tse TOME A PIRE T ERO EE EHE ERE SURE ERO URN POESIE HET XE I EE IRR Be ERD OMe ETN SEINE ESE TN Pee ae aN a o A an a a alae Ao Volume 97, Number 2 2010 Chiapella & Zuloaga 161 Revision of Deschampsia, Avenella, and Vahlodea Hooker, J. D. 1847. The Botany of the I! me of i n the Y Identification, he and Distribution in ~ c" Isles, sed by J. C. E. Hubbard. n Books, Harm Hultén, E. 1941. Flora of Alaska and Yukon. C. W. Gleerup, Lund. ———— . Flora of n A MM Territories. Stanford pei Press, Jørgensen, P. M. & C. Ulloa Ulloa. e Seed Plants of the High Andes of Ada A Checklist. Aalborg University evolution of the . 1966. Biosystematic studies of the Deschampsia complex with special reference to the karyology of Icelandic EN p Mag. (Tokyo) 79: 293-307. Linnaeus, C y i tarum. Holmiae, Stockholm. Maclos 904. Reports of the ee p co to Patagonia 1896-1899. 8: 38. The University, Pri rinceton. McNeill, J., e, H. M. Burdet, V. Demoulin, D. L. Hawksworth, K Marhold. D. H. Nicolson, J. Prad Silva, J. E. Skog, J. H. Wiersema & Turland (editors). IL MEM Code of E Nomenclature (Vienna Code). Regnum Veg. 1 Middleton, D. J. 2006 NU be EM: notes on N. J. Asian pocynaceae, solos Rauvolfioideae and Apocynoi- deae. Taxon 55: poen "m ks . € 0. 1. Typification of Nordic ascular plant E Nase published by G. Wahlenberg. Nordic J. Bot. 11: 287-299. Nicora, E. 1978. Poaceae. Pp. 2 a A Patapóniea, Vol. e ae ehe de Tecnología "qp Buenos Aires. Nixon, E Ca . D. Wheeler. 1990. An que p of the oo species concept. Cladistics 6: — coso, O. R. E Tode cni in the E of Mapa, South America. Int. J. Naut. Archaeol. 5 179. Palisot de Beauvois, x T F. J. 1812. Essai d'une nouvelle Agros ograpl ie; ou nouveau genres a raminées; avec figures représentant les 1 res. Paris V (V). Parodi, L. R. 1949. Las gramíneas sudamericanas del género Deschampsia. Darwiniana 8: 415—475. Philippi, R. A. 1858. Plantarum novarum Chilensium V. Linnaea 29: 48—95. 1864. Plantarum Novarum Chilensiam Centuriae, inclusis quibusdam Mendocinis et Patagonicis. Linnaea 33: 1-308. MEGMOM bec i literarias. Botánica. Anales tiv. Chile 43 ——. me Plantas init Chilenas. Anales Univ. Chile 94: 5-34. Porter, D. M. 1986. Charles Darwin's vascular plant specimens from the voyage of HMS Beagle. Bot. J. Linn. Soc. 93: 1-172. Quicke, D. L. J. 1993. Principles and Techniques of Contemporary Taxonomy. Blackie Academic & Profes sional, London. Quintanar, A., S. Castroviejo & P. Catalán. 2007. Phylogeny of the tribe Aveneae (Pooideae, Poaceae) inferred from plastid trnT-F and nuclear ITS sequences. Amer. J. Bot. Raven, P. H. & D. I. Axelrod. 1974. Mp eren bio- geography n. Missouri Bot. Gard. 61: 539-673. Rügolo de Agrasar, Z. 1986. Las especies extrapatagóni del género Deyeuxia (Cramine 1 IL. erp de la to ha Parodiana Rzedowski, J. & G. Rzedowski. 1990. Flora octane del Valle de Mexico 2. Publicaciones del Instituto de Ecologia, Michoac Soreng, R. J. & J. I. Davis. 2000. Ph — structure in Piceni subfamily Pooideae as inferred f rom molecular and paps me ap j; Mi n S. itors), Grasses: Common- wealth Scientific e Industrial Research Organisation, Collingwood, Victori &M a Voionmaa. 2007. A sig eo analysis zi Poaceae tribe Poeae sensu lato morphological characters and sequence data from des dent odd genes: Evidence for T: and a new classification for the tribe. Kew B : 42 Stebbins, C. L. 1975. The role of polyploid complexes i in the wya of Nah American grasslands. Taxon 24: di 1962. Notes on some grasses. XIV. oo e genera of ee p Mag. (Tokyo) 75 zvelev, N. N. 1976. Grasses of the Soviet ba. Nauka "abes House, Leningrad. Valencia, J. 1941. Especies críticas de Trisetum = deben pasar al género Deschampsia. Revista Argent. Agron. 8: 122-130. van de Vouw, M., n Dijk € A. H. L. Huiskes. 2007. Regional genetic diversity ET in Antarctic hairgrass ). J. Biogeogr. 35: 365-3 Vigi i Sele: J o” Flora E la Vall de Ribes. Acta Bot. Barcinon. 35: 1-7 APPENDIX 1. Examined material of Deschampsia. Each specimen is cited by the last name of the first collector when there i is more ma one colector. — number is to the List of Species below. LisT oF SPECIES 1. Deschampsia airiformis T Benth. & Hook. f. 2. Deschampsia antarctica 3. Deschampsia berteroana odo Trin. 4a eds cespitosa (L.) P. Beauv. var. cespitosa D y Deschampsia cespitosa (Nees & Meyen) Nicora var. pulchra 5. Desc cordilleraru um 6. Descham ia danthonivides e Munro 7. Deschampsia d (Hook.) Munro 8. Deschampsia kingii (Hook. f.) E. Desv. 9. Descha ie Phil. 10. Deschampsia looseriana Parodi 11. Deschampsia mendocina Pa 12. Deschampsia parvula (Hook. f. s 13. Deschampsia patula (Phil.) ie ex Skousb. 14. Deschampsia setacea (Huds.) H 15. Deschampsia venustula P. Annals of the Missouri Botanical Garden Abrams 2833 agen. fagi e s.n. (12); Allen 38 (7); Ambrosetti 206 (2), 1202 (3), 7713 (3); Arneberg 9632 (8); Arroyo 83-1340 (15), 85-155 (13), 87-0007 (12), s.n. (2). Barnier 232 Barrientos 11 (10), 220 (7), 511 leg 976 (3), ER 1655 (3), AE 7 (1), 5871 (1), 99 (3); Beetle 1731 (6); Behn 12493 ip 599 3201 (1), 4122 oe 41 “e 72 ab. (2). 6051 (7), 9765 (5), 10213 (4a), 12358 (13), 12: 13830 (4b), 14056 T 14330 (4a); Boelcke et al. Dy (15); Bonarelli 78 Bossieu s.n. (2); Bravo 23 (10); Burkart (7); Burmeister s.n. (13), s.n. (8). Calder 29623 (6), 35255 (7); Carette 22 Castellanos 12831 (12), 7572 (2), 12846 (8), s.n. (4a); Colonie 2107 qu pm 923 (2), 3082 (2), 5598 (7); Corte 1 (2); Covas 1 Dauber 168, 195 (2% De Giorgia 452 (3); De La Riie s.n. (2); Dimitri 2843 (4a), 4455 (4a), 8243 (2); Durán 3507 (6); Dusén 405 (2), 548 9 (7). Elmer 1664 (7); M X o, ue (8). ee a S (1 i igueroa 3094 (Aa). € 667 (3) 2838 (3); king 19 4a C 00 (8); m e 15a (2 “e 7226 (1 6211 (4a), sae es, Se 6169 ( ), 3486" 4480 (2), 7226 (12); pod E Gunci 18244 (3), n e 25067 d 26730 E Ou 474 (8). Haene 1 n. ( ller Tei Stk Hitchcock Iro. 1419 (6% Hoover 6730 789 (6); Hueck 18191 (15); Hunziker, A. T. 8218 (8), 8225 (2), 10112 Q) It T (2), 10147 (2), 10150 e 10152 (2), 10153 (2), 10190 (2), 10196 (2, 10200 (2, 10205 2); Hunziker, J. H. 6709 8). 6763 @) 167 (7), 224 (7), 226 (4a); Iter Patagonicum 126 (12), € sn. (7); Jiles 3623 (5), 4143 (14), 6073 (3); Johnson 586 (9); pompa "M ER es Jones 2157 (6). Kildale 6100 (7); Koslows, 142 (8), 22. a Pede 631 (1). 2004 s Kurtz 32 (8), m (4b). 9667 (4a), 9727 (4a), 10991 (15). Laffuel 1838 (10), 1903 (2); Land s.n. (14); Lauria sn. (2); Leén 2400 (13); Levi 2674 (10); Longton 601 (2); Looser 1111 (14), 1384 (3), 3438 (10), 3718 (10); Luti 1435 (8, 485 (2) Maldonado 129 29 (1); Marticorena 143 (6), 216 (6), 228 ( 387 (10); Martinez 2 (2); Martínez 52495 (3); Martínez Crovetto 26 (7); Morrison 17424 Navas 8123 (10); Nicora ed -17 (7), 3635 (7), 3768 (4a), 9340 (1), nes (2), 26417 (2). Parodi 9550 (8), 11425 (7), 15358 (1), s Popovici s.n. (2); Póppig s.n. (3); Pringle 4743 (1), 13244 (Ty. Procter 16 (2). 3864 (4a); Ricardi 375 (7); Ritter 2199 (Aa); Roig 77 (13); = 9695 (4a); Ruiz Leal 7843 (4a), 15025 (2); Ryves 96/081 (3). Santana Michel 3411 (7); Schlegel 2590 €: Se 1735 — 4a); Siple 336 (2); Skottsberg 63 (2), s.n. (8); S (2); Smith 13371 (Aa), 15713 (Aa); Soriano 1511 Sr ud 2245 (2), 2554 (2), 3083 (2), 31964 a, 4474 (2), 4626 (1), 5368 (8), 5415 (2), 5802 (1); Spegazz (12). : TBPA 1912 e. 2139 (2), 2916 (12), E e A: ^ 5103 (9), 54 ur 14258 (6); Tortorelli s.n. s. a s.n. Ulibarri 106 Vallerini vy ©. 3900 qas = 2394 (4a). erdermann 582 (4a); W. 2). Zöllner 9623 (12), 46212 ( p roD EE EFL EIU AE ex A TAXONOMIC REVISION OF RHODODENDRON SUBG. TSUTSUSI SECT. BRACHYCALYX (ERICACEAE)! Jin Xiao-Feng,? Ding Bing-Yang,° ng Yue-Jiao,* and Hong De-Yuan? ABSTRACT ly 30 spares in espi sm L. subg. Tus (Sweet) Pojark. (Ericaceae) and Sent is iine fisiributeji from i Chine to Japan a ell eight s pecies ized. Poss um Miq. var. decandrum Makino is s newly recognized Me ula at the new rank P eae as R lant subsp. ean (Makino) X. F. Jin & B. Y. Ding. Lectotypes are designated for R. Le T" => Hatus., R. quise € ex Sweet var. leucotrichum Franch., R. mariesii Hemsl. & E. H. Wilson, R. reticulatum D m Makino x G. Don, Key words: E a Asia, E pers ae sect. Brachycalyx. The genus Rhododendron L. (Ericaceae), which is well known as a group of alpine flowers, contains about 1000 species worldwide (Chamberlain et al., 1996; Fang et al, 2005) The Sino-Himalayan, southwest China, and northern Burma regions are the largest diversity centers, with western Sichuan, northwestern Yunnan, and southeastern Tibet consid- 1979). peared with Azalea L. (Linnaeus, 1753). Salisbury retained Azalea within Rhododendron, which is now followed widely (Philipson & Philipson, 1973). In terms of roblems (Kurashig 1). (1870) published his Rhododendreae Asiae Orientalis which took the greatest step forward on classification (Philipson & Philipson, 1973). He used the position of flower buds and their relationship with leaf buds to divide the infrageneric ranks, which contained eight sections. Hooker’s treatment of Rhododendron in Genera Plantarum was similar to Maximowicz, but ag le ranks (Hooker, 1876), B a 1980) recognized eight sub- genera using the following characters: relationship of flower buds and leaf buds, habitat, flower structure, and je or non-lepidote leaves. He divided the lepidote group into three subgenera. Cullen and (laba (1978, 1979) and Philipson and Philip- son presented a synopsis of infrageneric division. Their taxa were mainly based on Sleumer's classification, but the few changes were for the better. ndron sect. Brachycalyx Sweet was first proposed by Tate, based on a typified Chinese pecies, R. farrerae Tate ex Sweet. Unfortunately, Tate placed R. dauricum L., a deciduous but lepidote taxon, in this section. Tate also used Kaempfer's name Tsutsusi for the azalea section. De Candolle treated the evergreen azaleas as a section (section Tsutsusi Sweet) of Rhododendron, but Philipson and Philipson (1973) placed R. farrerae in their Eurhododendron un ! This work is supported by the National Natural Science Foundation of China (NSFC grant 30370106). The authors are grateful to the mem of the didus herbaria: B, CCTM, CDBI, FJFC, FMP, e GXMI, |, NAS, NF, P, PE, SCFI SZ, TI author to — their collections. We are snail to Yasuyuki Watano, I Minamitani, Shuichi Xiao-Mei, Chen Hu, Gui Xiao-Sheng, Huang Guo-Lin, and W nks to Wang Wen-Tsai HTC, HZU, IBK, IBSC, KUN, KYO, LBG, N Toma, Wu Yan, Zhao fieldwork. "n diio give our sincere tha GZTM, HGAS, HHBC, HNNU, W, ZJFC, and ZM, who permitted the first Kurogi, Tetsuo Ohi- ng Hong for their assistance during > . and Zheng Chao-Zong for their critical comments on an earlier this manuscript; Victoria C. Hollowell for providing editorial help and improving the Englis h; Wu Fei-Jie, Cao Pei- Jian, Sus Sheng-Xiang, and Xu Xue-Hong for providing some literature; and Pan Yi-Jing for clarifying the locality names in J apa "School of Life and Environment Sciences, Hangz Zone, Hangzhou, Zhejian: * School P Republic of China. dby@wzu. Normal Uni s No. 16 Xuelin Street, Xiasha Higher Educational g, 310036, People’s Est of China. docxfjin@163.com Life - Environment Sciences, Wenzhou University, No. 276 Kueyusu Road, Wenzhou 325027, People's "College of Life peciit ae University, No. 232 Wensan Road, Hangzhou, Zhejiang, 310012, People’s Republic of Chi na. zhangyj_moonO163.com. s Key aS of Systematic and Evolutionary Botany, c rq Botany, Chinese Academy of Sciences, angshan, Beijing 100093, People’s Republic of China. hongdyOns.ibcas.ac "m 10.3417/2007139 Ann. Missourt Bor. Garp. 97: 163—190. PUBLISHED on 9 JuLy 2010. Annals of the Missouri Botanical Garden and R. dauricum, with R. dauricum now placed in section Rhododendron (Cullen, 1980). Don (1834) ` then described R. reticulatum D. Don ex G. Don in À 3 General History of Dichlamydeous Plants, and laterR. dilatatum Miq. would become the third species in this _ group. Maximowicz (1870) was innovative in that he used the character of flower buds. The evergreen/ Indian azaleas, which have terminal flower buds, formed section Tsusia Maxim., this name restricted to these species. The features of buds are often difficult to observe, and Maximowicz failed to explain his species, R. schli ii Maxim. (Philipson & Philipson, 1973). Until now, the pl tof R. schlippenbachii i still confused (Philipson & Philipson, 1982; He, 1994; Judd & Kron, 1995; Yamazaki, 1996; He & Chamber- lain, 2005). Wilson and Rehder (1921), in A Mono- of Azaleas, p section ion Rehder & E. H. Wilson to replace section Brachycalyx. Section Sciadorhodion was accepted by Kitamura and Murata (Kitamura, 1971) and Judd and Kron (1995), but later was combined at the ubgeneric (Yamazaki, 1993, 1996). Nakai (1924, 1927) another section name, section Verticillata Nakai, and species of this section have mixed flower and leaf buds except in R. schlippenbachii. In Sleumer’s system, section Brachycalyx was placed in subgenus Tsutsusi (Sweet) Pojark., with section Tsusiopsi established as a new section. Section Tsusiopsis, the x ran and leaves 2-opposite or 3-verticillate at the apices of branchlets (Sleumer, 1949, 1980). Spethmann (1987) treated subsection Brachycalyces Spethmann within subgenus Pentanthera (G. Don) Pojark. sect. Tsutsusi, and posed subsection Tashiroia (Rehder) Spethmann instead of section Tsusiopsis. Chamberlai (1990) retained section Tsusiopsis to section Tsutsusi, but Yamazaki (1993, 1996) retained it to subgenus Sciadorhodion (E. H. Wilson & Rehder) T. Yamaz (Table 1). During a recent visit to three herbaria (TI, KYO and TNS) in Japan, the first author was able examine all collections of subgenus Sciadorhod (sensu Yamazaki, 1993, 1996). We found that it was to Tsusiopsis to the synonymy of section Brachycalyx. re ITS sequence data and pollen morphology support this taxonomic view as well (Gao et al., 2002a, b). Brier Taxonomic History As mentioned above, men n sect. Brachy- calyx initially contained only two e species, R. farrerae section. During his eastern Asian azalea research, ; Maximowicz described the species R. weyric Maxim. and later R. tashiroi (Maximowiez, 1870, . ndron quinquefolium Bisset Moore was described at around the same time. In the late 19th century, a new variety of R. dilatatum was named by Makino (Makino, 1893). From the early 20th century to 1920, Makino and Nakai published several taxa for this section during their research of Japanese plants (Makino, 1917, 1926a, b; Nakai, 1926), and Nakai (1927) placed them all in section Verticillata and also made a small revision. Then, five species, namely R. mayebarae Nakai H Azalea amagiana Makino (— R. amagianum Makino), A. kiyosumensis Makino (— R. kiyosumense Makino), R. viscistylum Nakai, and R. sanctum Nakai were designated (Makino, 1931: Nakai, 1932, 1935; Hara, 1935). Hara (1948) made an enumeration of Japanese seed plants, which provided a detailed list of Japanese ron and also proposed several new names. In Flora of Japan, Ohwi's treatment was very similar to Hara's, but some varieties and forms were neglected (Ohwi, 1953). Kitamura and Murata (1971) published Coloured Illustrations of Woody Plants of Japan; their roader-scale understanding of the Japanese Rhodo- dendron led to fewer taxa than Hara and Ohwi. Later, Hara (1974) described R. hidakanum H. Hara and placed the species in section Brachycalyx. Yamazaki was regarded as the most comprehensive taxonomist across section Brachycalyx, not only because he proposed many new species, varieties, and combina- tions, but also because he investigated this section presented a new system (Yamazaki, 1981, 1984, 1987a, b, 1988, 1991, 1993, 1996). veral species of section Brachycalyx were discovered in China. Hemsley and Wilson (1907) designated on mariesii Hemsl. & E. H. Wilson as a new species, which was collected in northwestern Hubei and widely distributed in the drainage area of the Yangtze River (Fang, 1935). Hayata studied the collections from Taiwan and R. shojoense Hayata and R. phalocarpum Hayata (Hayata, 1913; Yamazaki, 1996). Tam Pei- Cheung i ig iJ doas n : China and described R. cinereoserratum P. C. Tam and R. daiyunicum P. C. Tam as new species (Tam, 1982). However, R. daiyuenshanicum P. C. Tam later replaced R. daiyunicum (Tam, 1983). Ding and Fang (1990) discovered R. huadi nse B. Y. Ding & Y. Y. Fang, with this name not validly published until 2005. a iiid. AA uS: 165 of Rhododendron sect. Brachycalyx Jin et al. Volume 97, Number 2 2010 evision R UuOs|I M (pəpnjoxə) 'zewe g ‘L (UNA ( itxe y 'H M» zepuey Dryooquaddijyag “1098 nyapquaddiyyos nyovquaddyyos “y UO1POYLOPDIIG 1998 "Y IX JA Suipnjour) uos[tA, unppAydpjuad 'H UH Jepyey ‘y = uuewyjedg UO1POYLOPDIIS '19Əs nsuas) UOS|IA\ 'H ` 9 PYY uoipot1oppiog 1908 199MG “Zee A “L JIMS uueuyodg (199M9) 199MG 199MG TENEN xAqpoKuoDag 1998 pyofanbuine) 1998 xAqpoKuyop4g 1998 —— sooKqpoKwyop4g "1o9sqns xApDIAYIDIG “1998 xAqpoXuopa4g 1098 DID]NOYLAA 1998 Joumo[s ‘ZBUIB ‘L uupuiu1ədç (19pyay) 1oumo[s Aəuunə|ç Sal Y 199MS 15NSIM8 *1998 sisdoisns[ 1998 UOIPOYAOPDIIS 1998 D1041/$0 [, "oosqns sisdoisns[ 11998 sisdoisnsp *joos. uoupuapopoiuymg “1998 UL "UIXe[N 1041150] uospuapopoyy ‘zewg ‘I (Pyy 9 uos[t A ^H 7) uoimowy4opriog '3qns 1ƏƏAÇ 1sns1ns | 1998 "Ze We A (urxe 10414507 Mp srjsououosg *109s "y 3urpn[our) uuevwyjedg (1apyay) 199MS ISNSINS] 03S AMG ISNSINS] ']2os 199MG 199MS IsNSINS] “oes 199MS 15NS1M5,J, 1998 psnigg “joesqns 19NSIMS j, 1998 yrefoq apelog (199mg) efod uoq ‘9 SHefoq (əəwçs) “yefog (199mg) (1996) 19nSmMS y ‘Bqns isnsins J “3qns (199MG) Isnsyns 7 "aqns isnsins[ 1098 i8nsins] "dqns isnsqms p "qns s00¿ 9661 0661 ‘Y L861 'uueungiads Z861 “uosdiliuq 0961 LZ6T ‘HYEN 161 a poquieyo 3» oH “S661 “Pyezeure 1 = ere 9 uosdi[tuq '6P6T "1eume[s DP Y A ‘isnsms | snuasqns YILM Jayesoy ‘xAppodkyooig “1998 UoLpuapopoyy jo suonrsod onguiojsás juo19giq.--."[ e[qPL Annals of the Missouri Botanical Garden since two collections were cited as type (Ding & Jin, 2005). Further examination of the type and observa- tion of seed coat and pollen revealed that R. huadingense should belong to section Pentanthera G. Don (Jin, 2006). Ding and Fang (19892) also named a white-flowered form of R. mariesii when they surveyed the rhododendrons in Zhejiang, eastern China. Kurashige (1999) published R. chilanshanense Y. Kurashige, which was collected in Taiwan. Chamberlain n Ree DS revised the entire ubgenus as lron subg. Tsutsusi, hist Woh Sole oben Pt acta Bodo in doubt. Yamazaki (1996) later revised this group, which was distributed in Japan, Korea, and Taiwan. Many specimens of R. farrerae were examined, but herein we cite only two or three specimens from the same locality rather than a comprehensive listing. MORPHOLOGICAL CHARACTERS We discuss the principal diagnostic characters used to identify members ron sect. Brachycalyx (Chamberlain & Rae, 1990; Yamazaki 1993, 1996; He, 1994; He & Chamberlain, 2005). HABIT From previous reports, all species of Rhododendron sect. Brachycalyx are deciduous shrubs, except R. tashiroi. Based on specimen examination, we found R. tashiroi and R. daiyunicum to be ev n, with leaves that may be persistent in winter. The deciduous shrub species are commonly less than 5 m tall and as shrubs are typically ramified. LEAF Leaves are generally verticillate at the top of young shoots. Most species in this section have leaves in a whorl of three, but the leaves of Rhododendron quinquefolium are 5-verticillate. The leaves of R. tashiroi are sometimes opposite or 3-verticillate, and leaves of reticulatum var. bifolium T. Yamaz. are also 3-verticillate, with one blade lanceolate or setaceous er than the other two. The leaf shape is usually ovate or triangular-ovate, but shapes may be variable, especially for widespread species (e.g., R. and R. mariesii), with their leaves ranging from oblong to ovate-elliptic. Rhododendron tashiroi is the only taxon known to have coriaceous leaves, with other taxa in the section having chartaceous or thickly chartaceous blades. Leaf apices are often acute or acuminate and terminate in a mucro or gland. Leaf margins are minutely denticulate, or sometimes incon- spicuous, and those of R. quinquefolium are ciliate. Indumentum on the leaf dorsal surface is variable. Yamazaki distinguished some taxa mainly by the villose pubescence on the dorsal midribs (Yamazaki, 1993, 1996), but we found this to be a fallible ` character for some species identification. From fieldwork, weyrichii, R. Yamaz. are characterized by glands on dorsal surfaces of immature leaf blades. Petiole length ranges from 2—10 mm. Rhododendron farrerae differs from R. mariesii mainly in its shorter but pubescent petioles. Examination of specimens reveal ° considerable overlap, with the petiole indumentum in various patterns. Four types of indumentum can be i J. (1) (D > K s x 3 y villose (R. amagianum and R. sanctum); (3) densely or ly soft pubescent (R. nudipes Nakai and related taxa); and (4) glandular, lm -glandular, or some- times with sparse soft trichomes (R. weyrichii, R. dilatatum, and related taxa). PEDICEL Pedicels range from 5—10 mm and usually elongate when fruiting, with the pedicels of Rhododendron huadingense often 12—20 mm in length. The indumen- tum of pedicels correlates with that seen for petioles. INFLORESCENCE Tan f tho ecies in Rhododendi sect Brachycalyx have fi Q one to three (to four) flowers, in terminal umbels. Yamazaki (1993, 1996) used the character of solitary flowers to identify R. osuzuya- mense, R. hyugaense (T. Yamaz.) T. Yamaz., R. ce and R. amakusaense (Takada ex _ T. az.) T. Yamaz. Species seen in Kyushu, Japan, bit that this character was not consistently reliable, as R. osuzu and R. 2-flowered umbels. Occasionally, R. mayebarae and R. nudipes have only a single flower as a reduced inflorescence (Minamitani, 1984). amakusaense, FLOWER Flowers in Rhododendron sect. Brachycalyx appear prior to or with leaf emergence, ranging from late February to early June. Within a species, flowering time is mainly impacted by altitude (Minamitani, 1984). Flowers of three species (R. sanctum, R. amagianum, and R. quinquefolium) appear in May to mid-July, opening after the leaves appear. This character has been used frequently to distinguish species in Japan. EN Mareen Volume 97, Number 2 2010 Jin et al. 167 Revision of Rhododendron sect. Brachycalyx Only Rhododendron daiyunicum has distinct calyx lobes ca. 5 mm (Tam, 1982), but the species type shows an indistinct calyx. Calyces of all species in ron sect. Brachycalyx are minute (3-4 mm diam.) with the lobes inconspicuous or slightly conspicuous (e.g. R. quinquefolium). The calyx indumentum correlates with that seen on the pedicels. Corollas are funnelform or rotate-funnelform, and the corolla tubes are conspicuous. Colors are variable, e.g., pale pink, rose-pink, lilac, xn reddish purple to red, rarely white. Most species have dark blotches on the upper internal surface of the i but rarely pale blotches occur (e.g., Rhododendron osuzuya- mense). Corolla length is from 20—35 mm, but some species reach mm R. weyrichii and R amagianum). Corolla Eo are oblong or elliptic, deeply divided, and spreading. Stamens are five to 10 in section Brachycalyx, with only Rhododendron dilatatum having five stamens. The remaining species have 10 stamens, but occa- sionally eight or nine stamens may be seen in flowers. The stamens are generally unequal and are shorter than or equal to the corolla in length. Anthers are s 2-3 mm long; filaments are s or rarely sparsely pubescent on the lower half (e.g., AE Only R. quinquefolium has filaments are densely pubescent in their lower third. Rhodo- dendron farrerae was described with its filaments ER En trichomes on the lower half (He, Chamberlain, 2005), but Fang (1935) and our ds indicate the filaments to be glabrou (Ding & Fang, 1989b). Styles in Rhododendron sect. Brachycalyx are 25— 50 mm long, usually curved at the base, and longer than or — to the corolla in length. The stylar well, but most members in section Brachya m nigeria styles. Styles of Rhododendron R. sanctum are occasionally bade Senet R. wadanum has styles glandular on the lower half indumentum ariable Ovary shapes are almost ovoid versus oblong-ovoid (only ‘Rhododendron dilatatum). Three types of ovary indumentum are recognized: (1) glabrous (e.g., R. quinquefolium); (2) with dense or sparse soft trichomes (e.g., R. farrerae, R. mariesii, R. reticulatum, R. lagopus Nakai, R. nudipes, R. uadanum, R. sanctu R. weyrichii); and (3) sparsely to densely Waysa pubescent, sometimes with s t trichomes (e.g., R dilatatum, R. hyugaense, R. osuzuyamense, R. viscistylum, R. chilanshanense). CAPSULE The size and shape of the capsule are variable both within infraspecies and among species in Rhododen- dron sect. Brachycalyx. Capsules are usually oblique- -q is similar to the dilatan of the ovaries, and that of R. quinquefolium is glabrous. Members of Rhododen- dron ser. Dilatata T. Yamaz. (sensu Yamazaki, 1993, 1996) always have capsules with glandular indumen- tum, occasionally with sparse trichomes. Capsules in this section are otherwise sparsely or densely hirsute, and trichomes may be conspicuously spreading (e.g., R. reticulatum, R. mayebarae, and R. mariesii). SEED Seeds in Rhododendron sect. eas alyx are v small, ES and without wings. Mo iced characters of seeds for "ww species were available to us, namely R. reticulatum, R. tashiroi, R. quinquefo- The surface cells of R. nquefolium are protruding, short, and broad versus slightly concave, long, and narrow (Ding et al., 1995; 996). pae and R. mariesii. Yamazaki, 1 MATERIALS AND METHODS Over 10,000 collections of Rhododend Poles, preserved in 30 herbaria B. "CCTM [Herbarium of the Institute of Canton Chinese Traditional Medicine], CDBI, FJFC, FMP, FNU, GXMI, GZTM, HGAS, HHBG, HNNU, HTC, HZU, IBK, IBSC, KUN, KYO, AS, NP, P, PE, FI, SZ, TI, TNS, W, ZJFC, and ZM) were examined. Descriptions for each species were based on these specimens. It was not possible to examine D of R. chilanshanense, and this species is d 2 the original description (Kurashige, 999 he subsequent Flora of China treatment (He & bien. 2005). Leaf blade measurements were taken from fruiting collections, and px of indumentum were taken from these ma specimens as well. The lengths of both the oe and fruits were measured from the calyx apices to the corolla or capsule apices. Corolla colors were taken mainly from collection notes, Yamazaki’s (1993, edm t and our fieldwork. Taxa in Japan Po Mee to Yamazaki's concept (Tasai i 3, 1996). For LE rank, we recognize only subspecies, but this differentiation intergrades among taxa. Our subspecies concept imet a oop differen- y delimited. In section Bysckycalou, taxa with white flowers had been previously designated as variety or form (Ding & Fang, ; Yamazaki, 1993, 1996), and these two wd. um 1 f, + Tta d SE tiation Annals of the Missouri Botanical Garden variation for a single character such as the corolla color. These taxonomic entities often encompass few individuals, limited to the population level, and are better suited for horticultural recognition. Specimen localities in China are resolved to the counties (-xian) or mountains (-shan), and those in Japan are often called -gun or -yama/mura, respectively. TAXONOMIC TREATMENT Rhododendron L., Sp. Pl. 1: 392. 1753. TYPE: Rhododendron ferrugineum L. Azalea L., Sp. Pl. 1: 150. 1753. TYPE: Azalea indica L. [= Rhododendron indicum (L.) Sweet]. Trees or shrubs, terrestrial or sometimes epiphytic; indumentum various (see Seith & Hoff, 1980), with peltate scales, glabrous, c or sometimes with trichomes. sometimes lateral, 1- to 30-flowered. Calyx 5- to 8- lobed, lobes minute and triangular to large and conspicuous, sometimes reduced to a rim; eats funnelform to campanulate, occasionally rota panulate, regular or slightly zygomorphic, 5 n 3. ah tame 5» 10, pel 5 to 20 (to 27), inserted dal glabrous or basally ; pilose; sula without appe opening from terminal or oblique pores; ovary b 5-locular, rarely 6- to 20-locular, with trichomes and/or scales, rarely glabrous; style straight or declinate to deflexed, persistent; stigma capitate, crenate to lobed. Capsule dehiscing from the apex and moving down, cylindrical, coniform, or ovoid, sometimes curved; valves ligneous, thick or thin, lio twisted. Seeds numerous, minute, fusiform, always winged, or with appendages or — tails on both ends, rarely without appendag Rhododendron sect. Brachyealyx Tate ex Sweet, Brit. Fl. Gard. ser. 2, 1: 95. 1831. Rhododendron subsect. Brachycalyces (Sweet) Spethmann, PI. Syst. Evol. 157: 28. 1987. TYPE: Rhododendron farrerae Tate ex Sweet. ser. Dilatata T. Yamaz., Fl. Jap. (Iwatsuki et al. eds) (ed. 2) 3a: 32. 1993. TYPE: Rhododendron dilatatum Miq. Rhododendron ser Glangulistyi Boas (Iwatsuki po de e 2 de 95 Me Rhododendron wadanum M. Key To Species OF RHODODENDRON SECT. BRACHYCALYX a. Leaves ev evergreen, coriaceous, opposite in pairs or 3-verticillate ^ Leaves deciduous, eous, 3-verticil — erticillate. chartac: 2a. Leaves 5-verticillate; pedicels and ovari : . Yamaz., Fl. Jap. (Iwatsuki et i al., eds.) es 2) 3a: 35. 1993. TYPE: ndron nudipes Nakai [= Rhododendron farrerae Tate ex Sweet]. sect. Quinquefolia T. Yamaz., Fl. Jap. (Iwatsuki et al., eds.) (ed. 2) 3a: 30. [^ E. : Rhododendron quinquefolium Bisset & S Rhododendron ser. Reticulata T. Yamaz., Fl. je: pu : al., ser Ae yee 37. 1993. TYPE: E: Rhododendron Don ex G. Don [= Rhododendron Posse Tate ex Sweet]. ser. Sciadorhodion T. Yamaz. Fl. Jap. (Iwatsuki et al., eds.) = 2) 3a: uu 1993. TYPE: Rhododendron farrerae Tate ex Swee sect. Tsusiopsis Sleumer, et: Jahrb. Syst. 74: 552. 1949. on subsect. Tashiroia (Rehder) Spethmann, Pl. Syst. E. 157: 28. 1987. TYPE: Rhododendron tashiroi M sect. Verticillata Nakai, Trees Shrubs T: : T 1922. TYPE: Rhododendron reticulatum D. Don [= Rhododendron farrerae Tate ex Sweet]. cirio ser. Weyrichia T. Yamaz., Fl. Jap. (Iwatsuki et al., eds.) (ed. 2 3a: 31. 1993. TYPE: Rhododendron weyrichii Maxi SH BE o d | 2 x :n —9Ó ¡dá or ia: feines pw: or thin-chartaceous, glandular, villose, or silky- vui when young, glabrescent or partly glabres- cent later. Both flowers and leaves emerge from the same mixed buds. Inflorescence 1- to 4-flowered; corymb terminal. Calyx lobes minute, only to 2 mm; corolla rotate-funnelform or funnelform, pale purple, pink, lilac-purple, purplish red to reddish purple or red, rarely white, often with dark blotches or spots inside and glabrous on outer surface; stamens 5 to 10, unequal; filaments glabrous, or rarely with pubescence on lower half; ovary villose and/or glandular, sometimes glabrous; style generally glabrous, rarely glandular and/or villose on lower half. Capsules oblong-ovoid to cylindric, rarely ovoid, sometimes slightly curved. Seeds numerous, minute, brown Rhododendron sect. Brachycalyx comprises nine taxa (eight species and one subspe- cies), with three species distributed in China, six species and one — in Japan, and one species in South Korea Distribution. Discuss Rhododend sect. Sciadorhodion Rehder & E H. Wilson (Wilson & Rehder, 1921: 79) and Azalea subg. Sciadorhodion (Rehder & E. H. M Copeland (1943: 597), with R. quinquefolium type, could be encompassed within section k... with the exception of the species R. schlippenbachii. 6. R. tashiroi 5. R. quinquefolium Volume 97, Number 2 2010 Jin et al. 169 Revision of Rhododendron sect. Brachycalyx 2b. Leaves K pedicels and ovaries glandular, glandular-pilose, and/or hirsute. 3a. Sty! 4a. 3b. i — or sparsely hirsute at base wers opening after ular 4b. Ovaries villose, with glands, viscous; style glandular, ce with sparse villose iion R. wadanum 2.R. NA er leaf pine petioles and blade midribs densely et lamina x agi vd Sige inate MA oe 1. R. amagianum 5b. Flossie opening usually before or with | dicels and blade midribs glabrous, villose, and/or glandular; lamina usually ovate to triangular-ovate. en Ovaries vilo without glands, not viscous. 7a. Corollas iid, 35—40 mm long; leaves glandular when young ............. R. weyrichii 7b. Corollas Soriana lilac, to pale purple, rarely white, 22-35 mm long; leaves - besce R. farr when young . ...... pu 6b. Ovaries Mie. but anth plAnds CONS 23.6 nee ee oe oUt oe ee So 3. r^ dilatatum L. T 3 1 > Makino, J. Jap. Bot. 7: 21. 1931. Rhodsdendron weyrichii Maxim. var. ew esas E Hatus., Sci. Rep. Yoko- a City Mus. 15: 23. 1969. TYPE: Japan. RIED ux. e , Mt. Amagi, T. Makino s.n. (holotype, MAK!). Fi igure 1 — sanctum B Bot. Mag. ag a 46: 630. weyrichii Max var. sanctum db Hatus., s Re ep. Yokosuka City Mus. 15: 23. 1969, syn. nov. TYPE: Japan. Honshü: Pref. be June 1932, A. Ando s.n. (lectotype, designated by Yamazaki, 1996: 89, TI!). — sanctum Nakai f. albiflorum n. Rhododen Yamaz., Revis. Shisuoka), Inasa-gun, Shizutama-mura, cultivated in Tokyo, 22 May 1995, T. Yamazaki 54970 (holotype, TI). Rhododendron sanctum Nakai var. lasigema Nakai ex Sugim., Key Tr. & Shr. Jap. (ed. 1): 304. en TYPE: Japan Honshü: Toonoe (Pref. Shizuoka), oiii Shizutama-mun, May 1935, J. cas s.n. (holotype, TI). Shrubs deciduous, 2—4 m tall, sometimes to 6 m; young shoots densely pilose. Leaves chartaceous, in a whorl of 3 (3- se iwa, rhombic or rhombic-ovate, cm, acute or acuminate, with an a gland, cuneate or rounded at base, entire, aen dorsally glabrous except midribs villose, ventrally pubescent, later becoming glabrous; petioles 3—7(—10) mm, densely villose. Inflorescences 2- or 3-flowered; pedicels 5-10 mm, villose. Calyx bowl-shaped, ca. 3 mm diam., villose, lobes inconspicuous; corolla purplish red or red, rarely white, broadly m 35-45 X 40—50 mm, deeply 5-divided, tube 10-15(-18 m, glabrous on both surfaces, lobes eii or E 25-32 "1 13-20 mm, upper lobes with dark purplish red spots at base; stamens 10, rarely 8 or 9, unequal in length, 20—45 mm, filaments glabrous, anthers oblong, 2-2.5 mm; ovary ovoid, densely villose; style 35-50 mm, rous or sparsely hirsute at base. Capsule obliquely cylindrical, 12— 17(-20) X 5-7 mm, densely hirsute; seeds 1.5-2 X ca. 0.5 mm. Distribution and habitat. Rhododendron amagia- num is restricted to Izu Oshima and the adjacent mainland of Japan. It grows in forests at elevations of 1000 m above sea level (a.s.l.). Phenology. Rhododendron amagianum flowers from late May to mid-July, with the flowers opening after the emergence of leaves. It fruits from late oor to early December Discuss Rhododendron amagianum is a re- es taxon in that its flowers open after the emergence of the leaves. Furthermore, its bios and midribs are densely villose, and the leaves are rhombic or rhombic-ovate in shape. Rhododendron amagianum is similar to R. weyrichii, another Japanese species in section Brachycalyx, in having red flowers and the leaves also being rhombic-ovate. Rhododendron ama- gianum differs in its petioles and leaf midribs being densely villose dorsally and in its flowers opening after leaf emergence. In contrast, the petioles of R. weyrichii are only sparsely pubescent, the leaf midribs are pubescent on both surfaces and later glabrescent, and the flowers open before or with the m Rhododendron sanctum shed as a species based on its leaves hos E smaller, with shorter flowering buds than R. amagianum, and the styles sparsely hirsute at the base (Nakai, 1932). The TI pe which was designated by Yamazaki in 1996, reveals glabrous styles. Using Nakai's diagnos- tic a we can hardly distinguish R. amagia- num from R. sanctum. Considering the similar morphology and distribution, we reduce R. sanctum and its related taxa to the synonymy of R. amagianum. nal specimens examined. JAPAN. Honshú: Pref. Aichi: Horai, beca Mt. e K. Tori 13969 (KYO); Yana-gun, Tsugeno, S. Kitamura & G. Murata 335 (KYO). f. wa: Sagami, Hakone, hee s. Okuyama & I. seit s.n. (TNS); S i I T. Ookawac n. (TNS). Pref. Mie: Ise, Mt. a, T. Tashiro 51742 vie 51743 us s.n. (KYO), M. Annals of the € Missouri Botanical Garden gure ]. = oe shoot. —B. Leaf, showing indumentum. —C. Stamen. —D. a "M A—D from Y. Kimura s.n.; E from Hara a s.n. amagianum Makino. Volume 97, Number 2 2010 Jin et al. 171 Revision of Rhododendron sect. Brachycalyx Togashi 7403 (P, TNS), C. Chuma & M. Togashi s.n. (KYO), * Murata 8714 (KYO), 8720 x Shima, Isl. E Y. Momotani s.n. (KYO). Pref. uok Kiwarq s 8 (TI), H. Hara s.n. (TI), T Naka s.n. (TI), F. e e (TD, M. Kimura s.n. Anon. s.n. (TI hon T. Sato Mizushima s.n. (TD), F. nomoto s.n. (TI), T. k MN d: be n, M. Togas (KYO, P), A. Ito s.n. (KYO); Shibukawa-shi, Inasa-gun, c J. Sugiki s.n. (KYO); Izu Peninsula, Mt. Togasa, H. Idzumi & M. Togashi s.n. ah P. ox M. Togashi (TNS), R. Morimoto s.n. S), "n Mt. — Hayashi s.n. as Ikeda s.n. (TL), Z. Sato n. (TI), F. Yamazaki s.n. (TI), M. Mizushima s.n. (TI); Kamo- pe Hissin oh Mt. Houkigi, 7. Sato 1843 (TNS). 2. Rhododendron chilanshanense degens Edinburgh J. Bot. 56: 75, m 1A—F. PE: China. Taiwan: Taipe Mt. dl shan, 22 Oct. 1992, ETOT 136 ole K not seen; isotype, TAIF!). Figure 2F Shrubs deciduous, to 2 m tall; young shoots with appressed filiform trichomes, later sparsely glabres- cent. Leaves chartaceous, scattered I upper shoots, ovate to ovate-rhomboid, 3.5—4.5 15 2 cm, acute with a gland at apex, cuneate at base, margins undulate or minutely crenulate, blades dorsally sparsely pilose, ventrally gl 7—11 mm, sparsely spreading pilose. Inflorescences 2- or 3-flowered; pedicels 5-7 mm, densely glandular and whitish pubescent. Calyx bowl-shaped, ca. 3 mm diam., sparsely villose and densely glandular, lobes buche corolla deeply reddish purple, broadly funnelform, 30—35 mm, deeply 5-divided, corolla tube 7-8 mm, lor on both surfaces, lobes oblong, 23— 27 X 1—8 mm, upper lobes with dark purple spots at base; stamens 10, rarely 8, unequal in length, 10— 22 mm, filaments glabrous, anthers oblong, ca. 2 mm; ovary ovoid, densely villose and glandular; style 20— 21 mm, with glands and mixed with sparse pilose trichomes on lower half. Mature capsules not seen. Distribution and habitat. Rhododendron chilan- shanense is endemic to Taiwan and known from Mount Chilan. It grows in mixed forest at 1600—1700 m a.s.l. Phenology. Rhododendron chilanshanense flowers in May (He & Chamberlain, 2005), with the flowers opening with the emergence of leaves (Kurashige, 1999). Discussion. No material was available to the authors, and this species was verified only from the line art cas in the protologue (Kurashige, 1999: 75, fig. 1). The author who described the species indicated that Rhododendron chilanshanense is similar to R. mariesii, which we refer to R. farrerae in synonymy; they share the same corolla shape and leaves that are broadest below the middle. n- dron chilanshanense was assigned to section Brachy- rous; petioles . calyx by Kurashige in the 1999 protologue by its mixed buds, monomorphic and deciduous leaves, and lack of strigose trichomes. From the 1999 figure and description, the s R. wadanum in the styles with dpi but differs in the ovaries being villose with glands and the styles being glandular and sparsely villose in the lower half, versus the ovaries villose only and the styles only glandular in R. wadanum pecies seems similar to 3. Rhododendron dilatatum Miq., Ann. Mus. Bot. pe 1: 34. 1836. TYPE: Japan. s. loc ., P. F. von Siebold s.n. (holotype, L not id Shrubs deciduous, 1.5-3 m tall; young shoots densely hirsute, later glabrescent. Leaves chartaceous, in a whorl of 3 (3-verticillate), ovate, broadly ovate, or rhombic-ovate, 2-5(-7) X 1 acuminate, mucrona —5) cm, acute or te at apex, cuneate or round base, entire, sparsely silky-pubescent on both e midribs glabrescent or sparsely villose dorsally, tertiary venation reticulate pn s 2-5(-8) mm, glandular or sparsely p nflorescence 1- or 2-flowered; pedicels pea mm, glandular and/or sparsely pubescenct. Calyx bowl-shaped, ca. 3 mm diam., densely to sparsely glandular, sparsely pubes- cent, calyx lobes inconspicuous; corolla pale purple to purple, rarely white, rotate-funnelform, 20-25 X 2. 30 mm, deeply 5-divided, corolla tube 5-7 mm, glabrous on both surfaces, lobes narrowly elliptic, oblong, or oblong-obovate, 15-20 X 7-11 mm, e obes with dark purplish or whitish spots, sometim without spots at base; stamens 5, or (8 to) 10, pl in length, 10-20 mm, filaments glabrous, anthers oblong, 1-2 mm; ovary narrowly ovoid or ovoid, pd glandular, sometimes sparse ent; s 30 mm. glabrous. Capsule obliquely cylindrical to dde, 6-10-13) X 3-5 mm diam., glandular; 0.9-1.9 X 0.4-0.7 mm. KEY To THE TWO SUBSPECIES OF RHODODENDRON DILATATUM IN JAPAN R. dilatatum subsp. dilatatum gland la. Stamens 5; ovary glandular onl 3a. lb. Stamens 10, sometimes 7 to 9; ovary mes 3a. Rhododendron dilatatum subsp. dilatatum. Figure 3A-F. Distribution and habitat. The typical subspecies of Rhododendron dilatatum is distributed principally in central Honshü, Japan. It grows on slopes, in thickets, and in forests at 300-1 172 Annals of the Missouri Botanical Garden A | ea Fi Moika ; A and ovary. m E riter Ro RM 9 ee B. Leaf, showing indumentum. —C. Stame s-an; D, E from Hara s.n.; F redrawn from lonis ion. n chilanshanense Kurashige. Style à and ovary. A-C from misi 173 Volume 97, Number 2 Jin et al. 0 Revision of Rhododendron sect. Brachycalyx i 3. A-F. Rhododendron dilatatum Miq. subsp. dilatatum. —A. Fruiting shoot. —B. Leaf, showing indumentum. —C. Flowering shoot. —D. Stamen. —E. Style and ovary. —F. Capsule. G, H. Rhododendron dilatatum subsp. decandrum (Makino) X. F. Jin & B. Y. Ding. —G. Flower. —H. Style and ovary. A, B, F from J. Murata 11402; C—E from X. F. Jin 1408; G, H from X. F. Jin 1415. 174 Annals of the Missouri Botanical Garden Phenology. Rhododendron dilatatum subsp. dila- tatum flowers from mid-March to mid-May, opening before or with the leaves. It fruits from mid-September to October. The ees A of Rhododen- dron dilatum i ly t taxon in section Brachycalyx that has Die iaman. Additional specimens $ pis s Pref. Aichi: Minamishitara-gun, Horai-cho, Mt. Horaiji, G. Murata 41058 (KYO), Nanashi s.n. (TI); Mikawa, K To Torii s.n. (KYO, 2 Mt. Horaiji, T. Tashiro s.n. (KYO); Tomiyama-mura, G. Murata 7314 (KYO); Kitashi Toyone-mura, K. Torii s.n. (KYO). Pref. Chiba: Kimites-guti, Mt. Kame, Mt. Mitsuishi, G. Murata & K. n, Mino-city, 1, near uita, H. T & H. Takano diee RT. Mt. Kinka, J. Murata cope 02 m; Kamo-gun, Yaotsu-cho, Mi akahashi et 5222 (KYO); Gujo-gun, UNA NT cnn s. loc., K. Asano & K. 16261 (TI). Pref. Tano-gun, Onishi-machi, J. Murata 4643 (KYO), 662 (KYO); Tano-gun, Manba-machi, J. Murata et al. 835 KYO% Tanpa; Bala Nakazato- Mt. Kanoo- & K. Asano 7568 (TI) sm Okawara-Sanpukutoge Saito s.n. (TI; Usuitoge, m DE Fins ' machi, Nakayama s.n. (TD; Taio- M š Pref. Shizuoka-city, Ikawa Lake, J. Saugimoto et ° 14 mS 32 2 KYO} paler e Se Sangochi to ux E al. 71 v ding. e Ooya River, from Eb £ Miki 16 (KYO); Shizuoka-city, Maganji to inge E. ao 28 (KYO); Shizuoka- uji-gun, |. Kanai s.n. (TT); pg Sakuma-machi, H. Kanai et a s.n. (TI): Sibukoma, T. Yamazaki 3886 3886 (TT); Mt. Ogasa, T. Tashiro s.n. rae Š T s n. (KYO); Shita- = E O), T. Tashiro ` D . Tokyo: a -gun, d Mt. Tenso, 1169 (KYO). Pref. nobu- cho, Mt. Minobu, N. Kurosaki 12992 (KYO); Minamikoma- — gun, Nanbu-machi, Mt. Tenshi, Y. Tateishi et al. 4578 (KYO, TI, oe Y. Quadota et al. 4592 (TI); EE G. n. (KYO); Minamikoma-gun, Nambu-c ozari, J. odis et al. o (TD, Y. Quadota et al. 1599 (KYO); Minamitsuru-gun, Yamanakako-mura, M. Togashi s.n. (KYO, TNS), M. Tagashi s s.n. (KYO); Minamitsuru-gun, Kawagu- chiko-machi, Yakemage-hara, N foot of Mt. Fuji, N. Kurosaki 3501 (KYO); Minamitsuru-gun, Mt. Mitsutoge, T. Shimizu sn. (KYO); L L Oshino-mura, Uchino, M. Togashi s.n. (KYO); Minamitsuru-gun, Nambu-cho, Kozori, z Quadota et T P (KYO); n M. "Tog ashi n. (TD; Kofu-city, from. Anaguc Obina, N. Fukuoka 8159 (KYO); MT Madii. J. Murata et al. 5585 (TI), H. Kanei s.n. (Tl); Kai, Nakakoma-gun, Aaiyasu- rate T. Yamaziki 3223 (TI); Kai, H. Kanei s.n. (TI); pa Minamitsuru-gun, Oshino-mura, Uchino, M. Tog ashi (KYO); Tsuro shi, Mt. Kuki, T. Yamazaki 794 (TI); Kista gun, Hatsukari, H. Kanai 9413 (KYO, TI); Yamato-m from Ohkura-zawa to Komeshoi Pass, T. Yahara et al. 5038 (KYO); Fuji, Mesias S. Watari s.n. (TD. Shikoku: Pref. ime: Uma-gun, Beeshiyama-mura, Mt. Higashiakaishi, Kazumi Tsuchiya 536 (KYO). 3b. Rhododendron dilatatum subsp. decandrum (Makino) X. F. Jin & B. Y. Ding, stat. nov. Basionym: ndron dilatatum Mig. var. decandrum mens PR. Mag. (Tokyo) E ipinm pps Rhodo- p. Bot. 1: 21. 1917. TYPE: Japan. Shikoku: B e Ochi, Apr. 1887, T. Makino s.n. (holotype, TI!; isotype, MAK not seen, MAK photo!). Figure 3G, H. on decandrum (Makino) Makino f. pm H. Bum Enum. rarae ophytarum cale 29. 1948, syn. nov. Rhodode. ilatatum Miq. var. lasiocar- pum (H. Han) T. Vice. Fl. Jap. (Iwatsuki A a eds.) (ed. 2) 3a: 1993. TYPE: Japan. Honshú: Pref. Wakayama, pea Mt. m 27 Apr. 1935, S. Okamoto s.n. ARES KT On. Rhododendron decandrum Makino var. dore H. Hara, Enum. Spermatophytarum Japon . TYPE: Japan. Honshú: Pref Mie, gr nam i T. Magofuku n. (holotype, TI!). Rhododendron Miq. var. satsumense T. Yamaz., J. Jap. Bot. 56: 363. 1981. TYPE: Japan. Kyushu: Pref. c Tatakumayama, cult. Tokyo, 1 Apr. 1980, T- amazaki 2534 TI (holotype, 1). H. Hara, J. Jap. Bot. 49: 353- 1974, syn. nov. = nd: dilatatum M greet synonym ron boreale Sugim., Ñaw Keys Woody e P. (ed. N “509. 1972, nom. illeg. TYPE: Japan. kkaido: Hidaka, M vicc pin 11 Sep. 1974, H. ^R et al. s.n. (holotype, TI H 1939. TYPE: Japan. Shikoku: Pref. Tokushima, 1939, N. Inobe s.n. (holotype, TI). Volume 97, Number 2 2010 Jin et al. 175 Revision of Rhododendron sect. Brachycalyx — osuzuyamense T. Yamaz., J. Jap. Bot. 59: 208. 984, syn. nov. vec eros ndron s Miq. e Sci. Rep. Yokosuka City Me rs P Rhododendron viscistylum Nakai var. glaucum E) Sugim., New Keys Woody Pl. Japan (ed. 2): 509, 1972. TYPE: Japan. Kyúshú: Hyuga, Osuzu, S. Sako 3384 (lectotype, designated here, TI EET a Nakai, Bot. Mag. (Tokyo) 49: 498. 1935, syn. nov. Rhododendron dilatatum Miq. var. L ecu Hatus., Sci. Rep. Yokosuka City 969. TYPE: how. es Pref. — Ti m 5 June 1932, J. (holotype, TI!). Rhododendron viscistylum Nakai var. amakusaense T Yamaz., J. Jap. Bot. 59: 208. 1984. ME amakusaense (Takada ex T. Yamaz.) T ax. 5, Jn. Bot. 62: 72. 1987. TYPE: Japan. m ish. hago 24 Aug. 1978, K. Takada s.n. (holotype, TI!). hododendron viscistylum Nakai var. hyugaense T. Yamaz., J Jap. Bot. 59: 208 L oc n hyugae amaz.) T. Yamaz., J. Jap. Bot. 62: 72 pes aaron Japan. Kyüshü: Pref. x Koyugun, Nish Shiono, 11 Sep. 1978, K. Takeda 89101 kaa KYO!; isotype, TI!). Calyx densely to sparsely glandular, sparsely pubescent, calyx lobes inconspicuous; corolla pale purple to purple, rarely white, upper lobes with dark purplish or whitish spots; stamens (8 to) 10, unequal in length; ovary densely glandular, sometimes with sparse pubescence. Capsule obliquely cylindrical to oblong-ovoid. Distribution and habitat. Rhododendron dilata- tum subsp. decandrum is found from Kyüshü to entral Honshü provinces, as well as in Hokkaido (Hidaka), Japan. The subspecies is widely distributed in western Honshū and Shikoku. It grows in thickets, in forests, or on slopes at 100—1400 m a.s.l. Phenology. Rhododendron dilatatum subsp. de- candrum flowers from late April to mid-May, opening before or with leaf emergence. It fruits from mid- September to mid-November. . Subspecies decandrum differs from ndron dilatatum subsp. dilatatum by having twice as many (10) stamens (sometimes wi seven to nine). The ovary is covered with glands and is sometimes sparsely pubescent. The distribution area of subspecies Iud is more southern than that of the autonymic subspecies. Because these two infra- specific entities of R. dilatatum differ in both morphology and distribution, the infraspecific status is changed here from variety to su les. According to Articles 37.1 and 37.2 (with Art. 8.1) of the International Code of Botanical Nomenclature (McNeill et al., 2006), a name published after 1 anuary 1958 is not m en if more than one collection is indicated as ndron dilata- tum var. glaucum was not validly published because two collections, S. Sako 3384 and S. Hatusima & S. Sako 31427, were designated as types. This name was combined as R. viscistylum var. a in 1972 and replaced with R. osuzuyamense in 1984. It can be easily identified by the leaves beta whitish green abaxially, and the collection S. Sako 3384 is more accordant. Herein, this collection is designated as the lectotype for the formal application of these names. Additional specimens examined. JAPAN. Hokkaido: ver Hidaka: Syoya, Mt. Maru, S. Kurosawa & Y. Tateishi n. (TD; Hidaka, ig n F. m Togashi s.n. (TT), Y. Jokuhuchi s.n. (TI). H yogo: Isl. Awaji-shima, Sumoto-city, Sinya ey 6330 d N. Fukuoka & N. “upaqa 1575 (KY0); Tsuna-gun, S. Hosomi 13746 (KYO). Pref. Mie: Ise-shi, Keane G. rici 19503 e = Mt. Yuno, G. Ki a a Nakai s & S. EN. s r jus oki-goya to Fudonotaki, Y. en 7268 (TD; atarai-gun, Nan: i- -> Y & 5. Ki ma s.n. (TI); , Kawakami, T. Magofuku s.n. (TI; Komoto, Mt. Yuno, Yoshii et al. s.n. (TI); Ise, p Mt. Yuno, — et al. s.n. (TD); T T E Hara s.n. (TI); Mt. Ohdaiga f. Nara: Tab Shimokitayama-mura, G. Murata et al. 19 (KYO); Yoshino- Mt. Oomine, G. Murata et al. 37315 (KYO); Yoshino- , Kamikitayama-mura, asamata to Mt. Daihugen Murata 22244 (KYO), 22241 (KYO); n Inter Mt. Sanjogadake and Kotako, C. Murat ata & K. Iwatsuki 88 (KYO); Mt. Im 5 Yamaz 10128 (KYO). ragi Kuwashima s.n. pos Izumisano-shi, T. Tashiro s.n. (KYO). Pref. Shiga: Gamou-gun, Kiakake, S. Kitamura s.n. (KYO); Gamou-gun, Mt. Watamuko, T. Tashiro s.n. (KYO), . Hashimoto s.n. (KYO); In pi s.n. ; In & Hongu-cho, N. Naruhashi 1726 (KYO); Arida-gun, Okamoto 7153 (TI); Arida-gun, Shimizu-cho, Okamoto s.n. (KYO); Higashimuro-gun, Kitayama-m Kanei s.n. (TD. ü: Pref. Kagoshima: Ohsumi, Takak Kyü Idzumi & M. Togashi s.n. (IBSC, P, TNS), F dieit 24542 s T: sag T. Tashiro s.n. (KYO); Imuda-ike, n. (TD, G. Koidzumi s.n. (TI); uS UE L pru, s.n. (KYO); s. loc., K. Maruno 19238 (TI). Pref. qnd Koyu-gun, Nishimera-mura, S. Mitsuta 12504 (KYO); Koyu-gun, Kijo-cho, Ryuma, T. Minamitani 29417 n 29499 (KYO); Koyu-gun, Kijo- cho, Matsuo-dam, 7. ce ee 29394 (KYO); Koyu-gun, Kijo-cho, Mt. € e f: n 1429 (HZU), 1432 (HZU); i -gun, Yok Takada 89 106 (KYO), 89104 (KYO), 89102 «vo, i as (KYO); Nishimera-gun, Mamako-da Minamitani 29348 (KYO), 29351 (KYO); E Mt. Kamon-dake, T. Minamitani 30251 (KYO); Higashiusuki-gun, Mt. Ohkue, 7. Minamitani 28076 KYO). Pref. Oita: Saekishi, Ohgoshi, f. Ehime: creme , Y. Nomura 14 (KYO): Ó— q. y. Nomura 20 (KYO); Kitauwa-gun, J. Murata 15046 (TD, Annals of the Missouri Botanical Garden — Uwajima, T. Tashiro s.n. (Tl; Kamiuk Kuroson, S. i, Anon. s.n. (TNS); Engyouji, i Kamiyama 45 (TNS); Naka-gun Kisawa-mura, Ç. al. 56050 (KYO); Mt: Ikedatyou-cho, s. e 1379 (KYO). 4. farrerae Tate ex Sweet, Brit. Fl. Gard. ser 2(1): tab. 95. 1831. Azalea farrerae ie ate ex Sweet) K. Koch, Dendrologie 2(1): 178. PE: tab. 95 in Sweet, 1831, based on “a d plant introduced from China by Capt. Farrer in 1829" (holotype, Sweet, 1831: tab. 95). igure 4. ndron cinereoserratum P. C. Tam, Bull. Bot. Res., Harbin 2(4): 77. 1982. TYPE: China. ume Nanjing Co., saei ¿ U!). Rhododendron dai Tam, Bull. Bot. Res., Harbin 2(4): 78. 1982 e yuenshanicum P. C. Tam, Save. Car Moimi & China 9 962 t. 22: 3. 1983, nom. illeg. superfl. TYPE: China. Fujian: Dehua Co., - Daiyunshan, 20 Apr. 1975, L K. Ling 3140 (holotype, FNU!; isotypes, FNU[8}}). farrerae Tate ex Sweet var. Franch., J. Bot. (Morot) 9: 394. 1895. TYPE: China. Sichuan, E Sichuan, 1892, P. Farges 846 (lectotype, designated here, P!). Rhodode gnaphalocarpum Hayata, Icon. Pl. Formosan. 3: 132. 1913, syn. nov. TYPE: China. Fujian: Isan, 1910, T. Nagasawa 239 n. —— Makino, £ jep: Bot. 6: 18. 1929, ig. var. kiyosu- mense r (Makino) Hatus., Sci. Rep. Yokosuka City Mus. a 22. 1969. TYPE: voie nei Shikoku: Pref. Awa, Mt. ivosumi, 1929, t zo by Yamazaki, ae. 113, peso io pen i. Bot. Mag. (Tokyo) 40: 483. 1926, sy — = elo (Nakai) H. Hara, Enum. Sperm. Jap. 1 1948. Rhododendron reticulatum D. Don ex G. "totins var. lagopus (Nakai) oe Sei. Rep. Ys City Mus. E: Japan. Honshü: 15: 22. 1969. TY Mt. Daisen, 9 nov. TYPE: China. Hubei, Apr. 1900, E. H. Wilson 29 ectotype, ; Pl: isotypes, A not seen, E Zhejiang: Qingyuan, Zuoxi, 23 Apr. | 1984, B. Y. Ding & € M. "Cai 3825 (holotype, HZU!). mayebarae Nakai & H. Hara, J. Jap. Bot. 11: 825. 1935, syn. Nak var. silat chess he H. Hara) Kitam., Acta Phytotax. Geobot. 25: 37. 1972. Rhododendron viscist viscistylum Nakai var. mayebarae (Nakai & H. Hara) Sugim., New Keys Woody Pl. Japan. 509. 1972. TYPE: Japan. Kyūshū: Pref. Higo, Mt. Kurobaru, 24 ed 1927, K. Mayebare 2159 (holotype, TI!; isotype, ron mayebarae Nakai & Ë s var. ohsumiense T. Yamaz., J. Jap. Bo € e ERE 3 PL. Pref. oshima, — 21 iculatum D. Don ex p. Yakosuka City , Mt. Kicishimn, Sonoura, Aug. 1972, T Miwamisaai s.n. (holotype, TI!). ron nudipes Nakai subsp. niphophilum T. Y amaz., J. Jap. Bot. 56: 363. 1981, syn. nov. ndron lagopus Nakai var. — (T. Yamaz.) T. Yamaz., J. Jap. Bot. 63: 410. 1988. TYPE: Japan. Honshū: Oziya Shi, Oziya, euli, Tokyo, 18 May 1974, T. Yamazaki s.n. (holotype, TI!). Rhododendron nudipes Nakai var. tokushimense T. Yamaz., J. Rhododendro Jap. Bot. 56: 1981, syn. nov n m Nakai var. tokushimense (T. Yamaz) T p. Bot. 63: 410. 1988. TYPE: Japan. irem Pref. Awa, n Sasatoge, 14 Aug. 1941, C. Abe s.n. — n. pes Nakai var. tsurugisanense T. Yamaz., 2 J. Jap. Bot. 59: 1984, syn. nov s lagopus N var. tsurugisanense (T. Yamaz.) T. Yamaz., J ine Bot. 63: 410. 1988. Rhododendron tsurugisane Yamaz., J. Ja 66 . Bot. 125. 1991. "TYPE: € — Pref. Tokushima, Mt. Tokushimasan, 9 Aug. 1976, T. Yamazaki 1128 (holotype, T1) Nakai var. yakumontanum T. Yamaz., s.n. (lectotype, designated here, TI!). ron psi Don var. bifolium T. Yamaz., J. Bot. 62: syn. ° n reticulatum D. kia ae. Dos f: bifolium (T. Y amaz) T. Y , Fl. Jap. (Iwatsuki et al., eds.) (ed. 2) 3a: 37. 1993. TYPE: Japan. Shikoku: Pref. Oshima, Tokoshima, 13 July 1951, K. Abe 35670 ulatum D. Don ex G. Don var. ciliat arm syn. nov. hi, Yoshikigun. Higami, 17 June 1895, u "-— s.n. LC. TH; isotype, TNS)). Rhododendron reticulatum D. Don ex G. Don var. parvifolium Man, ee a Rhododendron D. parvifolium (T. Yamaz) T. vides FL i da O : Nakai, Bot. Mag. Tokyo 40: 484. 1926, G. Don - Volume 97, Number 2 2010 Jin et al. 177 Revision of Rhododendron sect. Brachycalyx ph Figure 4. A et al., eds.) (ed. 2) 3a: 37. 1993. De Japan. Shikoku: Tosa, Takaokagun, Kiyama, 21 Oct. 1942, T. Yashi- naga s.n. (holotype, TI). n reticulatum D. Don ex G. Don f. trichostylum M. Mizush. ex Okuhara, J. Jap. Bot. 36: = 1961, syn. nov. TYPE: Japan. Honshü: agano, Kiso, Y hi, 22 Apr. 1956, H. dH s.n. (holotype MAR not seei, MAK photo oD). Mab 2- N. +, Fl pres ed. Venen & irc 890. 1931, syn. nov. TYPE: Japan. Honshü: Pref. Shizouka, Shidagun, Mt. Hanashi, 10 e 1930, D. Shimidzu 2 (holotype, TI!). Rhododendron farrerae Tate ex Sweet. —A. Flowering shoot. shoot. —E. Leaf, BE Fu aman —F. Caps Rhododendron, m H. Lév., PES Y [Z7 2 — = "UN B. Stamen. —C. Style and ovary. —D. Fruiting ule. A-C from X. F. Jin 1485; D-F from W. S. Jin & B. Y. Ding 3475. on shojoense Hayata, J. Coll. Sci. Imp. Univ. — 20: 174. 1911, € nov. TYPE: China. Taiwan: antou Co., 12 Aug. 1 Kawakami & V. Mori ; 160 e TI. ndron nse (T. Yamaz.) T. Yamaz. var. io atum T. Pd. J. Jap. Bot. 66: 125. 1991, — nov. TYPE: Japan. n Pref. Ehime, 12 June 983, C. Abe s.n. (holotype, TI Repe . Nov. Regni. Veg. 12: 102. 1913, syn. nov. TYPE: China. Guizhou: le 2 Apr. 1902, Cavalerie 10 (holotype, E not seen). Annals of the Missouri Botanical Garden Shrub deciduous, 1—4 m tall; young shoots hirsute, later glabrescent. Leaves chartaceous or thin-charta- ceous, usually in a whorl of 3 (3-verticillate), ovate, triangular-ovate, oblong-ovate, elliptic, or rhombic, (1.5-)2.5-7(-9) x (1-)1.5-5 em, acute and mucronate at apex, cuneate or rounded at base, entire or sometimes minutely denticulate at margin, villose or silky pubescent on both surfaces, glabrescent or densely to sparsely villose on dorsal midrib, and reticulate on dorsal surfaces; petioles 2-10(-20) mm, glabrous or densely to sparsely villose. Inflorescences l- or 2-flowered; pedicels 5-10(-12) mm, with brown villose indument. Calyx bowl-shaped, ca. 3 mm diam., densely pubescent, lobes inconspicuous; corolla pale purple, pink, lilac-purple, or purplish red, rarely white, rotate-funnelform, 22-35 x 30-40 mm, deeply 5-divided, tube 6-10 mm, glabrous on both surfaces, corolla lobes elliptic, oblong, oblong-lanceolate, broad- ly oblong, oblong-obovate, or obovate, 15-20 x 8- length, 10-25 mm; filaments glabrous; anthers oblong, 1-2 mm; ovary ovoid, densely villose, style 25-35 mm, - Capsule obliquely oblong-ovoid to cylindri- cal, 10-15(-18) mm, 4-5 mm diam., densely to sparsely hirsute; seeds 1.1—1.8 x 0.5-0.8 mm. Distribution and habitat. Rhododendron farrerae is distributed from the southern Yangtze River in ina across the provinces of Anhui, Fujian, Guangdong, Guangxi, Guizhou, Hebei, Henan, Hong Kong, Hubei, Hunan, Jiangsu, Jiangxi, Shaanxi, Sichuan, Yun ji grows in mixed forest, under forest, or on slopes at 50-2100 m as.] Phenology. Rhododendron Jarrerae flowers from late March to mid-May, with the flowers openin before or with the emergence of the leaves. I fruits from September to November. Discussion. Rhododendron Jarrerae is a common species in mountainous regions adjacent to the at forest Margins, 2005). We examined one population of 70 individuals in Zhejiang, China, and these Specimens demonstrate that the Species vary greatly in both leaf size and indumentum from glabrate to pubescent forms. No other morpho- logical distinctions were *vident, and it is difficult to distinguish R. mariesii from R. farrerae. Furthermore, xÇ the geographic range of R. mariesii is from Hebei to. Guangdong and Guangxi, while that of R. farrerae i from Jiangxi to Guangdong and Guangxi. Because f the morphological similarities and because the geo- graphic range of the two species overlaps in the : provinces of Jiangxi, Fujian, Guangdong, and Guangxi x (He, 1994; He & Chamberlain, 2005), R. mariesii is 1 i placed here as a synonym of R. farrerae. 1 Tam (1982: 78) described Rhododendron daiyuni- cum and indicated that this taxon differs from R. mariesii in having distinctive calyx lobes 5-6 mm in x length and evergreen leaves. The holotype and eight isotypes deposited at FNU show that the calyx lobes are inconspicuous and that leaf persistence sometimes 1 also occurs (e.g., Lou & Li 67, Linou collector 82075). 1 He (1994) and He and Chamberlain (2005) reduced R. I daiyunicum to the synonymy of R. mariesii, and herein a this name shifts to the synonymy of R. farrerae. U In Japan, the species entity Rhododendron Jarrerae has been subdivided into multiple taxa. Miquel, Makino, Nakai, and Yamazaki described R. reticula- tum, R. mayebarae, R. nudipes, R. lagopus, and other infraspecific taxa based principally on leaf shape, the indumentum of petioles and leaf surfaces, the reticulated pattern of veins on the abaxial surfaces of the leaves, and the presence of minute teeth or denticles along leaf margins. We do not find these differences to distinguish these infraspecies from R. farrerae. on farrerae var. leucotrichum was de- in the protologue. Consequently, the name of this variety is not validly published according to Articles 37.1 and 372 of the International Code of Botanical. Nomenclature (McNeill et al., 2006). The two syntypes were preserved at P, but we were only able to examine P. Farges 846. To validly publish this name, the collection P. F, arges 646, which is in good condition, is designated as the lectotype. Similarly, Rhododendron mariesii was not validly published because six collections were cited as types- Within these collections, Wilson 29 at P is in good condition, and several of its duplicates are preserved in A, E, and W. We here designate the collection of Wilson 29 as lectotype and the remaining collections as paratypes. ; was described by Don (1834: 846) as a new species, but Don indicated that Neither a collection nor an illustration was cited as Lype by G. Don and D. Don in the protologue, and a lectotype must be designated in order to validly establish R. rericulatum and its infraspecific taxa. Don Volume 97, Number 2 2010 Jin et al. 179 Revision of Rhododendron sect. Brachycalyx only recognized this species with reticulated leaves, but without any flower description. The collection F. amazaki s.n., which is preserved at TI, has ine leaves and a few flowers, and it is designated here as the lectotype. nal specimens examined. CHINA. Anhui: Guichi, Additio Meijie, Anon. 7400 (NAS). Huangshan, Mt. Huangshan, — — 1870 (NAS), W. H. Tsu 66 (NF), S. S. Chien 1253 (W). Huoshan, Majiahe For. Farm, Bot. Res. Exped. 456 (PE), 478 (PE). Qimen, s. loc., M. B. Deng et al. 3218 (PE), 4964 (NAS). Qingyang, Mt. Jiuhuashan, Anon. 5518 (NAS), A. N. Steward 1133 (N). Shexian, Shanyang, Anon. 1805 (PE). Shucheng, Mt. Wanfoshan, M. B. Deng & J. Fang 11012 (PE). TI. Changting, Hetian, S. S. You s.n. (FJFC); Yanghou, L. K. Li 75006 (FMP); NUMEN Anon. ishan nyuan, Q. 598 Jianning, Mt. Ra Mt. Renshan, For. Coll. Exped. 82075 (FJFC). EE Ro T. S. sie 1123 (FNU). oo Boping, T. S. Wan, d Jiumu, G. S. He 1717 (PE). Wout 56 (FNU); Baofu, C. Hoo 1982 (FNU); n, G. S. He 1473 (PE); s . G. S. He 9884 (PE), 1429 (PE). Pingnan, s. em G. Y. P 889 (FNU), 909 (FNU). Shanghang, Tiechang, Y. Ling 4087 (FNU); Buyun, Q. Q. Zhang s.n. (FNU), Q. Q. n "w pee i Ling 4135 (FNU); Guanfuban, L. 6 (PE); Chucaodong, Y. Ling 4087 (PE). as das . S. He 115 (FNU); s. loc., P. Lin 10163 (FJFC). Shaxian, Mele, P: C. Tsoong 903 (FNU, PE); Jiulidong, P. C. Tsoong 881 cg 927 Res PE E Tiantaishan, M. S. l & Z. E; M DS Ti & Z. Y. i 6552 E oda E “s 48 (PE). Yong'an, Luof. Foca e 53 (FJFC); Shangping, Anon. 11 uu e a : Boluo, pigeon River T Y. F. Deng et al. 15684 (PE): Mt. A eg > x Chun 40884 (PE). Conghua, Longmen, Mt. Sanjiaoshan, W. T. Tsang 20507 (IBSC, N, NAS, P, PE); Wenquan, S. H. Chen Fengshun, Dati PE); Guangan, Mt. Fengbianshan, P. E Tam 7332 (IBSC ansha 8778 (P). Huaiji, Mt. Dachouding, £ C. Ng 2997 (PE). e si Mt. Lianhuashan, W. T. ong, 25645 (BSC): Chang'an, Z. F. Wei 121595 (PE). Huidong, Pingshan, P. Y. Chen & B. H. n 195 (IBSC). Jiaoling, Shihu, L. Teng 4674 (IBSC). Lechang, Jiulongkeng, N. K. Chun 42389 (IBSC); Honglisakeng N. K. Chun 42111 Pingshi, Banshang, S. Chen 226 (IBK, IBSC). tied Mt. Wuzhishan, S. : Lau 4500 (IBSC). Meixian, Yingjia, Mt. Yinnashan, W. Tsang 21412 idend op "ae Dakou 7324 (IBSC). X. G. Li 201931 c " Zouhuang, L. f 4157 (BSO). Feilaish; S. H. Jin & J. Xu QY-002 (HTC). Qingyuan, Mt. Xianxiadong, S. W. (IBSC); Feilaishi, C. Le 3 Taiping, N. K. Chen 42602 (IBK xi P. Ko 52581 (IBSC, KUN, NAS, PE); Shangshan : 53312 (IBSC, KUN, PE, SZ). Shenzhen, Shajiaotou Forestry Farm, Mt. Wutongshan, W. C. Ko & B. H. Chen 347 ae Nan'ao, F. W. Xing 10360 (IBSC). Wuhua, Changbu, Mt. Qimuzhang, X. c Li 201579 x PE). Xinfeng, Mt. Yingde, Mt. Hua- : Binyang, Silong, Binyang Exped. “iy 1 ET Bobai, Santan, = ws ng 463463 (1 n, Mt. Yaoshan, (IBSC), 404 (IBSC). Guilin, m smi, e s Ee 155 (IBSC), S. L. Huang 20006 (IBK), S. Q. Zhong (IBK). Guiping, s. loc., N. K. Liang 10873 ce Hes, Xishan, L. X. Chen 500044 (IBSC, LB Pe t al. 500044 (IBK). Huanjiang, Dongxing, Peking Exped. 894038 (PE); Jiuren, Peking Exped. 895118 (PE). Jinxiu, Liugang, Mt. Shengtan n Exped. 12440 (IBSC), B. Y. Ding & Y. P. Chen 7617 (HTC); Mt. Lianhuashan, 14469 (PE); Mt. Laoshan, G. Z. Li 14502 (PE); s. loc., J. Y. & Z. H. Ps 512-67 (GXMI). Lingui, Chaotian, C. F. Liang 30241 (IBK), L. Q. Chen 94593 (IBK); Mt. Qifenshan, Anon. 53796 (IBK), C. F. Liang 31364 (IBK); Wantian, C. F. Liang 31615 (IBK). eng, Dadi, Mt. Hongyashan, Guangfu For. Exped. 147 (IBK, IBSC, PE, SZ), 204 (IBK, PE, SZ); Huaping, Anon. 272 (PE). gioi Mt. r... €: Ching 6088 (PE). Nandan, Yueli, Hualian C. Mo 8 (GXMD). Pingnan, Mt. Yaoshan, C. en 39207 e» IBSC), 39153 (IBK). Quanxian, Shanchuan, C. H. Tsoong 82036 (IBK, IBSC); Mt Baodingshan, C. H. Tsoong 81621 (IBK). Rongshui, Mt. Damiaoshan, Mt. J E 16418 (IBK, KUN, PE); Mt. Jiuwanshan, Paling Exped. 892482 (PE). Shanglin, Mt. Damingshan, S. F. Yuan 6508 (CDBI, -— C. S. Tsia 5397 (IBK); Shanglin — Farm, S. F. Yua ming, Mt. Damingshan, C. S. Tsai 5397 (BSC), D. Fang & D. H. Qin 24526 (GXMI); Matou, G. = LI (IBSC), G. Z. Li 1 any 2. 2: e 51407 (IBSC, KUN, PE), Guangxi em 690 (PE ). Yangshuo, Yuanda, Mt. Changyushan, H. F. Qin 700171 (IBK). Žij ip cil: Z. = Wei 120934 (IBSC, KUN, PE). Ziyuan, — mr C. g ( ). Guizhou: Huangping, Pingxi, R. E Li 1562 (GZTM). Jiangkou, Macaohe River, z `s. Zhang 400359 (HGAS, IBSC), 400454 m" Mt. Fanjingshan, — Exped. 796 (KUN, PE). Kaili, Mt. Leishan Guizhou Exped. 1525 (NAS, PE), 3893 (PE); Woles š Guizhou Exped. 1042 (HGAS, NAS), N. Guizhou Exped. 879 (HGAS, KUN, PE); Fangxiang, C. = Tsien et al. 51101 (KUN). Pingfa, Mt. Yunwushan, D. . X. Ji 443 ( ). Qingzhen, panzi, Sichuan-Guizhou Exped. 2210 (PE). Shibing, Maxi, Mt. oe Wulingshan Exped. 2565 (KUN, PE). Shigian, Jiuchashu, Wulingshan Exped. 2779 (KUN, z Songtao, Ti Farm, Wulingshan Exped. 51 (KUN, PE); Muerxi, N. Guizhou Exped. 1839 (HGAS, IBK, KUN, PE). Tongren, Yangtou, Jiulongdong, Wulingshan Exped. 1570 (KUN, PE). Wen'an, Bip. Libo poma 2019 (HGAS, KUN, PE). Xiashun, s. loc., Z. X. Zhao E Yinjiang, Mt. Fanjingshan, Anon. 46 (NAS), N. Exped. 90 (HGAS), B. Bartholomew et al. 1723 (PE); Xie S. Guizhou Exped. 31805 (HGAS); a Guizhou Exped. 32210 (HGAS); s. loc., N. Guizhou Exped. Annals of the Missouri Botanical Garden E d Hebei: Changping, Chengyucheng, P. C. n. (PE). Lingnan, Heloudou, W. T. Wang 2065 (PE), n. Anon. 2027 27 (IBSC). Henan: Lushi, hi.’ Wulichuan. Minglanghe River, Anon. 34158 (PE). Songxian, Shifang, Henan Exped. 2191 (NAS, PE); Xiqi, Xiaman, Henan For. Bureau 969 (PE); Miaozi, fleni me 1834 ag deme s. loc., Bot. Exped. 20201 (PE). H ong: onshan, S. Y. Hu 5122 (IBSC), 6378 PE). V Victoria ses n Y. Hu 11603 (IBSC); Jiutiaokeng, N. K. Chun 42600 (IBK); s. loc., Wright 1 E Hu 6654 (PE Badong, Xiagu, Bot. Exped. 24600 (PE); Siyangqiao, H. C. Zhou 622 pn s. E HC. L. Y. Dai & C. H. Qian 1037 (PE), 1453 PE). uev W. B. Lin 361 (PE). Wanxi odaoxi, T. C. Hwa 275 (PE). Xingshan, s. loc., C. M. Hu 1014 (LBG); Mt. Tianzhushan, Y. Chen 850 (N). Xuan'en, an, 904 (IBSC); Yujiazui, X. G. 203966 (IBSC); d W. Hunan Exped. 42 (PE). e Zhushitou Forestry Farm, T. R. Cao 84385 (NF). Dayong, Zhangjiajie, Central-. South Fot. Coll. Exped. 31021 (IBSC); Zhangjiajie Forestry Farm, L. H. Liu 762173 (HNNU). Dongkou, Nakou, P. C. Tom 62806 (HNNU, pre 62812 (IBSC). Guidong, Xiaowuxi, T. R. Cao 5 (NF) (I E Liu 1814 (PE); Tw B. = Yang 2125 "E Nanyue, Cangjingdian, Y. i , PE). Ningyuan, Mt SC, PE) himen, m sche Hupingshan 57 (PE); Xiaoxi, Hupingshan Exped. 1286 (PE), 87376 (PE); _Jiangpin ng. Hupingshan E. E) Mangshan, Liang 83479 (IBSC), M. X. H 112740 (HNNU, s m Pingtoushan, W. T. Tsang 23468 (W); Meitian, P. C. Tsoong 656 (PE); Mt. Genshan, Z. C. Luo 1289 84 (IBSC, PE); Muyexi, Wuli SC, PE). Zixing, s. loc., P. H. Liang 85921 iban, Anon. eq 2044 (N); Mt. Konggiagshan, F ng, ijingshan, G. N. Chen 8742 (W), S. X. Yang et al. 411 (PE); ixiashan, Herbarium 160 (IBK, LBG, NAS), C. Y. [o (N, PE). n Mt. Taipingshan, Anon. 3576 (NAS), H. B. Zhou 2082 (IBSC, PE); Mt. Shangfangshan, H. Migo s.n. (PE). Wuxi, Mt. Yéxidianishah, H. B. Zhou 2541 (PE). Wuxian, Guangfu, W. Z. Fang et al. 117 (NAS, PE), 5. X. Sun & P. P. Ling 14 (KUN). Xishan, Mt. Baoshan, W. X. Wu 4031 (IBSC). Yixing, Mt. Panshan, F. X. Liu 1905 (NAS); Mt. Longchishan, S. H. Mao et al. 122 (KUN, LBG, ps PE), Y. L. Keng 2372 (IBSC); Zhangzhu, C. Y. Luh 361 (NAS); Huhou, Mt. Shizishan, S. H. Mao et al. 266 (KUN, vi PE, SZ) henghong. Mt. beet t" age pes (NAS). : Anfu, Mt. Wugongshan, J. S. Yue 3417 (IBSC KUN, E Anyuan, Dujiang, C. M. Hu 2564 (IBK, IBSC, KUN, LBG), 2769 (IBSC, KUN, LBG, PE); Shuangmao, S. S. Lai et al. 165 sa See Mt. Sanbaishan, L. X. Ding 21 (IBSC); , Geao, C. M. Hu 2141 (LBG, PE). Dexing, Mt. bius (PE) Longshou, S. S. Lai et al. 348 (LBG Dagan S. S. Lai 43 (PE). Guangfe i. S. Lai 5950 (IBSC, KUN, LBG). Ganxian, Huangpodi, Z. Yang & K. Yao 1125 (IBSC, oh Xiaocha, Z. 2 Yu 1566 aa Guixi, Mt. Xiaolanggang, Shen & Hua (LBG). Jiujiang, Mt. Lushan, M. J. Wang 150 (NAS), H. š Hu 2392 (IBSC). Laicheng, Mt. Daluoshan, Y. Tsiang 10351 (IBSC). ngnan, Tuntou, Mt. Jiulianshan, Anon. 1358 (LBG). Nanfeng, Jiafeng, Mt. Jiafengshan, M. X. Nie 2483 (KUN, LBG); Changbi Farm Center, X. X. Yang et al. 650128 (PE); Sanxi, E = “q et al. 650454 (PE). Pun. pr Jiangx d. 2989 (LBG); Mt. Wugongshan Gao 1523 ( a e D. Chu & C. S. Chao 1240 2: eit Gaoyuan, Jiangxi Exped. 2989 (PE). Qianshan, Mt. Wuyishan, C. P. Tsien 400996 (FNU, PE), C. P. Tsien et al. 400787 me Mt. Huanggangshan, X. Q. Huang 235 oe Hao 890148 (NF); pun €. a Tsien et al. 4012 BG, PE). Shangrao, WM. & a N, LBG, PE). S chuan, Mt. da weishan, J. Xiong 4769 (LBG), 5106 (LBG). Wuning. Shimenlou, Y. C. Xiong 4138 (LBG); Yishan, S. S. Lai 2481 (PE). Wuyuan, Mt. Wugongshan, X. X. Yang 17381 (IBSC). Xinjian, in Forestry Farm, M. X. Nie 2026 (KUN, LBG); Mt. Mengshan, X. X. on 10302 (PE); Liushulong, Y. Lin 13451 (PE), 13452 (PE). Xiushui, Mt. Huangquanshan, J. IT 5982 (LBG); Baishagiao, Y. G. Mense — oe PE). wu, Luotang, Y. Lin 15038 (LBG); Di M. Tan T (B), Student Exped. 1119 BSC. E a (PE); heju, Danxi, Y. = 15287 (PE). Yongxin, Lianshan Farm eae S. S. Lai 969 (LBG, PE); Yunshan Farm Center, S. 5. Lai 2024 (PE). Zixi, Mt. Matoushan, S. S. Lai 2 F. Huang 14 (LBG); Niuyuan, M. J. Wang 2452 (IBSC Chenggu, Panlong, ae S M. Su 419 >. Foping; N. ugang, J. X. (PE). ger Pingding, M. C. e 220 (S2. Yangxian, ae Sar 10948 ee eer — o» ing Esped.9 96 ( (PE) from gongba to g. T. N. Lio P. C. Tsoo "(P Mt. Tashan C. S Niu 3105 (S2). Near es 869 (PE). Pingli, Mt. : Denis. near Niutoudi ndi P. Y. Li 1348 (NAS), Mt. Xishan, Q. H. He 1263 Houping, T. L. Dai 105783 (CDBI, KUN, NAS, ays v Volume 97, Number 2 2010 jin et al. 181 Revision of Rhododendron sect. Brachycalyx P. Fang 10083 (SZ); Yanmai, T. L. Dai 106775 NaS Yiziba, Baimuping, T. L. Dai 103986 (IBSC, NAS, PE, anshan, T. L. Dai 103 753 (IBSC, NAS); Taiyishan Exped. 610 (CDBI); Beiping, T. L. Dai 101574 (CDBI); s. = W. P. Fang 10083 (IBSC, PE), T. L. Dai 105449 (CDBI, SCFI). Fengjie, Longchi, H. F. Zhou & H. Y. Su 11824 über 109471 (IBSC, : apu C. Y. Cha 5632 (IBSC, NAS, PE, SZ), H. F. u & H. Y. Su 110734 (IBSC, PE); Vira; M. Y. Feng n (IBSC, KUN, Mes (IBSC, KUN, NAS), J. H. Xiong & Z. L. Zhou 93025 (IBSC, KUN, PE); Baiwuping, G. F. Li 60480 (N, SZ), 60475 (KUN, PE); Xiaohekanba, J. H. Xiong & Z. L. Zhou 91982 (IBSC, SZ), 93830 (IBSC, PE, SZ); Toudu uan et al. 300 apo ae Jinfoshan Exped. 223 (PE); Mt. Jinfoshan, G. F. Li 63681 (IBSC e Nanini = D. Pu & Y. L. Cao 899 Huangshui, F. D. Pu & Y. L. Cao 1141 (CDBI, PE); Yuchi, R. Chen 25 (CDBI, SZ). Wulong, Baima Forestry Farm, Pu & Y. L. Cao 303 (CDBI, PE). Wushan, Zhuxian, p H. Yang 57888 (IBSC, PE, SZ), 59910 (CDBI, PE, SZ); bopt H. Yang 65530 (CDBI, IBSC, KUN, PE). Wuxi, Hekou, P. Y. Li 2994 (NAS); Baiguo, G. H. Yang 58314 (IBSC, PE, SZ), D. P. He 57764 (SZ); Yuanfeng, K. L. Chii 1955 (PE). Taiwan: Taihoku, = $ s z = a a5 M = m B5 ° ta . E e š -> C pansh e "A: € Mt. S. Yandangshan, Anon. D12 (PE). Pujiang uo, Q. H. Zhang 3161 (ZJFC), L. G. MK s. E jos an, Shuanghong Forestry Farm, Anon. 725 AoE mr 6513 E Shangyu, Chenxi, Shangyu For. a 0275 (ZJFC). — Fengping, L. H. Lou et al. sy043 (ZJFC). Suichang, Dabei, M. L. Sheh et al. 555 (NAS); Dazhe, Zhejiang Bot. Exped. 25552 (HHBC, re Mt. Baimashan, S. Chen 1197 (SZ); Mt. Leaping ge Q. B. Cheng 3046 (ZM), F. G. Zhang & M. H. Wu 53 (ZM). Tai S. Y. Chang 2875 (IBSC); Pr Sid. Chang 3582 (IBSC, PE); Mt. Wuyanling, 5. Y. Chang 5617 (HHBC, KUN, PE), G. Y. Li et al. 579 (ZM); Yangxi, S. L Zhou 277 (ZJFC), Z. G. Mao 10262 (HHBG). Tiantai, Mt. Huadingshan, Zhejiang Bot. Exped. 27935 (NAS, PE), X. F. Jin 1473 (HTC); Mt. Tiantaishan, L. Q. Qiu & R. L. Lu 1938, 2066 (IBK); s. loc., G. R. Chen 2375 (KUN), G. L. Que 27935 G). Wencheng, . Bot. Exped. 046 (ZJFC), L. L. Pci et al. J8322-021 (ZJFC). Xianju, s. i. Anon. 45001 oh Aen 7816 gas mim s. loc., Agric. Exped. 93 1285 (ZJFC); Mt. use sup & L Zhou Jingshanshi, S. Che Yunhe, dive. $ Chen 2756 (SZ); Jisbus, Andi, s imer 983 (SZ). Zhuji, Shisidou, S. Chen 48 ( e, Mt anglangshan, C. S. Ding s.n. (ZJFC), F. M. Los took 177 care. JAPAN. o Pref. Aichi: Nagoya, S. Okuyama 344 (TNS). Pref. Chiba, Pref. eee Mt. Kiyosumi, H. Ohashi & Y. Ta s.n. D. . Gifu: Nakatsugawa-shi, garu 03 (KYO); Yoro-gun, Yoro-cho, H. T ‘aed et uL as (KYO). Mt. ee M. Honda s.n. (TI); Oniiwa, H. Funakoshi 641 (TI); s. loc., N. Kurosaki 7 (TI). Pref. Hiroshima: Yam ~Œ me mura, H. Kana 213 (TI; Sima-gun, Ago-cho, S. a et al. 939 (TI). Pref. Hyogo: Akou-gun, Kamigouri-c uoka 13893 (TNS); Mi kt shi, Todo. Shirimi-cho, G. Masa & H. Nishimura 657 (TI); Isl. dedi: -shima, T. Tu (TD. Pr Kyoto: P. Se H. Takahashi 1173 (TN E Maidzuru sugaru & T. Takahashi 24716 a, pa (KYO): Kamecka-shi, Hodzu-cho, Mt. Ushimatsuyama, S. Tsugaru et al. ti (KYO); Kocuskabi, Sogabe-cho, S. Tsugaru et al. 299 (KYO); Kumano-gun, emunt S. Tsugaru et al. 21372 (KYO); Kasa-gun, ias -cho, Bussoji, S. Tsugaru et al. 21958 (KYO); I -ike, Z Sao =a; (TD); Kitakuwata-gun, Miyamachi, i Tateishi & J. Murata 4156 (TI); Sakyo-ku, LI i kyoku, Oh y 6. PE N. Morimoto 3903 (KYO); Nara-shi, Ninni- kusan, M. Ito & E. Kinoshita 64 (KYO); x ino-gun, Kamikitayama-munm M. Ito 598 (KYO); hino-gun, Tenkaw. ra, H. a 1845 (P); Mt. ea Takada 79201 TD: oed, Mt. Katsuragi, H. Ohashi et al. 607 ). 606 E Pref. de ues a Min Per 13557 ram Ton e ee Yogo-machi, Y. Tateishi & T. Nemoto 12188 (TD. Shimane: Kanoashi-gun, Nichihara-cho, N. ery r. 15 (KYO) Hamada-shi, T. Fukuhara 7080 (KYO); Hikawa, Mt. Hanatakayama, H. Hara s.n. (TI). Pref. Shizuoka: Mt. Higane, H. Hara 4035 (PE); Mt. Amagi, T. Annals of the Missouri Botanical Garden Yamazaki 9502 (PE); Syuchi-gun Haruno-cho, Mt. Watake, G. Murata et al. 112 (P). Pref. Tottori: Misasa-machi, Mt. Mitoku, M. Togashi 10227 (KYO); Saihako, e K. Midorikawa 2246 (TY), M. Togashi s. E (TD; Mt. Daisen, N. dzumi & M. ER Yamazaki 1811 (TI). Pref. Wakayama: n Nachi, H. Hara s.n. (TI; Ito-gun, Koya-cho, T. Makino Pref. Yamaguchi: Yanai-shi, F. Tatsundo 5292 ZU Nagatoshi, Isl. pen T Saito 640 (B); Segen T. Koponen 1 (W). Pre anashi: Kohu-shi, Mt. Kitayama, H. Uemats 524 (TI). dE Pref. yir Bic ra py, Mi: easel, T. Yahara et al. 5513 (KYO); Mt. Homan, S. Saito s.n. Pref. Kagoshima: Isl. Yakushima, T. Tashiro s.n. (KYO), H. Ikeda & T. Yahara 254 (KUN); Ohsumi-hanto, | e, K. ; Mt. Shibisan, K. M 19915 (TT). 19916 (TI). Pref. Kumamoto: Higo, Mt. Ichifusa, K. Takada 24113 (TI), K. A 2419 (TI), 2418 (TI), S. Yamaguchi . Pref. Miyazaki: Higashiusuki-gun, Mt. Tsunodake, G. Murata 67881 (KYO); Higashiusuki-gun, Mt. Shiraiwa, T. Shimizu 3475 (KYO), X. F. Jin 1437 (HZU); Nishiusuki-gun, n. (TD; Higashi taga machi, K. Inoue 1109 (TI), 1129 S T rs H. Idzumi & M. Togashi s.n. (TI), S. guchi 6892 (TT); Nishimorokata-gun, K. Takada pe m. Nishi-gun, d mura, > Takada 22356 (TI). Pref. Shi gun, Mitoshima-cho, Mt. Shitodake, jo Hotta s.n. (KYO), Shi RE Izuhara-cho, Isl. Tsushima, E. Mii 847 (KYO); Shimoagata-gun, Isl. Tsushima, H. Ohashi 299 (KYO); Mt. Inasayama, S. Saito s.n. (TI). Pref. Ni par Minamikanbara, Takasi & F. Yamazaki 9400 (TI); Kitawno- hikanbara-gun, Yahiko- T Yonmok 3167 (KUN). Pref. Oita: imoke-gun, ci Mt. prax G. Te 45530 E 0); v Himnka-yama, F. oku: Pref. Ehime: Uma-gun, Mt. re es M. m 10778 (KYO); Siea ity, Mt. Ishizuchi 4876 (KY0), H. Hara s.n. (TI; i a Kami-gun, -mura, Mt. Ishitate, N. Kurosaki 7397 (KYO); Tomiokamura, sutsujosan, G. Murata & T. Shimizu 848 (KYO); Mt. Rokko, T. Makino 82304 1 (TI). Pref. Tala Naruto-city, H. Koyama & G. Murata 4183 (TNS). 5. Rhododendron quinquefolium Bisset & S. oore, J. Bot. 15: 292. 1877. Azalea quinquefolia ae & S. Moss) Olmsted, Coville & Kelsey, Stand. Pl. Names: 27. 1923. TYPE: Japan Honshü: Nikko, 23 May 1876, J. Bisset D (lectotype, ee coe by Judd & Kron, 1995: 16, E not seen). Rhododendron e Bisset & S. Moore f. ipic N. Yonez., J. Phytogeogr. Taxon. 35: 101. 1 Japan. Honshi: Pref. Shiga, Mt. Hira, 24 May 1987, N. Yonezawa s.n. (holotype, KANA not seen). Shrubs deciduous, 2-5 m tall; young shoots glabrous. Leaves chartaceous, in a whorl of 5 subverticillate), obovate or broadly obovate, 2-4 x 1.5-2.5 em, acute and mucronate at apex, cuneate at base, entire, softly ciliate at margin, glabrous on both surfaces except midribs pilose; petioles 0.5-4 mm, we bowl-shaped, 2-3 mm diam., glabrous, ides lanceo- late or linear, 1-2 X ca. 1 mm; corolla white, rotate- funnelform, 28-33 X 30-40 mm, 5-divided, tube 10- 13 mm, glabrous on both surfaces, lobes broadly ovate, 15-20 X 10-15 mm, upper lobes with green spots at base; stamens 10, unequal in length, 12- 20 mm, filaments A pilose on lower third, anthers oblong, 2 mm; ovary narrowly ovoid, abrous; style 20-27 mm, glabrous. Capsule ovoid, 7-9 X 4-5 mm, glabrous; seeds 2.5-3 X 1-1.5 mm. Distribution and habitat. Rhododendron quinque- folium is known only from Honshü and Shikoku provinces in Japan. It grows in forests at 200-1800 m a.s.l. Phenology. Rhododendron quinquefolium flowers from early May to mid-June, with the floral buds opening after the leaves. It fruits from September to November. Discussion. Rhododendron quinquefolium is a dis- tinctive species in its obovate leaves in a whorl of five clustered at the tops of young shoots. It resembles R. pentaphyllum Maxim., another species endemic to Japan, in its 5-whorled leaves. Rhododendron penta- phyllum is distributed in northern to central Honshü and the leaves are elliptic. Rhododendron quinquefo- lium has sometimes been recognized as a member of section Sciadorhodion (sensu Judd & Kron,1995) and is closely related to two other members of section R. pentaphyllum and R. schlippenbachii, in having fué leaves forming a whorl at the tip of the branches (Judd & Kron, 1995). However, both flowers and leaves emerge from the same mixed buds in K quinquefolium, and for this reason we regard it as a member of section Brachycalyx Additional imens nsa d c Honshü: Pref. Fukushima: ura, G. Murata et al. 68817 (KYO), sano dort P Mt. Akai, H. Hara s.n. (TI). Pref. Gifu i-gun, Itadori-mura, H. Takahashi 20505 (KYO). Pref, ie Mt. Rokko, S. Okamoto 20052 e T. Tashiro s.n. . TNS). Pref. Ibaraki: Kitaibarakishi, re d ado 3324 (KYO). Pref. Kanagawa: amakita-machi, Y. Hassegama 1463. M Hobo. n sena: T. Sawada 841 (KYO, TI), T. s.n. (TD, H. Yamamoto sn. LN N. Masuda s.n. (TNS). Pref. Mie: Marducie-des Mie-gun, near Mt. Yuno, K. Iwatsuki & N. Kitagawa 74 (KYO); Mie-gun, Mt. ci M. Hiroe 12944 (KYO); Mie-gun, Hirauar , G. Murata & N. Fukuoka 37 (P, TI); men Kato 6039 (TD; bilan Yawata-mura, H. Kanai n. (TI); Ise, a valley of Ohsugitani, M s.n. (TT); Ise, Mt. re H. Hara s.n. (TI), Kuwashima n. (TNS). Pref. Miyagi: Miyagi-gun, J. H. Ohba & K. Ols sa (B, KYO, P, PE, TI); Katta-zun, T. Naito 72512 (B, Volume 97, Number 2 Jin et al. 183 2010 Revision of Rhododendron sect. Brachycalyx Figure 5. Rhododendron nm. Bisset & S. Moore. —A. Flowering shoot. —B. = showing indumentum. —C. š —D. Style and ovary. —E. Capsule. A-D from S. Kawatsuki s.n.; E from Kanai s. KYO); Shibata-gun, H. Ohba & M. Yashima s.n. (TI); Iwanuma (NAS); Yoshino-gun, Kamikitayama- qa Mt. Om x e City, Taketoma, M. Honda s.n. (TI); Sekiyamatouge, T. "Tashiro Okada 1385 (KYO), 1405 (KYO), S. Tsugaru et al. s.n. (KYO). Pref. Nagano: Shinano, Shimoina- gun, Hiraoka- (TNS), G. Murrata s.n. (TNS); Mt. ded M. Hotla Ps E muta, K. Katsumata 15675 (TI). T. Pref. N vues Yasqa. Fujiwara 33 (KYO); Ohdaigahara, T. Yamazaki et al. 892 (TI, Kamikitayama-mura, G. Murata 70385 (KYO), H. Migo s.n. TNS); Mt. Ohmine, H. Hara s.n. (TI), M. Togasi s.n. (Tl), 483 Annals of the Missouri Botanical Garden (B, KYO, P, W). Pref. Shiga: Mt. Hira, Kanakusotoge, G. Murata 44451 (KYO, TI); Yakumogahara, Mt. Doman, M. Ito 1240 (TI); Oumi, Ohara-mura, N. Hashimoto s.n. (TNS). Pref. Shizuoka: Haibara-gun, Honkawane-cho, H. Koyama 80 (KYO), Mastuda s.n. (Tl); Haibara-gun, T. Yamazaki 6215 (TI); Godenba, Mt. Fuji, M. Hireo 17713 (KYO); Shizuoka-shi, Abetoge, Yamazaki i 6. Rhododendron tashiroi Maxim., Bull. Acad. Imp. Sci. Saint-Pétersbourg, ser. 3(31): 64. 1887. tashiroi (Maxim.) H. F. Copel., Amer. Midl. Naturalist 30: 597. 1943. TYPE: Japan. “Southern islands, Tanega-sima," s.d., Y. Tashiro s.n. (holotype, LE not seen). Figure 6. Rhododendron tashiroi Maxim. var. lasiophyllum Hatus. ex T. Yamaz., Fl. Jap. (Iwatsuki et al., eds.) (ed. 2) 3a: 31. 1993. TYPE: Japan. Kyüshü: hima, Kasedashi Mt. Choya 16 Apr. 1967, H. Hatusima & S. Sal 30554 (holotype, TI!). Shrubs evergreen, 1.5-4 m tall, sometimes to 6 m; young shoots hirsute, later glabrescent. coriaceous, in whorls of 2 or 3 posite or verticillate), elliptic-ovate, elliptic-obovate, or ob- long-elliptie, 3-65 x 1-3 em, acute or shortly acuminate, with an apical gland, cuneate at base, entire or minutely denticulate at margin, with appressed, cinereous-brown trichomes on both sur- faces, glabrescent or sparsely hispid on dorsal surfaces except midribs hispid; petioles mm, with appressed brown trichomes. I to 5-flowered; pedicels 6-15 mm, with brown Leaves . oblong, ca. 2 mm; ov ovoid, densely villose; style 25-35 mm, ole. Capsule obliquely cylindrical or narrowly ovoid, 9-13 _ | 5—6 mm, densely to sparsely hirsute; seeds 1—-1.5 X 0.4—0.7 mm. Distribution and habitat. Rhododendron tashiroi has been collected from Taiwan, China, as well as from Kyüshü and Shikoku provinces in Japan. It grows in forests or at forest margins at 200—1300 m a.s.l. Phenology. ndron tashiroi flowers from mid-March to early May and fruits from August to November. Yamazaki described and published a variety of Rhododendron tashiroi (Yamazaki, 1993), considering variety lasiophyllum distinct from the taxon by its leaves pubescent on the abaxial surface. After examining the type and additional specimens, we determine that this character is not stable, and that pubescent and glabrous leaves can be seen within the same specimen or even along the same young shoot (e.g., A. Naiki 5284; S. Fujii 9134, 9366; H. Hatusima 16394). We therefore reduce R. tashiroi var. lasio- phyllum to synonymy with R. tashiroi. Based on this species, Sleumer (1980) established section Tsusiopsis, and this section differed from section Brachycalyx in having evergreen leaves, with the leaf blades and young shoots sometimes hirsute. (1990) transferred the species to section Tsutsusi Sweet. Yamazaki (1993, 1996) synonymized section Tsusiopsis within subgenus Sciadorhodion. Yamazaki (1993) later considered this within section Brachyca- lyx (sensu Sleumer, 1949). Pollen of Rhododendron tashiroi is tricolporate, subspheroidal, and conspicu- ously granulated (Zhang et al., 2009). Based on the leaf indumentum, leaf arrangement, and pollen mic logy, R. tashiroi is similar to other taxa in section Brachycalyx more so than to taxa of section Tsutsusi (Jin, 2006; Zhang et al., 2009). Leaves of section Tsutsusi are Tsutsusi are smaller than those of R. tashiroi, and the exine sculpturing is compact granulated (Zhang et al., 2009). , ^dditional specimens examined. CHINA. Taiwan: Gao- xiong, Mt. Oodake, J. Ohwi 1742 (KYO), 1854 (KYO). JAPAN. Kyüshü: Pref. Kagoshima: Isl. Amami i i, Ooshima-gun, Uken-mura, Mt. Volume 97, Number 2 2010 Jin et al. 185 Revision of Rhododendron sect. Brachycalyx Figu Rhododendron tashiroi Maxim. —B. Serien E ovary. —E. Capsule. A-D from S. ad et al. D433; E from Y. Miyagi 1960. Togashi 74-4-1 (P), A. Yamamoto 186 (TNS); Isl. Amami, ima- Yakushima, N. Fukuoka & M. Okamoto 1078 shoot. Leaf, showing indumentum. —C. Stamen. —D. Hamavya s.n. (TI), S. Saito 1557 (PE, TD, G. Murata et al. 286 (TD, . T. Yahara et al. 10528 (TI), 10538 (TI), 10544 (TD, 10237 (TD, 10209 (TT), 6026 eE, SZ), 10036 P. PE); z Yakushima, Ohkawa-rindo, Z. Sato hima- e EE p S. Kobayashi 1960 (TD: Isl. A mami- dile t. Takabachi, 5. pom & H. Nagamasu 1035 Annals of the Missouri Botanical Garden to M. Ozawa s.n. E Isl. Amami-ohshima, Mt. Yuwan, Saito 4076 9487 (TT), K. Enomoto s.n. (TI), J. Murata Ex Endo 150 (TI), J. Murata 4966 (TI); Isl. Amami, Nase, Y. Miyagi 8698 (TI); Isl. Amami, S. Sako 3955 (TI); Isl. i okunoshima-cho, Mt. Inokawa, G. Murata 56257 (KYO); Isl. Tokuno-shima, — of NHK, J. Murata 9354 (KYO); Isl. Tokuno-shima, H. Nagamasu 1771 (KYO); Isl. Tokuno-shima, m, Inokawa, s Tala 85-223 (Tp, umage-gun, Y aku-cho, Mt. Kuniwaridake, T. Yahara a al. 9186 (KYO); — Peninsula, Yakushima, G. Koidzumi s.n. (KYO); Mt. bsp Kouishi, T. Tashiro s.n. (KYO); Ohsumi, Mt Takakum 2488 K - Okinawa: Kunigami Kunigami-mura, Mt. Yonaha-dake, S. Fujii 1795 (TNS), 1801 (TNS), K. housuli et al. 13 (KY i es (TNS); Kunigami & 992 (PE); Isl. Okinawa, Mt. Yon H. 96 (TNS), S. & - Nagamasu 764 ei & Med 1780 (KYO); Isl. Okinawa, Tanaga- nai 732559 (TNS); Ryukyu, M. Nu Makers 24140 rs Pref. Saga: Usu- shi, Haba 6 S), Kuranari s.n. (TL, TN S), I. Enomoto s.n. (TI; Usu-shi, Mt. Shiro, Haba s.n. (KYO); Mt. pcd ` kay 6884 E Miyaki-gun, Tashiro- s.n. (TD. Shikoku: Pref. Kochi: Tosakuni, Mn 1 Enomoto s.n. m 7. Rhododendron wadanum Makino, J. Jap. Bot. k 21. 1917. EN Lm D. Don ex G. Don var. m (Makino) Hatus., Sci. Rep. Yokosuka City, Mus. 15: 22. 1969, TYPE: Japan. Honshà: Pref. Kanagawa, Hakone, Mt. Kintokiyama, 15 May 1927, T. Sawada s.n. s designated here, TI). Figure 2A—E Rhododendron psp Makino f. ee Hiyam. a, J. J Bot. 28: 1953, as “kaiens > TYPE: Japan $ Honshú: ^d ru Mt. _ Misuage, 12 May 1938, K Hiyama s.n. (holot TNS). Rhododendron wadanum Makino var. leucanthum Makino, J. Jap. Bot. 3: 11. 1926. Rhododendron wadanum Maki f. leucanthum (Makino) H. Hara, Enum. no Spermatophy- tarum Japon. 1: 56. 1948. TYPE: Japan. I Pref. wa, Hakone, T. Sawada now Te n. (holotype, Rhododendron Mean ino f. kaimontanum Okuyama, J. Jap. Bot. 24: 112. 1949. TYPE: Japan. Honshii: Pref. Kai pe, mu June 1949, S. Okuyama s.n. (holoty, Shrubs deciduous, 1.5-3 m tall; young shoots glabrous. Leaves chartaceous, in a whorl of 3 (3- verticillate), ovate-rhombic or rhombic, 3—7 X 2—6 cm, acute and mucronate at apex, cuneate or rounded at base, entire or sometimes minutely denticulate at margin, sparsely villose on dorsal surfaces, densely so on midribs dorsally, rous on ventral surfaces; petioles 3—7 mm, mia villose. Inflorescences 1- or 2-flowered; pedicels 4-10 mm, pilose and glandular. alyx bowl-shaped, ca. 3 mm diam. sparse p ent, lobes inconspicuous; corolla purple or rose-pink, rotate-funnelform, 25-30 X ca. 40 mm, deeply 5-divided, corolla tube ca. 7 mm, glabrous on both surfaces, lobes obovate to oblong, 17-20 X ca. 10 mm, upper lobes with dark purple spots at base; stamens 10, unequal in length, 10-25 mm, filaments glabrous; "e 2 ca. 2 mm; ovary ovoid, densely villose 5 mm, glandular. Capsule obliquely sono 10-13 X ca. 5 mm diam, hirsute; seeds 0.8-1.2 X 0.4-0 Distribution and habitat. Rhododendron wada- num is endemic and known only from Honshü Province in Japan. It grows in mixed forest at 900- Phenology. Rhododendron wadanum flowers from mid- to late May, with the flowers opening before or with the emergence of leaves. It fruits from August to October Discussion. Rhododendron wadanum is similar to R. farrerae in its 3-verticillate leaves and 1- or 2- flowered inflorescences, but differs in its styles with glandular trichomes. Makino (1917: 21) described Rhododendron wada- num as a new ies, but no collection or illustration was indicated as ope, Akbosgh this porien i was not validly published. it from the other species of Sri Balota w we ero designate as lectotype here the collection T. (TI), a flowering specimen in good Pei Rhododendron wadanum f. kaimontanum was described by Okuyama (1949) and distinguished by its 1- or 2-flowered inflorescences. However, for the 10 inflorescences seen for its holotype, eight had only one flower. Therefore, we reduce this form to synonymy with R. wadanum Additional ns examined. JAPAN. Honshü: Pref. Aichi: n K. Torii 10526 (KYO). Pref. Fukui: ugi-gun, m i-mura, iba, H. Takahashi - 5i (KYO). Pref. Fukushima: s. loc., G. pter et al. 68 (KYO); Nakiska gm H. Hara s.n. (TI); Nishishi akawan-gun, Saigo-mu ura, Ç. Suka. al s.n. gun, H Hara s.n. om T kem. Zaimouiwa, m. jd (TD; Sh Azuma-cho, ten Nakahara (KYO); Fas, Naraha-machi, 7. Nemoto 2952 0; e T. Fukuda & K. Volume 97, Number 2 2010 Jin et al. 187 Revision of Rhododendron sect. Brachycalyx n (PE). Pref. a Mino-City, Hirugano, G Takasu-mura, ata 16163 (KYO); PE eis - P egt 6232 (KYO); Fuha-gun, from Sekigahara-cho to Myojin-pass, G. Murata & T. Shimizu 1592 (KYO), 1606 (KYO); Mashita-gun, Hagiwara-cho, Mt. Gozen, G. Murata 28 (KYO); Motosu-gun, Neo-mura, Midori- dani, H. Takahashi 17048 (KYO). Pref. Gunma: Akagi-gun, Z. Sato s.n. (TI); Kiryu-shi, Mt. Narukamiyama, J. am al. 11018 (KYO, PE); Usui-gun, Hakuunzan in Mt. Myogi Murata 27468 (KYO); Tano-gun, Onishi-machi, s ac J. Murata 1655 (KY0). Pref. Ibaraki: Kuji-gun, Suifu-mura, ada 3445 Hanasyuu, N. . Murata et P 105224 (KYO); Kamae, d Co., ks Sinus 4073 (KYO); Ise, Mitsuk dake, G. Murata 11257 gg 11260 (KYO); be, Kitadani, ie ew shyo, G. Mur E reed € E 0); — usei-cho, c Kurosaki 14917 g> "Pref. Miro Sendai-shi, Mt. De M. ima s.n Pref. Nagano: Minamisaku-gun, D re dia 12217 (KYO); Shinano, Minami- saku-gun, from Mt. Azusa to Mt. Mikuni, G. Murata 11824 (KYO); apra Shimoina-gun, Ohs| P Aokigawa, T. Yamazaki ; Shinano, Shimoina-gun, K. Katsumata 16544 (T ^r x Asana 9873 (TI); Suwa- r Fe mee Mizushima s.n. (TI); Tobira, H. ovo e 64 (TI); Karuizawa, S. Watari s.n. itm Amts cho Akasawa, Murata & Pikia a s.n. (KYO); K m Kyrokawa, H. Kanai s.n. (Tl); Takatoku, a Ohwi Okamoto 442 (B, KYO, P, bi Pref. Saitama: Iru from Mt. Kuro to m Pass, H. Ohashi et A 1381 1 (KYO. ad, Buheiuge, G. Murata 21045 (KYO), E. Miki 158 qe 165 ae Y. Kamijo 177 (KYO); ete = Am uoka 7252 (P. m N. Fujita & M yama 3 (KYO), T Pars et al. 2040 KYO, bre Mts. “Ama "=a T Fukuoka 7242 Fudou, H. no s.n. (KYO), H. Ohashi et al. 11214 (IBSC), 11603 ds Nikko-shi, Mt. Akanagi, M. Tagawa & G. Murata 36 (KYO), 53 (KYO); Nikko-shi, hope. Fall, H. Ohashi et al. 11603 KYO), 1 iras (KYO); Nasu-gun Nasu-cho, A Kimura s.n. (PE). Pref. Tokyo: — d ea s.n. (TD). Pref. ee Mt. H. Hara s.n. (TI). Pre amanashi: Uchino, aa s Oshino-mura, x Togashi s.n. (KYO, P); Minamitsuru-gun, Mt. Mitsutoge, N. Fukuoka 6676 (KYO), 6672 e respect -gun, H. Kanei s.n. (TI), M. Togashi s.n. (TI), J. 1108 (TD, T. Satou 1 $ win suru-gun, “esa mura, M. Togashi s.n. (TI, KYO); Mt. Daibosatsu, G. Murata 16940 (KYO); Nishiawa, H. Funakoshi 35 (TD); t. Komagadake, Z. Sato s.n. (TI), G. Murata 11947 (KYO); Mt. "Fuji Y. Satake 47 (TD, T. Sawada s.n. (TI); Mt. Fuji, Yoshidaguchi, M. Togashi s.n. (KYO) . Rhododendron weyrichii Maxim., Mém. Acad. Imp. Sci. St-Pétersbourg, ser. VII, 16: 26, t. 2: 1- Rhododendron weyrichii ee N”. ple 6. 1870. TYPE: Japan. “In Archipelago Gotto, Insula Sylvestri, 1853,” H. Weyrich s.n. (holo- type, LE not seen). Figure 7. Rhododendron shikokianum Makino, Bot. Mag. Tokyo 6: = 1892. TYPE: Japan. Shikoku: Pref. Kochi, Takaokagu Sakawa M 1889, T. Makino s.n. (holotype, MAKn "i seen, photo!; isotype, K not seen). M: ichii Maxim. f. albiflorum GPL Jap. (Iwatsuki et al., eds.) (ed. 2) 3a: 31. 1 jum ae nov. : Japan. Shikoku: Pref. Kochi, cult. Tokyo, May ‘amazaki s.n. (holotype, TT!). tylum ^c MN Mag. (Tokyo) 40: 48 6, syn. nov. TYPE: K Chejudo hien > July 1911, Anon. 5785 (holotype, Rhododendron w axim. f. uses Fl. Jap. (Iwatsuki et ey eds.) (ed. 2) 3a: 1. 1993, w. nov. TYPE: Japan. Honshü: Pref. Mie, = Tokyo, 28 Apr. 1964, I. Enomoto s.n. (holotype, TI not seen). Shrubs deciduous, 2-5 m tall; young shoots with brown trichomes, later glabrescent. Leaves charta- ceous, usually in a whorl of 3 (3-verticillate), broadly rhombic-ovate, 3.5-8 X 2-6 cm, acute and mucronate at apex, rounded at base, minutely denticulate at margin, pubescent on both surfaces, later glabrescent; petioles 5-10 mm, sparsely pubescent. Inflorescences 2- to 3-flowered; pedicels 4-8 mm, densely pilose. Calyx bowl-shaped, ca. 3 mm diam., densely cent, lobes inconspicuous; corolla red, rarely purple or white, broadly funnelform, 3 x 50 mm. deeply 5-divided, tube ca. 15 mm, glabrous on both surfaces, lobes elliptic, 20-30 X 15-20 mm, upper lobes with dark red s at base; stamens 10, unequal in length, 10-30 mm, filaments glabrous, anthers oblong, ca. 2 mm; ovary ovoid, densely villose; style 35-40 mm, glabrous. Capsule obliquely ee 10-20 x 5-6 mm, densely pilose; seeds 0.5-0.6 mm. Distribution and habitat. Rhododendron weyrichii has been collected from Honshi, Shikoku, and Kyüshü provinces in Japan, as well as from southern inland Korea. It grows in closed forests, under forest, or on slopes at 200-1000 m a.s.l. Phenology. Rhododendron weyrichii flowers from mid-April to mid-May, opening before or with leaves. It fruits from late August to mid-Octo Discussion. Rhododendron weyrichii is similar to R. amagianum in having large flowers often red in color and corollas that exceed 35 mm in length. Corollas of R. ichii are red, rarely purple or white, and 35-40 mm long, while those of R. amagianum are purplish red or red, rarely white, and 35-45 mm long. However, R. weyrichii differs from R. amagianum in having young leaves with brown pubescence and sparsely pubescent petioles. Rhododendron amagianum has young leaves 188 Annals of the Missouri Botanical Garden C 9 _ Figure ichii Maxim. — Mie A-C "rom X. F. Jin 1426; D from S. Saito Ee ote —B. Stamen. —C. Style and ovary. —D. Fruiting shoot. that are glabrous dorsally except for the densely villose midribs and villose petioles. r or altitude. They are therefore tos ith R. weyrichi. f -— € as e The variety Rhododendron weyrichii var. psilosty- orma purpuriflorum Yamazaki š (1993:31). These t pen by lum differed from the typical entity in having from only one and cannot pubescence on the style base, but the indumentum em be differentiated in in of the style base is not sufficient to distinguish the Volume 97, Number 2 2010 i : 1 Revision of F'hododendron sect. Brachycalyx variety from R. weyrichii (Yamazaki, 1996). Variety psilostylum is therefore placed here as a synonym of R. ional e i examined. JAPAN. Honshü: Pref. A RR G. Koizumi s.n. ` KYO): rdc T. Tashiro s.n. (KYO); oe ee Mihama-cho. Koide s.n. (KYO); Kita- n, Sugari-mura, Anon. s.n. ee G. P 4299 (KYO), Owa satt po -dani, n. (KYO); Ronen 24, Arima-cho, T. ae m KYO). Pre. Wa- kayama: Higashimuro-gun, Koide s.n. aes ee Ukishima, K. lwatsuki s.n. pur f. goshi ushikino-shi, A s.n. he da. Shiku, M. n s.n. (TNS); s. E T. Makion s.n. (TNS). Pref. : Aie bu, Torida 14163 (KYO). Pref. yu-gun, T: -cho, Mt. Osuzu, X. F. Jin m Arakawa to YO), c. Murata & H. Koyama 14522 (KYO), N. Fujita & A Mitsuta 327 (KYO), 280 (KYO); Isl. Fukuejima, Ara-kawa, T. Omura-shi, Toyama s.n. (KYO), T. Š Pref. Oita: Oono-gun, Ogata-cho, Mt. Katamuki, N. Fukuoka 7224 (KYO), S. Kitamura s.n. LN Oono-gun, T. Tashiro y E phe s.n. (KYO). de q oa -mura, N. Fukuoka 8731 (KYO); Uvajima-shi, w ena Nishiuwa-gun, Mikame-cho, Izumi, N. Kurosaki 7168 (KYO): Nishiuwa-gun, Ikata-cho, E: Nomura 21 (KYO); Higashiuma- Shimizu cc (KYO), 05920 (KYO); Takes don, Hee itsuno-mura, G. Murata & T. Shimizu 2463 en WIR. Yuzuhara-mura, Murata & T. 2545 (KYO), 2487 (KYO) Viola, i "Mc Yokogura, H. Koyama 4253 (KYO); Erie Hidaka- ura, a. Ejiri, N. ES saki 6665 (KYO); NE of T oe ma 4225 (KYO); Mt. Godai 6271 (KYO), 6689 (KYO); Kami-gun, Monobe-mura, Mt. Kanjyo, G. Murata et al. fre T ie Mne | mada-cho, aruhashi (KYO); Miyoshi-gun, DN Mt. Kuni Murata 7685 (KYO); gun, Ikedatyou, s Tsugaru aie (KYO); Mima- nm wae o Y. Kato 46 (KYO); ma-gun, An o, Ogami-mura, N. Kurosaki 8156 (KYO). KOREA. Isl. RA loc., K. Katakura s.n. (KYO); Isl. Jeju, Mt. Hanja, Park s.n. (KYO), I. Nakashima s.n. (KYO). Literature Cited Chamberlain, D. F. & S. J. Rae. 1990. A es E ndron IV subgenus Tsutsusi. Edinburgh J. , R. Hyam, G. Argent, G. daga & K. S. Walter. 1996. The Genus Rhododendron: Its Classification and Synonymy. Royal Botanic Garden Edinburgh, Edin- Copeland, H. F. 1943. A study, anatomical and taxonomic, of the genera Rhododendroideae. Amer. Midl. Nat. 30: 533-625. Cullen, J. 1980. A revision of Rhododendron 1 — Rhododendron sections ndron & Pogonanthum Notes m It Gard. Edinburgh 39: 1-207 F. Chamberlain. 1978. A tcm synopsis of the genus Rhododendron. Notes Roy. Bot. Gard. Edinburgh 36: 105-126. & . 1979. A preliminary synopsis of the genus Rhododendron: II. Notes Roy. Bot. Gard. Edinburgh 37: os in Ding, B Y.& Y Fang. 1989a. A study on Rhododendro L. fron sm Zhejiang J. Hangzhou Univ. Nat. Sci. Ed. 16: 192 — ——. 1989b. M Pp. 6-25 in Y. Y. NM ditor), Flora of Zhejian = = Auris cds and Technology Publishing House gzhou & new species a of — from vd Chim. Bull. Bot. Res. 10(1): 31-33. — & X. | ERN Validation of Rhododendron China. Taxon 54: 804. , H. X. Wu, H. M. Zhang & Y. Y. Fang. 1995. Seed . o E Rhododendro n L. ya from Zhejiang its gia significance. Acta Bot. Boreal.-Occid. Sin. 15(6): 364. Don, G. 1834. 0 P G. Don Penis A General D of nag wes nig hq VoL Jc E E gto ington, London. € esting) Y. He, L. C. Hu, H. P. Yang & C. Chamberlain. 2005. Rhododendron. Pp. 260-455 in a Y. Wu & P.H. Et (editors), Flora of China, Vol. 14: Apiaceae throu Missouri Botanical ida TN s, St. Louis. Fang, W. P. 1935. Chinese Azalea. J. Bot. Soc. China 2: 5 Gao, L. M., g C. Q. Zhang & D. Z. Li. 2002a. ha lla of subgenus Tsutsusi (Rhodo- dendron) based on ITS sequences. Acta Bot. Yunnan. 24: le C. Q. Zhang, D. Z. Li & Z. X. Wei. 2002b. Pollen older of the Rhodoreae (Ericaceae) and its system- atic agree Acta Bot. Yunnan. 24: 471-482. Hara, H ee ad plantas Asiae Orientalis (V UD. i o. Bot. 11: 820-830. . 1948 ui ron. Pp. 26—59 in H. Hara sara - Iwa- Enumeratio eroe Japonicarum, Vol. 1 nami gn wo = ndron (sect. E tm Hokkaido. E 2 Bot. 49: 353-355. Hayata, B. 1913. Ericaceae. Pp. 129-146 in B. Hayata (editor), Icon. Pl. Formosa. Government of M Tai ihoku. He, M. Y. 1994. Rhododendron subgen. i. Pp. 36 436 in L. C. Hu & M. Y. Fang (editors), cm ibn Popularis Sinicae, Vol. 57(2). Science Press, Beijing. . C. Chamberlain. 2005. Rhododendron subgen. R Ericaceae. Science Press, Beijing, and Missouri Botanical Garden Press, St. Louis. Hemsley, W. B. & E. H. Wilson. 1907. A wr LM rhododendron. Kew Bull. Misc. Inform. 1907: 2 Annals of the Missouri Botanical Garden Hocker, J. D. 1876. Rhododendron. n Bentham Bs zi si le Pp. 148-176: in S. Kitamura & G. Messin — Coloured Illustrations of — ue of Japan, Vol. 1. Hoikusha, Osaka. C. Murata (editors). m Coloured Illustrations A Woody Plants of Japan, Vol. 1. Hoikusha, Osaka. . Y. 1999. a new species from T. Edinburgh J. Bot. 56: 56: 75-78. , 3. 1. Etoh, T. Handa, K. Takayanagi € T. Yukawa. Rhododendro -14. Azalea. Pp. s in C. Linnaeus itor), Species Plantarum, Vol. 1. St akian . T. 1893. Notes on Japanese ne. XVIII. Bot. Mag. CToyko) + 133-135. nl I Bot. 1 : Kio to the knowledge of the flora of pase J. je. Bot. 3 1926b. A Ron o the knowledge of the flora of Japan 2 Jap. Bot. 3 - es . - 5 ^ ———. 1887. novarum asiat x e Acad. Imp. Sei. St.-Pétersbourg Ser. 3, 31 31: vw Y F. R. Barrie, H. M. Burdet, V. Demoulin, IL Hawksworth, K. Marhold, D. H. Nicolson, J. Prado. Silva, J. E. Skog, J. H. Wiersema & N. s d ac 1 ernational Code 2, lature . Observa Rhododendro t iadorhodion from E Fukuoka Bot. 10: 19-36. Ming, T. L. & R. C. Fang. 1979. On the origin and geographic "ror of genus Rhododendron L. Acta Bot. Yunnan. Nisi, T. 1 1924. Abstract from T. Nakai “Trees and Shrubs — ——Ó D with additional bes m m Bot. Mag. yo) 38: 23-48. Notis ad plis. hows h Roni XXXII Ba. Mag. (Tokyo) 40: 463—494. ion, Ties and Sr idi oS m rees ai Indigenous in 1, Rev. Ed. Seibido Shoten, Tokyo. 932. Notulae el vise Japoniae & Koreae XLII. ` Bot. a Mag feo 36 1 = 2 YIVII Bot. ag eva 49: 491-804, Ohwi, J. . Rhodode . 883-896 in J. Ohwi “saqiq Ton. 2 Japan. Sa Tokyo. Okuy: A horse-in-hose form of Rhododendron se : Py Bot. 24: 112 Philipson, M. N. & W. R. Philipson. 1982. A preliminary synopsis of the genu ur ron III. Nise Roy. Bot. Gard. re ga 225- Philipson, W. aN. lige 1973. A history of a cates Notes Roy. Bot. Gard. Edinburgh 32: 223-238. acra H. 1949. Ein System der Gattung Rhododendron L. M none 74: 511—553. a Past present taxonomic systems of A on — a al characters. Pp. 19-26 in J. L. Luteyn & M. E. O'Brien (editi Contributions — a Classification of Rhododendron. al Garden, Spethmann, W. 1987. À new Bei classification and phylogenetic trends in the genus Rhododendron (Erica- ceae). ops x. Evol. 157: e Tam, endrons of eastern and hen tu Rhododendron in South in. Guangdong Science & Technology Press. Guan Wilson, E. H. 8 A. Rehder. 1921. A Monograph of Azaleas. Harvard esse Cambridge. Yamazaki, T. 1. Some new taxa of Rhododendron from Japan ind Taian J. = I kgs dece . Some hododendron sect. Broto in Rae xj S ide. Japan. J. Jap. Bot. 59: 205- n Nomenclatural change on three taxa of Riwdodendron sect. m J. Jap. Bot. 62: 72. — ———. 1981b. A new variety «praia reticulatum D. Don. J. Jap. Bot . 1988. On Bodsdindio on nudipes ssp. y and ssp. niphohilun. J. Jap. Bot. 63: 409-41 — Rhodode 6-44 in K. Iwatsuki, T. Yamazaki, D. E. Boufford & H. Ohba (editors), Flora of Japan, 3a. Kodansha, Tokyo. - 1996. Rhododendron subgen. d = 113 in T. M (editor), A EA pa “the Ge m Taiwan, Korea and a Sakhalin. umura Eli okyo. DRY. Ex ; Ax Y. Ding & J. P. Zhu. 2009. Pollen ogy o ndron Tsutsusi and its systematic hee J. Syst. Evol. 47: 123-138 MOLECULAR PHYLOGENETICS, CHARACTER EVOLUTION, AND SUPRAGENERIC CLASSIFICATION OF LAMIOIDEAE (LAMIACEAE)! Anne-Cathrine Scheen,?*" Mika Bendiksby,?* Olof Ryding,” Cecilie A 25 Victor A. Albert? and. Charlotte Lindquist** ABSTRACT This bars dime a € analysis of Lamiaceae subfam. m nn peru Pogostemonoideae) a M hui all “wm Tamioid and pogoste Pogostemonoideae) i is strongly supported has been reco; divided into nine tribes. Three new tribes are establis! gnized as a — is subsumed in E On the basis of the Thylpeneti hypothe p F intergenic spacer, and rps16 intron of genome. It i is the first monoid genera. "mph of picas s.l. (i.e., including , with Cymaria ele as > sister group, and Po ini ad - ch uu s, Lamioideae is ostemmateae Scheen & Lindqvist, Phlo iiia ae Mathiesen, mort., Marrubieae Vis. The genus Betonica L. is reest results also ls ae C strongly suggest that the genera Stachys L., Sideritis L Character evolution, Pogostemonoideae. classification, , Ballota L., and Leucas R. Br. are a or or paraphhylee. The results were used to examine evolution of osi di characters Piden. Lamioideae, molecular phylogenetics, morphology, g the past decade, the number of molecular ime studies on plants has increased at a pace. Advances in comparative DNA sequenc- s: d methods for phylogeny reconstruction have made it poss systematic ec evolut road ionary questions for large numbers of taxa. One important result of this has been that molecular phylogenetic studies have metimes overturned relationships suggested from traditional classifications. One such example is the range of iaceae, which is a large, cosmopolitan angiosperm family with 236 genera and more than 7000 species (Harley et al., 2004 e Lamiaceae is traditionally been regarded as one of the most distinctive angiosperm families, readily identified by a suite of morphological characters (Bentham, 1876; Briquet, 1895-1897). A close yet discrete relationship with Verbenaceae was also suggested by the early system builders. However, modern phylogenetic analyses of morphological data have suggested that Lamiaceae was polyphyletically derived within Verbenaceae (Abu-Asab & Cantino, 1992; Cantino, 1992a), with the consequence that some previously verbenaceous taxa were reassigned to Lamiaceae to pues the family’s mn did (Cantino, Cantino et al, 1992). phylogenetic sista were later resets xi tive DNA sequence analysis (Wagstaff & Olmstead, 1997; Wagstaff et al., 1998). Currently, seven subfamilies are recognized within Lamiaceae M authors thank the tusuni at. A, ei em O, P, S, TEX, UPS, US, and WU herbaria for permission to perform destructive w , Ric supported by a grant (no. 154145) from the Research C 2 ard G. Olmstead for a DNA sample of Gomphostem e , Janet Barber for DNA Pen of Sideritis L., and Philip D. Cantino for providing —— moschata Miq. We thank Steven J. Em and l2 I gems for useful comments on the man mma < egy P erial of Chelonops ad. This inb Wi was Norway to Victor A. Albert. Natural History Museum, C Oslo, P.O. Box 1172 Blindern, NO-0318 Oslo, Norway. a.m.bendiksby@nhm.uio.no * Curre wat din Department of Plant and Environmental Sciences, University of Gothenburg, Box 461, SE-405 30 erie Sweden. pat aN scheen@d .gu.se " Botanical Garden & Museum, Natural History liue of Denmark, University of Copenhagen, Gothersgade 130, DK- 1123 Ebene =a Denmark. OlofR@snm.ku.dk. 5 Current address: Department of Biology, University of Oslo, P.O. Box 1066 Blindern, NO-0316 Oslo, Norway. eecilie; vic aerei uio.no. ment of Biological Sciences, University at Buffalo (SUNY), Buffalo, New York 14260, U.S.A. cl243Gbuffalo.edu Ibert). nce: cl243Gbuffalo.edu. doi: 10.341 7/20071 74 Ann. Missouri Bot. Garp. 97: 191-217. PuBLISHED ON 9 JuLy 2010. Annals of the Missouri Botanical Garden (Harley et al., 2004), of which Nepetoideae is the largest, one of the most easily defined, and probably the best investigated. Throughout the taxonomic history of Lamiaceae, the i iption of another large subfamily, Lamioideae has changed considerably (see, e.g., Cantino, 1992b). Recently, Cantino et al. (1992) considered the pogoste- monoid labiates a separate subfamily, although they drew no clear distinction between Pogostemonoideae and Lamioideae. The pogostemonoid taxa were charac- terized by having stamens of equal length, and lamioid labiates by presence of laballenic acid and an unusual embryo sac. However, stamen length is likely to be an evolutionarily VALE k 4 deh p è sal 1 2 the other two characters is limited by the small taxonomic sample in which they have been documented (e.g. Hagemann et al, 1967; Wundedich, 1967; Cantino, 1992a, b, and references therein). On the other hand, pericarp structure (Ryding, 1995) and pollen morphology (Abu-Asab & Cantino, 1994) provide no distinction between the two groups. Moreover, phyloge- netic segregation of the Pogostemonoideae and Lamioi ae hae h vaiuc O1 (cpDNA) evidence, whereas the monophyletic group consisting of both subfamilies is strongly supported (Wagstaff et al, 1998). Consequently, in the latest classification of the Lamiaceae, pogostemonoid taxa have been subsumed into Lamioideae (Harley et al., 2004). However, the position of this subfamily within the Pogostemonoideae-Lamioideae clade (Wagstaff & Olmstead, 1997; Wagstaff et al., 1998). So, given the changing delimitation of the subfam- ily, how can the Lamioideae be diagnosed as currently circumscribed? As is apparent from the conflicting traditional classifications, no one set of morphological characters seems to distinguish this group from other labiate groups. They are mostly non-aromatic herbs or shrubs (or rarely small trees) that otherwise have the typical labiate bauplan. The inflorescences are thyrsoid or raceme-like, with single- to many-flowered cymes, and corollas that are zygomorphic and usually 2-lipped. They are distinguished from nepetoid labiates by having the pollen grains tricolpate and 2-celled when shed, seeds albuminous, and embryos spatulate (Cantino & Sanders, 1986). They differ from the remaining members of the family by having gynobasic styles. Within the subfamily, 63 genera including up to 1257 species are presently recognized (Harley et al., 2004). The taxonomic distribution of species within the subfamily is characterized by a large number of monotypic genera (approximately one third), and ca. 50% of the total number of species belonging to only four genera—Leucas R. Br., Phlomis L., Sideritis L., and Stachys L. These numbers seem very unbalanced an ciency of morphological syna nomic challenges that this subfamily represents. Although it has a cosmopolitan distribution, Lamioideae are rare outside of Eurasia and Africa. Only six genera and about 70 species are native to the New World. Lamioideae have many members in tropical regions of the world, particularly Africa and Southeast Asia. For example, pogostemonoids are largely tropical East Asian. Otherwise, Lamioideae are predominantly distributed in the Northern Hemi- sphere, and numerous genera are widespread in temperate to subtropical Eurasia; several are Asian endemics, whereas others are also widely spread throughout temperate Europe or are restricted to Europe and the Mediterranean region. Although Lamioideae comprise the second largest subfamily in Lamiaceae, the subfamily has not previously been the subject of targeted phylogenetic research, and suprageneric relationships within the ily, only limited phylogenetic studies at infrageneric and/or intergeneric levels have been published (e.g.. Ryding, 1998; Barber et al., 2002; Lindqvist & Albert, 2002; Scheen et al., 2008; Scheen & Albert, 2009). Our principal purpose with the present study is to ascertain major generic groupings and phylogenetic relationships within the subfamily Lamioideae. We applied molecular phylogenetic data in order to assess several questions concerning morphological trends and taxonomic subdivisions, including a first attempt at constructing a strongly needed classification of the major suprageneric groupings discovered. MATERIALS AND METHops TAXON AND OUTGROUP SELECTION À representative sample of subfamilies Lamioideae and Pogostemonoideae was selected using 167 accessions representing 159 species (13% of all species) from 50 genera (80% generic representation). See Table 1 for details on voucher information, GenBank accession numbers, and references. All major genera of lamioid and pogostemonoid labiates were included. Only a few monotypic or small genera have been omitted because no material was available or because attempts to amplify DNA failed. To evaluate the monophyly of subfamilies Lamioideae and Pogostemonoideae, 28 species of other Lamiaceae were also included: two species from subfamily Ajugoideae, 14 species from subfamily Nepetoideae, Volume 97, Number 2 2010 Scheen et al. 193 Phylogenetics of Lamioideae two species from subfamily Prostantheroideae, two species from subfamily Scutellarioideae, one species from subfamily Symphorematoideae, two species from subfamily Viticoideae, and five species that have not been ascribed to a subfamily (genera incertae sedis in Harley et al., 2004). Two species of Verbenaceae were selected as outgroup for all analyses. Most of the sequences for these 30 species were retrieved from GenBank (see Table 1). DNA EXTRACTION. (PCR) AMPLIFICATION, AND SEQUENCING DNA was “pes tig me — oe seem! herbarium Suwit ax: held at A, C, CH, O, P, S, TEX, UPS, US, and WU. Total DNA was extracted using the DNeasy Plant Mini Kit (Qiagen, Hilden, Germany) e the manufacturer's instructions. Several DNA mples from a m study were also used (Lindqvist & Albert, 2002). The trnL intron and trnL- trnF intergenic spacer were amplified using the iaa pirinin e Tela a al. 0991, either as I-I] F region a E t yit mers c and d, and e and f, pide. The rps1 6 intron was amplified using the primers rpsF and rpsR2R (Oxelman et al., 1997). When DNA of low quality was used as template, the following internal primers new to this study were used in addition to the two mentioned above: rpsLR (5'-TCATTGGGTTTA- GACATTACTTCG-3' ) and rpsLF (5'-CGGGAATCCA- CTGTCCATAG-3’). PCRs were performed in volumes of 25 uL using the AmpliTaq DNA polymerase buffer II kit (Applied Biosystems, Foster City, California, U.S.A.) containing 0.2 mM of each dNTP, 0.04% bovine serum albumin (BSA), 0.01 mM tetramethyl- ammonium chloride (TMACI), 0.8 uM of each primer, and 2 pL unquantified genomic DNA. Amplifications were performed in a GeneAmp PCR System 9700 (Applied Bend using a program consisting of 4 min. at 94^C followed by 30 cycles of 30 sec denaturation (94°C), 30 sec. annealing (60°C), and 1 min. extension (72°C), ending with a final 4 min. extension (72°C). Successful PCR reactions were purified using QIAquick PCR Purification Kit (Qiagen) or 8 uL 10X diluted exoSAP-IT (USB Corporation, Cleveland, Ohio, U.S.A.) per reaction. Cycle sequenc- ing was performed using the same primers as in the PCR and the BigDye Terminator v1.1 Cycle Sequenc- ing Kit (Applied Biosystems). Quarter reactions were prepared, i.e., 2 pL BigDye, 2 pL 5X buffer, 3 pL cleaned PCR produet, " distilled water to a Done of 10 pl d by the manufacturer on Gene ung PCR System 9700 “muras Biosystems). Sequenced products were either purified with CENTRI SEP Columns (Princeton Separations, Adelphia, New Jersey, U.S.A.) or precipitated in ethanol and sodium acetate to remove excess dye lerminators before being analyzed on an ABI Prism X madi Analyzer (Applied Mayai MK = DNA Laboratory tenis of Oslo). In addition, sequences from previous studies of lamioid labiates were used (Lindqvist & Albert, 2002; Scheen et al., 2008; Scheen & Albert, 2009; see Table 1). ALIGNMENT AND PHYLOGENY RECONSTRUCTIONS Sequences were assembled and edited using Se- quencher 4.1.4 (Gene Codes, Ann Arbor, Michigan, U.S.A.) before being aligned manually using BioEdit (Hall, 1999). Most of the alignments were straightfor- ward; ambiguities due to gaps were solved by following the advice of Kelchner (2000). Insertions/deletions "ri were seed as pro: "m and added the "m Se Sut (Miller, nS m 9h the Previous studies have shown that when iia separately, the trnL-F region and rps16 intron produce Me topologies (e.g., Wallander & d ; Jobson et al, 2003; Paton et al., ). eie the data sets resulting from the P region and rps16 intron were concatenated a priori to arsimony analyses. Two resulting matrices were analyzed: (1) data without indel coding, i.e., indels treated as missing data, and (2) data with indels coded and added to the matrix as binary characters. Parsimony analyses were run in “TNT (Goloboff et al., 2003) with the new technology option in a driven search using sectorial searches, tree-drifting, and tree-fusing (Goloboff, 1999). Analyses were run until a stabilized consensus had occurred twice using equal character weights and tree bisection-reconnection (TBR) branch swapping. Additional TBR branch swapping was performed on trees resulting from the initial search to find additional equally parsimonious trees. Parsimony jackknifing and bootstrap support for internal branches was also estimated using TNT. One thousand replicates were conducted, each performing TBR branch swapping with 10 random entry orders and saving one tree Z ==. Absolute support values were reported. Because the bootstrap support values were comparable to qe jackknife values, only the latter are reported here A cursory maximum likelihood (ML) analysis using the PHYML (Guindon & Gascuel, 2003) was performed using the online web server at . Specifications for 194 Annals of the Missouri Botanical Garden Table 1. List of species, voucher, and GenBank ion information for speci 1 in the molecular phylogeny of subfamily Lamioideae. GenBank accession no. trnL-F rps16 Taxon Origin/voucher information trnL intron spacer intron Lamioideae Achyrospermum africanum Baker Cameroon, M. bei & D. W. FJ854246 FJ854133 FJ853999 Thomas 441 (UPS A. carvalhoi Gürke Malawi, 7. Hedberg 89133 (UPS) FJ854248 FJ854135 FJ854001 A. cryptanthum Baker Malawi, R. K. Brummitt 10762 (UPS) FJ854249 FJ854136 FJ854002 A. fruticosum Benth., acc. 1 Madagascar, P. Phillipson 2082 (S) FJ854250 FJ854137 FJ854003 A. fruticosum, ac Madagascar, L. n 1083 (UPS) FJ854251 FJ854138 FJ854004 A. laterale Baker Malawi, R. K. Brummitt 11554 (UPS) FJ854252 FJ854139 FJ854005 A. parviflorum S. Moore, acc. 1 Uganda, R. A. Dummer 5603 (US) FJ854253 FJ854140 FJ854006 A. parviflorum, acc. Ethiopia, 1. Friis et al. 3844 (UPS) FJ854254 FJ854141 FJ854007 A. cf. parviflorum S. Moore E W. J. J. O. de Wilde & FJ854247 FJ854134 FJ854000 B.E.E de Wilde Dees 8874 (UPS) A. radicans Giirke Tanzania, E. Farkas & T. Pocs 86604 FJ854255 FJ854142 FJ854008 (UPS A. schimperi (Briq.) Perkins Ethiopia, W. Burger 695 (US) FJ854256 FJ854143 — FJ854009 Ach indet. cf. Ethiopia, M. Hedren 601 (UPS) FJ854257 FJ854144 FJ854010 schimperi Achyrospermum sp. indet. Burundi, J. Lewalle 1886 (UPS) FJ854258 FJ854145 FJ854011 Acrotome hispida Benth. South Africa, P. Herman 1990 (C)* EU138376 EU138299 FU138224 A. inflata Benth. Namibia, G. L. Maggs & L. Guarino EU138377 EU138300 EU138225 1072 (UPS)* A. pallescens Benth Namibia, /. Ortendahl 105 (UPS)* EU138379 EUl38302 EUl38226 Anisomeles indica Lk Kuntze Pakistan, E. Emanuelsson 2027 (S) FJ854259 FJ854146 FJ854012 A. malabarica (L.) Si ri Lanka, Fagerlind & Klackenberg FJ854260 FJ854147 FJ854013 343 (S) Ballota acetabulosa (L.) Benth. B. africana (L.) Benth. B. aucheri Boiss. B. integrifolia Benth. B. nigra L. subsp. ruderalis (Sw.) Briq B. lids (L.) Benth. B. undulata (Fresen. T Benth. Betonica alopecuros B. K. n B. macrostachya Wender. - officinalis L. B. scardica Griseb., acc. 1 B. scardica, acc. 2 Bostrychanthera deflexa Benth. Brazoria arenaria ll js i marrubiastrum (L.) on a ae annos Chelonopsis longipes C. moschata Miq. Greece, M. Bendiksby & A.-C. Scheen EU138342 . EU138365 EU138296 0412 (0)* South Africa, K. Bremer 247 (S) FJ854261 FJ854148 . FJ854014 Iran, S. Sabaghi s.n., 02.06.1993 (S) FJ854262 FJ854149 FJ854015 Cyprus, H. Lindberg s.n., a E 1939 (S) FJ854263 FJ854150 FJ854016 Greece, M. Bendiksby & A.-C. Scheen FJ854264 FJ854151 FJ854017 0431 (0 Greece, M. Bendiksby & A.-C. Scheen EF546935 EF546857 . EU138295 0420 (0)* Jerusalem, I. Amdursky m (US) FJ854265 FJ854152 FJ854018 Italy, S. Pani 2661390 (US) FJ 854088 Georgia, D. McNeal et al. = (C) FJ854266 FJ854153 FJ854019 Turkey, P. H. Davis & Hedge 31895 (C) FJ854320 FJ854221 FJ854106 cultivar, C. Lindqvist & V. A. Albert 357 AF502056 FJ854224 FJ854109 (UNA)* Greece, J. Ugelvig & L. S. Christiansen FJ854326 FJ854229 FJ854114 1048 Greece, J. D & L. S. Christiansen — FJ854327 FJ854230 FJ854115 1051 ( China, d merican Guizhou Bot. FJ854267 FJ854154 FJ854020 Exped. 1923 (A) U.S.A., M. W. Turner 25 (TEX)* EF546967 EF546890 FJ854021 Germany, A. Pedersen 14 (C) FJ854; FJ854155 FJ854022 FJ854156 FJ854023 Iran, K. H. E 50961 (C) FJ854269 EF. EF546861 FJ854024 apan, S. Okuyama & N. Maruyama s.n., D 1951 (UPS)* ultiv c P. D. Cantino 1429 (BHO) FJ854270 FJ854157 FJ854025 Volume 97, Number 2 2010 Scheen et al. Phylogenetics of Lamioideae Table 1. Continued. trnL-F rps16 Taxon Origin/voucher information trnL intron spacer intron Colquhounia coccinea Wall. Nepal, S. Einarsson et al. s.n., 29 EF546936 EF546858 . FJ854026 May 1973 (UPS)* C. elegans Wall. Thailand, C. F. van Beusekom & C. EF546937 EF546859 FJ854027 Phengklai 3008 (C)* Comanthosphace formosana Ohwi Taiwan, Cien-chang Hsu (S) FJ854271 FJ854158 FJ854028 C. japonica (Miq.) S. Moore, acc. 1 Japan, & S. Kobayashi 45908 (S) FJ854272 ]8541 FJ854029 C. j , acc. apan, Shigetaka Suzuki FJ854274 FJ854161 FJ854031 C. stellipila (Miq.) Briq. pan, T. Shimizu 12869 (S) FJ854273 FJ8541 FJ854030 Craniotome furcata (Link) Kuntze Nepal, O. Polunin et al. 5638 (UPS) FJ854275 FJ854162 FJ854032 — laciniata (L.) B Jordan, M. Kocher B-200 (U 3854276 FJ854163 FJ854033 wallichii Benth. in Stainton et al. 7748 (UPS) FJ854277 FJ854164 FJ854034 Caleopeis ipei Hoffm. France, E. Dahl s.n., 26 Aug. 1979 (O)* | EF5469. F FJ854035 pubescens r Poland. T. Tacik & M. Sychowa 366 (O)* EF. F FJ854036 G. speciosa Mill. Norway, T. Berg 04-01 (0) FJ854278 FJ854165 FJ854037 m javanicum (Blume) unknown, R. G. Olmstead 93-38* AF F FJ854038 Mitos haplostachya Hawaii, S. Perlman 14328 (NY)* AF502029 FJ854166 FJ854039 (A. Gray) H. St. John Isoleucas arabica O. Schwartz Yemen, M. Thulin et al. 8402 (UPS)* EU138380 EU138303 .— EU138227 somala (Patzak) Scheen Somalia, M. Thulin & A. M. Warfa 5395 EU138439 EU138362 . EU138285 (UPS)* Lagochilus cabulicus Benth. Pakistan, E. Emanuelsson 2456 (S) FJ854279 FJ854167 FJ854040 L. hirtus Fisch. & C. A. M Kazakhstan, /. O. Baitulin et al. s.n.,18 FJ854280 FJ854168 FJ854041 Sep. 1997 (UPS) L. ilicifolius Benth. Mongolia, T. Norlindh & T. Ahti FJ854281 FJ854169 FJ854042 29330 Lamiastrum montanum (Pers.) Austria, W. Till s.n., 24 May 1998 (WU) FJ854282 FJ854170 — FJ854043 Ehrend. Lamium album L. subsp. crinitum Iran, J. Bornmiiller 7947 (WU)* EF546932 EF546854 . FJ854044 (Monbret & Aucher ex Benth.) ennema L. tomentosum Willd. Russia, J. Klackenberg 820620-27 (S)* EF546933 EF546855 EUI38293 Leonotis leonurus (L.) R. Br. So ica, F. Venter & Eul38382 EUI38305 EUl38229 P. Vorster 171 (US)* L goin Iwarsson & Malawi, M. Iwarsson & O. Ryding EU138383 EU138306 EU138230 986 (UPS)* L oo (L) R. Br. var. Tanzania, R. Abdallah et al. 493 (UPS)* EU138386 — EU138509 EU138233 nepetifolia L. ocymifolia (Burm. f.) Iwarsson Botswana, R. Blomberg et al. 713 (UPS)* EU138389 EUI38312 — EUI38236 var. schinzii (Giirke) Iwarsson Dhire aiei L Argentina, T. M. Pedersen 16317 (UPS)* EF546930 EF546852 FJ854045 L. turkestanicus V. 1. Krecz. Kazakhstan, /. Roldugin € EF5469031 EF546853 FJ854046 & Kuprian V. Fissjun 5393 (S)* Leucas aspera (Willd.) Link Thailand, 0. Ryding 697 (UPS)* EU138395 EUI38318 E L. biflora (Vahl) Sm a, M. huarsson 610 (UPS)* — EU138396 — FU13839 — EUISEMS calostachys Oliv. us » ho PS)* EU138398 EU138321 EU138250 L. deflexa Hook. f. var. deflexa T ia, A. Hemp 4285 (0)* EU138405 — FU138253 L. flagellifera (Balf. f.) Giirke Yemen, Socotra, M. Thulin & EU138406 rus LN. i 8750 (UPS)* glabrata € Sm. ERR 0. Ryding 2351 (UPS)* 138407 EU138330 w L. inflata Be Ethiopia, M. Thulin et al. 3869 (UPS)* EUI38410 EUI38333 EU138257 L. jamesii ne ‘initia, ir Hedberg et al., Somalia 13841] EU138334 EU138258 Medicinal Plant Project 85 (UPS)* Annals of the Missouri Botanical Garden Table 1. Continued. GenBank accession no. trnL-F 16 Taxon Origin/voucher information trnL intron spacer intron L. lanata Benth. Nepal, Stainton et al. 661 (UPS)* EU138413 EU138336 138260 L. lavandulifolia Sm Palau, C. A. Salsedo 164 (US)* EU138414 EU138337 FEU138261 L. martinicensis Ones R. Br. Ethiopia, 0. ee et a € — EU138416 EU138339 .— EU138263 L. minimifolia Chiov. ia, M. Thulin & A. M. EUl138419 EUl38342 EUl38266 6706 (UPS)* L. sexdentata Skan Botswana, O. Ryding 2310 Et EU138424 EU138347 EU138271 L. spiculifolia (Balf. f.) Gürke Yemen, Socotra, M. Thulin EU138425 EU138348 EU138272 A. N. pd 8688 vecta L. stachydiformis (Benth.) Bri Ethiopia, K. Hylander et al. 97 uu EU138426 EU138349 EU138273 L. urticifolia (Vahl) Sm. Eritrea, 0. Ryding & Sileshi N. EU138427 EU138350 EU138274 var. urticifolia 1763 (UPS)* Leucosceptrum canum Sm. Nepal, C. T. Mason Jr. £ P. B. Mason FJ854283 FJ854171 FJ854047 y 3963 (US Marrubium alysson L. Italy, M. H. G. Gustafsson s.n., FJ854284 FJ854172 FJ854048 5 Apr. 1990 (UPS) M. peregrinum Greece, A. Strid 33875 (C) FJ854285 ND FJ854049 M. Meet as & Heldr. Greece, S. & B. Snogerup 15993 (UPS) FJ854286 FJ854173 FJ854050 M. vulgare Saudi Arabia, J. & O. Hedberg 92075 EU138443 EU138366 EU138294 VA qug (UPS)* Melittis melissophyllum L. ungary, M. E. Steiner et al. EF546929 EF54849 FJ854051 š 1127 (UPS)* icrotoena patchoulii hina, H. Y. Liang 66028 (US F J854052 (C. B. Clarke ex Hook. f.) pa = m E C. Y. Wu & S. J. Hsuan Moluccella aucheri (Boiss.) Pakistan, G. Popov 123 (C)* EUI38446 EUl38369 FJ854053 Scheen, ace. 1 " "Am acc. 2 Pakistan, K. H. Rechinger 54859 (S)* EU138447 EU138370 FJ854054 oe is : -A., W. C. Brumbach 7249 (S)* EUI38444 EU138367 FJ854055 xl pinosa Spain, Laza s.n., 16 June 1935 (S)* EU138445 EU138368 FJ854056 —— z at Nepal, Stainton et al. 3649 (UPS) FJ854288 FJ854175 FJ854057 egia erlangeri Gürke Ethiopia, M. G. Gilbert et al. EU138432 — EUl38355 EUl38279 O. fruticosa (Forssk.) “apaq l ¿cosa (Forssk.) Schweinf. Saudi Arabia, I. & 0. aan ia, . Hedberg 9218A EFU138433 EU138356 EU138280 O. modesta S. Moore rcm x G. Gilbert & D. Sebsebe EUI38437 EUl38360 EUl38283 ` PS E Panzerina lanata (L.) Soják, acc. 1 Russia, V. Reverdatto s.n., 24 July FJ854289 FJ854176 FJ854058 1927 (S) P. lanata, acc. 2 Mongolia, T. Norlindh & T. Ahti FJ854290 FJ854177 FJ854059 E 10044 (S) Paraphlomis javanica (Blume) China, Sino-American Guizhou FJ854291 ND FJ854060 " , acc. ] Bot. E: 1 ) rin 2 M J. F. Rock 1097 (US) FJ854292 FJ854178 FJ854061 iflorum ghanis! an, J. s (Benth.) Vved. L4 m FJ854293 FJ854179 FJ854062 e oe ee S € etd pap Apr. 1985 (UPS) Dien FJ854180 FJ854063 iesen & Ul 2 qa u Mi AR 38448 EUl38371 EU138292 Pp ae et al. 4782 (UPS)* U13849 EUI38372 EU138291 tuberosa en on C. Mathiesen & J. M. ien FJ854181 FJ854064 Phyllostegia glabra (Gaudich.) Hawaii Ld awaii, K Wood 3962 (NY)* AF502031 FJ854182 FJ854065 — — — — — — — — Volume 97, Number 2 Scheen et al. 197 2010 Phylogenetics of Lamioideae Table 1. Continued. GenBank accession no. trnL-F rps16 Taxon Origin/voucher information trnL intron spacer intron ysostegia intermedia (Nutt.) U.S.A., R. Dale Thomas 88861 (US)* — EF546948 EF546871 FJ854066 Engelm. & A. Gra P. virginiana (L.) Benth. U.S.A., B. E. Wofford 88-12 (US)* EF546961 — E FJ854067 Pogostemon glaber Benth. Nepal, Stainton et al. 8327 (UPS) FJ854296 FJ854183 FJ854068 P. heyneanus sia Sri Lanka, J. Klackenberg 100 (S) FJ854297 FJ854184 FJ854069 P. hirsutus Bent Sri Lanka, J. Klackenberg 51 (S) FJ854298 FJ854185 FJ854070 P. paniculatus Aa ) Benth. India, J. Klackenberg & FJ854299 FJ854186 FJ854071 R. Lundin 565 (S) Prasium majus L. M. Thulin 5752 (UPS) FJ854300 FJ854187 FJ854072 Pseuderemostachys sewerzovii Kazakhstan, N. P scheva s.n., FJ854301 FJ854188 FJ854073 (Herder) Popov 12 May 196. Rostrinucula dependens China, D. E. -— et al. 24415 (A) FJ854302 FJ854189 FJ854074 (Rehder) Kudô R. sinensis (Hemsl.) C. Y. Wu China, Sino-American Guizhou Bot. FJ854303 FJ854190 FJ854075 Exped. 40 (A) Roylea cinerea (D. Don) Baill. Nepal, O. Polunin et al. 837 (UPS)* EU138450 EU138373 EU138290 Rydingia integrifolia n Yemen, M. Thulin et al. 8161 (UPS)* EU138435 EUl38358 EUl38282 Scheen & V. A. A R. persica (Burm. f.) a 8 Iran, K. Nikookar s.n., 9 Sep. 1963 (S)* EU138438 EUl38361 EUl38284 V. A. Albert Sideritis dasygnaphala (Webb & Canary Islands, J. Barber 196 (TEX)* AF501993 — FJ854191 — FJ854076 Berthel.) Clos S. gomerae Bolle subsp. gomerae Canary Islands, J. Barber 256 (TEX)* AF502036 FJ854192 FJ854077 S. hyssopifolia L. Spain, J. Barber y AF502037 FJ854193 FJ854078 S. macrostachys Poir. Islands, J. Barber 254 (TEX)* AF502038 FJ854194 FJ854079 nta Romania, J. 2 (TEX)* AF502039 — FJ854195 FJ854080 S. romana L. Italy, J. Barber 209 (TEX)* 502040 FJ8541 FJ854081 S. syriaca L., acc. 1 Greece, J. Barber 210 (TEX)* AF335659 FJ854197 FJ854082 S. syriaca, ace. 2 Greece, M. Bendiksby & A.-C. J FJ8541 FJ854083 Scheen 0408 (O) Stachys aculeolata Hook. f. Kenya, Y. B. Harvey et al. s.n., FJ854305 FJ854199 FJ854084 Pie Oct. 1 1992 (C) S. aethiopica L. e, B. ux 2146 (UPS) FJ854307 FJ854201 — FJ854086 Š. affinis Bunge wei c. dius ist & V. A. Albert AF502041 FJ854202 FJ854087 359 (UNA)* S. alpigena T. C. E. Fr. ium 0. Ryding 2133 (UPS) FJ854309 F]854 FJ854089 S. arabica Hornem Israel, /. Gruenberg 685 (UPS) FJ854312 FJ854207 FJ854092 S. argillicola Sebsebe Ethiopia, /. Friis et al. 3104 (C AF502044 FJ854208 FJ854093 S. arvensis (L.) L. Canary Islands, N. Lundqrist 8157 (UPS) FJ854313 FJ854209 — FJ854094 S. byzantina K. Koch cultivar, C. Lindquist & V. A. Albert 356 AF502046 FJ854211 FJ854096 NA S. cassia (Boiss.) Boiss. Greece, 4 & B. Snogerup 14974 (UPS) — FJ854315 FJ854212 FJ854097 S. chamissonis Benth. U.S.A., H. N. Moldenke et AF502050 FJ854213 FJ854098 32097 (LL)* Š. coccinea Ortega cultivar : a & V. A. Albert 355 AF502048 — FJ854214 FJ854099 1. 911/97A (NYBG)* S. cretica L. ien A. Strid arl al. 4. : ) J854316 FJ854215 FJ854100 Š. debilis Kunth Ecuador, €. Jativa & C. pa 242 (US) FJ854317 FJ854216 — FJ8S410l S. graeca Boiss. & Heldr. Greece, K. H. Rechinger 16887 (U FJ854306 — FJ854200 — S. grandidentata Lindl. Chile, W. J. Eyerdam 10081 (US) FJ854318 FJ854217 vim S. hyssopoides Benth. South Africa, E. Retief 1080 (US) FJ854319 — FJ834218 FJ S. lavandulifolia Vahl Raj ES & A. G. Jensen F5020 FJ854219 — FJ854 198 Annals of the Missouri Botanical Garden Table 1. Continued. GenBank accession no. trnL-F Taxon Origin/voucher information trnL intron spacer intron Š. lindenii Benth. Mexico, R. Torres C. & P. Tenorio AF502054 FJ854220 FJ854105 L. 4602 * S. maritima Gouan Romania, I. Gergely 3362 (US) FJ854321 FJ854222 FJ854107 S. nephrophylla Rech. f. Iraq, K. H. Rechinger 11250 (WU) FJ854322 FJ854223 FJ854108 S. pilosa Nutt. U.S.A., H. Hapeman s.n., 30 July 1938 FJ854311 FJ854206 FJ854091 (UPS) Š. plumosa Griseb Greece, S. & B. Snogerup 15337 (UPS) — FJ854310 FJ854205 FJ854090 Š. quercetorum A. Heller U.S.A., G. K. Helmkamp et al. 2153 F502042 FJ854225 FJ854110 (UTC)* Š. recta L. MN P. Schénswetter 2517 (WU) 3854323 FJ854226 FJ854111 S. recta subsp. subcrenata Croatia, G. Schneewis et al. 6268 (WU) FJ854330 FJ854233 FJ854118 (Vis.) Briq. S. riederi Cham. Japan, H. Takahashi 2950 (C) 3854314 FJ854210 FJ854095 = NAME MAS Mexico, D. E. Breedlove 55575 (TEX) FJ854324 FJ854227 FJ854112 S. rugosa Aiton South Africa, W. J. Hanekom 2487 (US) FJ854325 FJ854228 FJ854113 S. setifera C. A. Mey. Iran, J. S. Andersen & I. C. Petersen J854328 FJ854231 — FJ854116 115 (C) S. spinosa L. Greece, M. Bendiksby & A.-C. Scheen FJ854329 FJ854232 . FJ854117 “za dg 0422 (0) S. swainsonii Benth. Greece, A. Strid et al. 39692 (C)* AF502062 FJ854234 FJ854119 S. sylvatica L. cultivar, C. Lindqvist & V. A. Albert 358 AF50; FJ854235 FJ854120 ' (UNA)* Stenogyne rugosa Benth. Hawaii, C. Lindqvist & V. A. Albert AF502067 FJ854236 FJ854121 DN 40 (NY)* Suzukia luchuensis Kudó Japan, S. Tawada & S. Hatusima FJ854331 FJ854237 FJ854122 18179 (US) & dd aie s iet „Taiwan, C-C. Liao et al. 564 (A) J854332 FJ854238 FJ854123 on ra hispidula (Michx) Baill. U.S.A., V. E. 3. 97-143 (GH)* ^ EF546970 ^ EF546893 FJ854124 uspeinanta brahuica (Boiss.) Tran, K. H. & F. Rechinger 4701 (US) FJ854333 FJ354239 FJ854125 T. š persica (Benth Briq. Iraq, K. H. Rechinger 9604 (S) FJ854334 FJ854240 F]854126 scutellarioides (Engelm. 1 M. H. Mayfield & G. Nesom EF546971 EF546894 F]854127 & A. Gray) M. W. Turner 970 (US)* Wiedemannia x multifida (L.) Benth. Thay. J. & F. Bornmüller 14536 (S) — F]854335 FJ854241 FJ854128 Call americana ; CM cultivar, K-0818400507 (K)* AJ505535 — AJ505535 — AJ505412 ^. Japonica Thun cultivar, K-1934-12904 (K)* Mie lbs ) AJ505536 AJ505536 AJ505413 ir Wagstaff s.n. (BHO)* AJ50 AJ505530 505411 ymaria Phili C. dic Benth. Ñ 38542. FJ854131 FJ853997 š wu ds China, C. Wang 33150 (US) FJ854245 FJ854132 FJ853998 unioni W 356 (BHO)* 5055 AJ505526 AJ505406 Gmelina hystrix Schult. ex Kurz cultivar, K-381-74-02999 (K)* 505401 Haumaniastrum kata. ngense cultivar, K-1995.1 197 Chase 13330 (K)* — = 7 (S. Moore) J. Duvign. & Plane > (K)* AJ505540 AJ505417 Hypenia macrantha (Benth.) Harley At Sic mds Á " M 150 (K AJ505445 AJ AJ505336 D. Don) Kad e (BKF,K,TCD* — AJ505454 AJ505454 AJ505342 Lantana camara CV azquez Yanes — * , Lavandula — Webb & Berthel. Upson 299 E AP231804 — AF231884 AF225294 Melissa Nepeta fissa C. A. Ñ. Origanum v HO)* Jamzad & Nita 80486 (TARI)* cultivar, K 0 40-1981, Chase 5529 AJ505430 Volume 97, Number 2 Scheen et al. 199 2010 Phylogenetics of Lamioideae j Table 1. Continued. GenBank accession no. trnL-F rps16 Taxon Origin/voucher information trnL intron spacer intron toma annamense Suddee et al. 1028 (BKF)* AJ505479 AJ505479 AJ505361 (G. Taylor) A. J. Paton Plectranthus buchananii Baker cultivar, K-1970-3559, Brummitt AJ505501 AJ505501 AJ505379 11597 (K)* P. helferi Hook. f. Chase 9768 (K)* AJ505552 AJ505552 AJ505429 Prostanthera nivea Benth. M. W. Chase 6980 (K)* AJ505524 AJ505524 AJ505403 P. petrophila B. J. Conn M. W. Chase 6975 (K)* AJ505525 AJ505525 AJ505404 Pycnostachys reticulata (E. Mey.) cultivar, K-1999-2425, Nat. Bot. AJ505516 AJ505516 AJ505395 Benth. . S. Africa (K)* Salvia guaranitica A. St.-Hil. cultivar, K-1973-14217 (K)* AJ505549 AJ505549 AJ505421 ex Benth. Scutellaria hirta Sm. Greece, M. Bendiksby & EF546927 EF546847 . EU138289 A.-C. Scheen 0411 (0)* S. sieberi Benth. Greece, M. Bendiksby & EF546928 EF546848 . EU138288 A.-C. Scheen 0418 (O)* Tectona grandis L. f. Waimea 73P172* AJ505528 AJ505528 AJ505408 Teucrium alpestre Sm. Greece, M. Bendiksby & AJ854242 AJ854129 AJ853995 A.-C. Scheen 0426 (O) T. scorodonia L. Norway, A.-C. Scheen 0412 (0) AJ854243 AJ854130 AJ853996 Thymus serpyllum L. var. cultivar, K-1975-1177, AJ505544 AJ505544 AJ505423 citriodorus (Schreb.) Becker Chase 13331 (K)* Verbena officinalis L. H. Kalheber 78-506 (GB)* AF231885 AF231885 AF225295 Vitex trifolia L. TCMK 15, Chase 8757 (K)* AJ505539 AJ505539 AJ505416 ND, sequences not determined. » I f f * Sequences that were not new to this study were retrieved from GenBank and were originally published by Lindqvist and Albert (2002), Paton et al. (2004), Wallander and Albert (2000), Scheen et al. (2008), or Scheen and Albert (2009). the analysis, using the data matrix without indels circumscribed at this time, although in some cases coded, were: general time reversible model, estimated they may occupy key phylogenetic positions. No gamma shape parameter = 1.36, four substitution rate subtribal names were pi p , princi lly because categories, empirically derived equilibrium state morphological characteristics rendered this impracti- frequencies ([A] — 0.34185, [C] — 0.16969, ([G] cal (e.g., within tribe Pogostemoneae Briq. and tri 7 0.18884, [T] = 0.29961), empirically derived Stachydeae Dumort.). Names for tribes were selected proportion of invariant sites = 0.164, starting tree following the rules of the International Code of determined by BIONJ neighbor-joining (Gascuel, Botanical Nomenclature (McNeill et sae 1997), and tree optimization using nearest neighbor Authorship, priority, and valid A > Í names interchange (NNI) rearrangements. Using the same were determined by examining pen n caa web server, a bootstrap analysis of 100 replicates was and by consulting several sources ( m : ges > performed to estimate internal robustness of the data. 1984; Reveal, 2007, pers. comm.; Govaerts et at. 2010; International Plant Names Index, 2010). TAXONOMY RESULTS AND DISCUSSION Only monophyletic were selected for Suprageneric adici dO of Lamioideae. Alignment of the 197 Lamiaceae and Verbenaceae: The criterion used was to circumscribe entities at the trnL-F. sequences resulted in a data matrix of $t tribal level (mostly with high jackknife support [JAC] characters, including indels and missing we i > 80%) that would be practical at present, with no simple indel coding in SeqState, 253 indels = attempt made to classify every clade that could have coded as present or absent (or missing), peii oe 2d equivalent hierarchical status. In order to avoid matrix size to 1494 characters. The rps] matrix : Phylogenetic redundancy, no monogeneric tribes were — an aligned length of 1201 bp including indels an ° 200 Annals of the Missouri Botanical Garden i Long-exserted stamens O Fieshy fruits Figure 1. Strict consensus of 256 MPTSs f in F region and rps16 intron. Jackknife values are given abov nony y i f indel o A 1 MPTs resulting from a parsimony analysi : © branches. Branches that coll psed in the strict trix of the trnL- nens of 1728 ysis where indels that were not coded are shown as stippled lines. M jor clades are X — = AP: saan new suprageneric classification of Lamioideae s.l. —A. Outgroups Colino Wall., and Porepblemio (Prin) Pas, Ries Wk. Cr ace — er - E E sd - and tribes Phlomi , Lamieae, Marrubiese, and Leucadeae. Non-Stachys taxa nested within tribe Stachydeae (B) are in U Did pa ied to in the text ( ichyd leae). Four selected EX i. t e ET shapes on the figure: black bra fica RA AR Skan also has a bearded posterior corolla li ph net re ). Note that Lois sexdentata p but that š ) ylogenetic resolution among the three ni sir = this s Acrotome species i Pg is not indicated on the figure due to lack of Volume 97, Number 2 Scheen e t al. 201 Phylogenetics of Lamioideae B Figure 1. Continued. missing data. SeqState coded 192 indels, which increased the matrix size to 1393 characters. The concatenated matrix had 2442 characters when indels were not coded and 2887 characters when indels were coded and included as binary characters. The maximum parsimony analysis of the concatenated matrix resulted in 1728 most parsimonious trees (MPTs) of 2302 steps with a consistency index (CI) of 0.61 and a retention index (RI) of 0.88 when indels were not coded and 256 MPTs of 3103 steps when indels were coded (CI — 0.59, RI — 0.87). The results of the parsimony analyses with and without indel coding were largely congruent (Fig. 1). — X Spinose/spinescent bracteoles O Fieshy fruits egopÁAu»eis Maximum likelihood analysis yielded an entirely consistent tree with that derived from parsimony, and most of the same branches supported by parsimony analysis were also supported by the maximum likelihood bootstrap results (results not shown). In all analyses, Cymaria Benth. was strongly supported (by jackknife and bootstrap resampling) as sister to Lamioideae plus Pogostemonoideae. This clade was in turn sister to Scutellaria L. (representing Scutellarioideae). In all analyses, members of the former subfamily Pogostemonoideae grouped with three members of Lamioideae (Achyrospermum Blume, Craniotome Rchb., and Microtoena Prain), which C Continued. Figure 1. therefore rendered subfamily Pogostemonoideae para- phyletic. Lamioideae s. str., a much larger group, formed a well-supported clade. The following major groups within this latter clade were supported (by jackknife and trap resampling) in all analyses: (1) a clade consisting of Gomphostemma Wall. ex Benth., Bostrychanthera Benth., and Chelonopsis Miq. Annals of the Missouri Botanical Garden c c i e Mee e ——————————— rae a edd | XX. Spinose/spinescent bracteoles |) Posterior corolla lip bearded | n d əəeəptuuolud ct oeajule"] eeeiqnaew eeepeone] as sister to the remaining taxa; (2) a clade of the North American genera Synandra Nutt., Brazoria Engelm. ; A. Gray, Warnockia M. W. Turner, and Physostegia Benth.; (3) the genus Galeopsis L.; (4) members of Stachys subg. Betonica (L.) R. Bhattacharjee: ( Melittis L. sister to a large clade of Stachys, Sideritts. and a number of smaller or monotypic genera; (6) the Volume 97, Number 2 Scheen et al. Phylogenetics of Lamioideae genus Phlomis, including members of Eremostachys Bunge, Notochaete Benth., and Pseuderemostachys Popov; (7) Lagochilus Bunge ex Benth. sister to the smaller genera Chaiturus Willd., Leonurus L., and Panzerina Soják; (8) the genus Lamium L. sister to Lamiastrum Heist. ex Fabr. plus Wiedemannia Fisch. & C. A. Mey.; (9) a clade of Ballota L., Marrubium L., ) Benth. ex Endl., — Isoleucas O. E Galeopsis and incide of Stachys subg. Betonica formed a group, although not supported by resam- pling, which was sister to the Melittis-Stachys s.l. group (Fig. 1 CIRCUMSCRIPTION OF LAMIOIDEAE Scutellaria. Scutellaria is a large cosmopolitan genus of ca. 360 species belonging to the subfamily Scutellarioideae. This subfamily also includes the genus Tinnea Kotschy & Peyr. (ca. 20 spp.) as well as the monotypic genera Holmskioldia Retz., Wenchengia C. Y. Wu & S. Chow, and Renschia Vatke, all of which are Old World tropical. Although Scutellarioideae is represented here by only two Scutellaria species and our outgroup sampling is otherwise relatively limited, our results corroborate earlier evidence (Wagst Olmstead, 1997; Wagstaff et al., 1998; Lindqvist & Albert, 2002) for the subfamily being closely related to Lubiidens in the classical sense (i.e. as circumscribed by Harley et al., 2004). The exact circumscription of Lamioideae still remains a problem. The first issue regards the status of pogostemonoid genera, formerly classified in a separate subfamily, Pogostemonoideae (Cantino et al., 1992). Morphological considerations led Harley et al. (2004) to subsume the pogostemonoids within a larger Lamioideae, and we provide here the first phyloge- netic evidence corroborating this view (see below). es the first in a enigmatic genus Cymaria is intercalated “ei . e and Lamioideae plus pogostemonoids. Cymaria. In all of our phylogenetic analyses, the broader ion — is ir — as e monophyl n (99% JAC; Fig. 1A). Dyndritt is a -— genus comprising two to three species from Southeast Asia. ymaria was not classified to a particular subfamily of Lamiaceae by Harley et al - 0006. although sugges- tions for pl based on the results of a niii phylogenetie analysis (Cantino et al., 1992). the past inf Other taxa unplaced by Harley et al. (2004) may be relevant to our interesting phylogenetic resolution of Cymaria. Cantino et al.’s (1992) classification, now superseded by Harley et al. (2004), placed Cymaria in a group together with the monotypic genera Acrymia Prain, Garrettia H. R. Fletcher, and Holocheila (Kudó) S. Chow, all occurring in areas of southeastern Asia. Cymaria shares a — inflorescence structure with A tia (Harley et al., 2004: 189) and pb een with Garrettia & Cantino whe Harley et al., 2004: 189-190). However, DNA data appear to place Holocheila within Lamioideae (R. G. Olmstead, unpubl. data; see Harley et al., 2004: 190), while phylogenetic studies of ndhF cpDNA sequences corroborate that Cymaria is sister to the Lamioideae clade (R. G. Olmstead, pers. comm.). One possible link between these taxa and pogostemonoid taxa may be inflorescences with prominently pedunculate cymes, a trait that is also seen in Craniotome and Microtoena. However, more data are required, especially from the tropical Fia a pe — apu Gar- rettia, luded here), in order to assess the possibility of assigning Cymaria and perhaps some of the other genera to Lamioideae or to a subfamily of their own. TRIBE POGOSTEMONEAE As stated above, our molecular phylogeny confirms the morphologically based view that lamioid and gostemonoid taxa are intermingled, and in fact together form a highly supported monophyletic group (99% JAC; Fig. 1A). Previous phylogenetic studies did not succeed in verifying the status of Lamioideae Pogostemonoideae as separate taxa. Only two cladistic treatments have included more than one representative of Pogostemonoideae (Cantino, 1992a; agstaff et al., 1998). In Wagstaff et al. (1998), Lamioideae and Pogostemonoideae were monophylet- ic sister taxa, although the pogostemonoid clade only received low bootstrap support. In Cantino (1992a), Pogostemonoideae was sister to a Lamioideae—Nepe- toideae clade. However, in our analyses, which are much better sampled, there is no — for a monophyletic subfamily Pogostemonoi The pogostemonoid labiates fall into two weil groups that, together with three genera of subfamily Lamioideae (Achyrospermum, Craniotome, and Micro- toena), form a highly supported group (89% JAC; Fig. 1A). The two pogostemonoid genera Anisomeles R. Br. (three spp.) and Pogostemon Desf. (ca. 80 spp.) are sister taxa with high support (100% JAC), corroborating the results of previous morphological Annals of the Missouri Botanical Garden studies by Cantino (1992a, b). A close relationship between these two genera had never been suggested prior to Cantino's work. However, Briquet (1895— 1897) grouped Anisomeles with Achyrospermum, Craniotome, and Microtoena, but did not recognize their close — to MAUS (Fig. 1A). In all our anal 1 and n group with monotypic E and Mio fe spp.) with high support (99% JAC). All species within this clade are mostly tropical East Asian, although Anisomeles species also occur in the West Indian Ocean and Pogostemon in Africa, and Craniotome and P. glaber Benth. reach the Himalayas. The monotypic Le Sm. Comantho- sphace S. Moore (three to four spp.), and Rostrinucula Kudó (two spp.) form another highly supported clade (100% JAC) within which Comanthosphace and Rostrinucula are well supported as sister taxa (99% JAC). This group is also primarily tropical East Asian, with some species reaching temperate East Asia, and Leucosceptrum reaching the Himalayas. These three pogostemonoid genera are highly supported as sister to the lamioid genus Achyrospermum (ca. 25 spp.) in all “re ss AS Jue 1A). Although only Afric: are includ ed in some e of de se also occur in tropical East Asia and the Himalayas. The non-monophyly of the pogostemonoids is further corroborated by a general lack of morpholog- ical synapomorphies. Although the same lack of morphological synapomorphies applies to the group that also includes three lamioid genera, there are derived morphological traits that corroborate the split of the pogostemonoid labiates into two groups. Anisomeles and Pogostemon both have minute leaf- epidermal glands with unicellular caps, bearded stamen filaments, and a lustrous pericarp (Cantino, 19922). These two genera also share characters of leaf epidermal anatomy that — them from other labiates (Cantino, 1990). A Ithough no morphological character is found that may serve as a synapo for all four genera, Ci , Anisomeles, and Pogostemon all have glossy idi (Harley et al., 2004). Furthermore, Craniotome and Pogostemon both have very small nutlets, a character they share with two et al., 2004). The latter two genera are not included in this study (but see below). There are also morphological characters that e a close Sip among the fes of the +h ace, Leuco. de and Rostrinucula nd the inicia Achyrospermum (Ryding, 1995). The entire clade deviates from the other pogostemonoids as well as most other lamioids in lacking a sclerenchyma region in the fruit pericarp (Ryding, 1994b, 1995). The shared presence of druses and many cells with pitted to scalariform wall ornamentation in the mesocarp is also a rather uncommon condition. Even though there are no clear morphological synapomorphies for all genera collectively, we do suggest that this molecularly well-supported group be recognized at the tribal level. The name Pogostemoneae is already available (see Appendix 1). In a phylogenetic e e the imL-F "i er ae Sen sce it iind Mies based on these results, and the strong morphological similarities of Colebrookea to this group, these two genera should also be included in Pogostemoneae. Excluding the three lamioid genera Achyrosper- mum, Craniotome and Microtoena, which group with former Pogostemonoideae as mentioned above, all other members of Lamioideae form a highly supported clade, the Lamioideae s. str. (100% JAC; Fig. 1A). TRIBE GOMPHOSTEMMATEAE Within Lamioideae s. str., two temperate East Asian genera, Bostrychanthera and Chelonopsis, and the tropical East Asian genus Gomphostemma form a highly supported clade (95% JAC), which is sister to all other taxa. In contrast to tribe Pogostemoneae, some species of all three of these genera have conspicuously large flowers. Both Bostrychanthera and Gomp stemma have fleshy fruits and have previously been circumscribed as belonging to the fleshy-fruited tribe Prasieae Benth., whereas Chelonopsis was circum- scribed as elogia to subtribe Melittidinae Endl. (Bentham, 1848, 1876; Briquet, 1895-1897; see also tribe Synandreae Raf., below). Molecular studies show both of these suprageneric groups to be polyphyletic (Lindqvist & Albert, 2002; Scheen et al., 2008). The current molecular iocis confirms a close relation- ship between the fleshy-fruited Gomphostemma and the dry-fruited Chelonopsis as suggested by studies of Lamiaceae fruit pericarp structure (Ryding, 1994c). Furthermore, Chelonopsis and Gomphostemma deviate from other lamioid labiates by having pollen with branched columellae (Abu-Asab & Cantino, 1994). It is not known whether or not Bostrychanthera species share this character. However, the molecular data show that Chelonopsis is sister to Bostrychanthera rather than b directly shir to - Comphossenma (Fig. na of Chelonopsis to be particularly shaile to that ef Pi strobilinum Wall. and G. wallichii Prain, neither of which were included in the current phylogeny. Two morphological characters corroborate the sister "e: Volume 97, Number 2 2010 Scheen et al. Phylogenetics of Lamioideae lax inflorescences of long-pedunculate cymes and bearded stamen-filaments (Harley et al, 2004) hostemma, on the other hand, has denser and short-pedunculate inflorescences and lacks the beard- ed stamen-filaments (Harley et al., 2004). Thus, the dry fruit of Chelonopsis represents a reversal from a fleshy fruit in the common ancestor to these three genera. Moreover, in Chelonopsis, the fruit mesocarp (which is fleshy in B ) L +h al ph " dd Lcd by g y I 11 y Er Only two species of Chelonopsis and one species of Gomphostemma and Bostrychanthera were included in our analyses. In the future, more species should be investigated to elucidate whether or not Bostry- chanthera (two spp.), Chelonopsis (16 spp.), and Gomphostemma (38 spp.) represent monophyletic groups. We recognize these genera as a new tribe Gomphostemmateae Scheen & Lindqvist to reflect the distinct floral traits of the group (see Appendix 1). GENUS COLQUHOUNIA The large group of lamioid labiates that is sister to Gomphostemmateae receives moderate resampling support (78% JAC; Fig. 1A). Two (of the ca. six) species of the Asian genus Colquhounia Wall. form a moderately supported monophyletic group (77% JAC) that is sister to all remaining taxa. Species of unia have a corolla tube that is strongly dilated in the distal part and nutlets winged at the apex (Harley et al., 2004). The latter character state is rare in Lamioideae. Although Colquhounia most likely occupy a phylogenetically distinct position within ioideae, we have at this time chosen to leave this clade unclassified at the tribal level. TRIBE SYNANDREAE The four North American genera Brazoria, Physo- stegia, Synandra, and Warnockia form a highly supported monophyletic clade (100% JAC; Fig. 1A). A previous study shown that a fifth American genus, Macbridea Elliott ex Nutt., is a close relative to the other four (Scheen et al., 2008). The monophyly of these five genera is corroborated by a single morphological synapomorphy: a racemose inflorescence with sessile or very shortly pedicellate flowers. All five genera are characterized by having villous stamen filaments (Harley et al. 2004). Although this character may serve as a synapomorphy for the group, it is not entirely unique to the group. Hairs are also present on the stamen filaments of, e.g. Pogostemon, Anisomeles, and Chamaesphacos Schrenk ex Fisch. & C. A. Mey. (Harley et al, 2004) F , all five genera represent monophyletic groups that are easily distinguished morphologically (Scheen et al., 2008). The monotypic genus Synandra is sister to the other genera and differs from them by having 4-lobed calyces and membranous and long- petiolate leaves that are pubescent on both surfaces, whereas Brazoria (two spp.), Macbridea (two spp.), : Li mostly sessile leaves (Cantino, 1982). Together with the European genus Melittis and the Asian genus Chelonopsis, the five North American endemic genera have been circumscribed as subtribe Melittidinae (Bentham, 1848, 1876; Briquet, 1895- 1897; see also Cantino, 1985). The current molecular phylogeny shows this group to be unnatural because Melittis is the sister taxon to the large Stachys clade (see tribe Stachydeae, below; Fig. 1B) and Chelonop- sis groups within an entirely different Asian clade (see tribe Gomphostemmateae, above; Fig. 1A). The mo- lecular data therefore corroborate the conclusions of several previous studies of morphology, anatomy, and karyology that subtribe Melittidinae should be abandoned (Cantino, 1985; Abu-Asab & Cantino, 1987; Ryding, 1994a). Instead, the five North American endemic genera are circumscribed as tribe Synandreae (Scheen et al., 2008). The current molecular phylogeny does not show a single genus as sister to the Synandreae. Instead, this group of North American endemics is supported as the sister to the majority of the taxa in Lamioideae s. str., excluding only tribe Gomphostemmateae and the genus Colquhounia (Fig. 1A). Although members of Gomphostemmateae and Colquhounia are East Asian, it is not possible to conclude how Synandreae arrived in North America, whether via a transatlantic or our results do migration into N that of the Stachys clade (see tribe Stachydeae, below). Thus, there have been at least two separate invasions of North America by lamioid labiates. The evolutionary histories of Synandreae and the Stachys clade differ greatly after their establishment in North America. The Stachys clade radiated into a morpho- logically and ecologically diverse group that spread farther into South rica and the Hawaiian archipelago (Lindqvist & Albert, 2002). The Hawaiian labiates alone comprise ca. 59 species and show a remarkable morphological and ecological variation, albeit with low levels of DNA sequence variation (Lindqvist et al., 2003). The 19 species of Synandreae do not show a similar radiation. Most of the taxa have restricted distributions and four of the five genera comprise three or fewer species (Harley et al., 2004). The exception is the more species-rich genus Annals of the Missouri Botanical Garden Physostegia. Although many of the 12 species have tolerate a broad ue of 2. acidity — nes howe owever Hh s low d can bed be described as kakidkacopie adi 1982). The low level of morphological variation is mirrored by low levels of DNA sequence variation (Scheen et al., 2008). The large sister clade of the Synandreae receives distinguished from the rest of Lamioideae in having fruit exocarp strongly differentiated into two types of cells, a thin-walled a thick-walled type (Ryding, 1995). However, the exocarp differentiation character is very homoplastic. Ryding (1995) has also recorded a weak and vague differentiation of the cells in the exocarp of Microtoena, which de well outside this clade in Pogostemoneae (Fig. 1A), but in this genus, the ee ae cells diverge in being ged in large gro GENERA BETONICA AND GALEOPSIS All included representatives of Stachys subg. Betonica form a strongly supported clade separate from all remaining members of Stachys (100% JAC; Fig. 1B). The five included species, and about 10 other Stachys species distributed in western Eurasia, are morphologically distinct from the remainder of Stachys and have at various times been assigned to a separate genus Betonica L. (e.g., Dumortier, 1827; Bentham, 1829; Reichenbach, 1830-1832; Cosson & German, 5455. Morphologically, es is rev e EE a persistent rosette of leaves, e stems bid i — sessile flowers, flowers and bracteoles with road and hardened base, and anther cells that are iuc (Ball, 1972; Bhattacharjee, 1980 980). Also, phytochemistry supports the distinction between Betonica and remaining Stachys species (Tomas- Barberan et al, 1992). An ostensibly great pollen similarity reported between Betonica and Stachys (Krestovskaya & Vasileva, 1997) was likely due to limited taxon sampling; no other lamioid genera were previously suggested (Lindqvist & Albert, 2002), our results clearly E" that the genus Betonica L. should be reestablishe Within the Betonica clade, no clear i" between the two sections Betonica (L.) Benth. and Macrostachya R. Bhattac ular data. Betonica alopecuros L., howev. ever, is sister to the remaining four species (Fig. 1B). This species is morphologically distinct with yellow flowers with a bifid upper corolla lip, and an annulate corolla tube (Ball, 1972; Bhattacharjee, 1980). Our results strongly support monophyly of Galeopsis (100% JAC; Fig. 1B). Galeopsis comprises 11 annual species, all with their center of diversity in Europe. There are two clear morphological synapomorphies for this genus: the presence of two conical protuberances near the base of the anterior lip of the corolla, and anthers dehiscing by two valves, of which the upper is fimbriate (Townsend, 1972; Harley et al., 2004). À comprehensive phylogenetic study of Galeopsis will be published elsewhere (Bendiksby et al., unpubl.). Both the clade comprising Betonica and Galeopsis, as well as its sister relationship to tribe Stachydeae, i is not supported with resampling and is retained onl strict consensus of the indel-coded analysis (Fig. 1B). It should be noted, however, that Betonica and Galeopsis share the same basal chromosome number (x = 8; Goldblatt & Johnson, 2006), and that flavonoid p- coumaroyl glucosides are present in both Betonica and subgenus Galeopsis (Tomas-Barberan et al. 1992) ELM it was an unexpected result that Galeopsis d be more closely related to Betonica than to asha and Lamiastrum, with which it has been classified in most traditional classifications; e.g. Galeopsis, Lamium, and Lamiastrum were classified as subtribe Galeopsidinae Dumort. based on the shared feature of a swollen corolla tube (Dumortier, 1827). use of the uncertain positions of these two genera in our current molecular phylogeny, and in order to avoid phylogenetic redundancy, we have chosen to leave the genera unclassified at the tribal level here. TRIBE STACHYDEAE The Melittis. distributed i Europe and -— Asia, is strongly supported as sister to the Stachys s.l. clade (100% JAC; Fig. 1B). We have chosen to re tom cognize this greater clade as Stachydeae (see Appendix 1). It should be noted, however, that the perennial herb, Melittis melisso- phyllum L., is clearly distinct from the Stachys s.l. clade, characterized by very large flowers and a 2- lipped calyx, with the upper lip entire or irregularly dentate (Harley et al., 2004). hys, as currently circumscribed, — approximately 300 species (Harley et al., 2004). It is the largest genus of subfamily Lamioideae and among the largest genera of the entire Lamiaceae. Results from our molecular phylogenetic analysis confirm that the subcosmopolitan genus Stachys represents an unnatural group in strong revision (Lindqvist & Albert, 2002; Fig. 1B). Lind- qvist and Albert (2002) have previously shown that v Volume 97, Number 2 2010 Scheen et al 207 Ph ylogenetics of Lamioideae the lamioid genera Sideritis, Prasium L., Phlomi- doschema Vved., and the Hawaiian endemic labiates (Haplostachys (A. Gray) Hillebr., Phyllostegia Benth., and Stenogyne Benth.) are nested within Stachys s.l. Our present results, which include a more extensive sampling of mostly Old World species, corroborate these findings and demonstrate that the Asian genera hai (Fig. 1B), relationships that have not been previously suggested. Our molecular data subdivide the large (Fig. 1B): clade A (99% JAC) comprises the Hawaiian endemics, temperate East Asian Suzukia, and largely New World Stachys species, including the North American Stachys, as well as a clade of sub-Saharan African species, and clade B (100% JAC) includes the genera Sideritis, Prasium, Phlo ma, Thuspeinanta, Chamaesphacos, and Old wail Sta- chys nem many small genera embedded within tribe ala vary in their degree of morphological distinctness. The genus Suzukia includes two species of creeping perennial herbs that are endemic to forests of Taiwan and the Ryukyu Islands (Harley et al., 2004). Monophyly of Suzukia is only weakly su by our cpDNA phylogeny (62% JAC; Fig. 1B, clade A), and the genus may be difficult to distinguish oo from related taxa. An orbicular leaf e, a moderately we posterior corolla lip eet et P 2004), and a haploid chromosome number of = 17 (Goldblatt & ibas 2006) may nd synapomorphic characters for the genus Haplostachys (five spp.), Phyllostegia (ca. 34 spp-), and Stenogyne (ca. 20 spp.) have been classified together with Prasium, s and Gom- ma as tribe Prasieae (Bentham, 1848) or as subfamily Prasioideae (Briquet, 1895-1897) because of the fleshy fruits borne by these genera (except Haplostachys). Although the Hawaiian labiates and the Mediterranean monotypic Prasium belong in the Stachys s.l. clade, they group in separate clades (A B, respectively; Fig. 1B), and it is clear that Lamioi Evolution, below). Prasium majus L., a small, usually glabrous shrub, is resolved as sister to a clade comprising species of Stachys, Sideritis, Phlomi- dose , Thuspeinanta, and Chamaesphacos (Fig. 1B, clade B). The western to central Asian Phlomi- doschema attains a more derived position in this clade and is diseriminated by a woody base, a dense cover of branched hairs, entire leaf margins, calyx — accrescent in fruit, and few-flowered cymes. The perennial monotypic Phlomidoschema and two species of Stachys form a polytomy that also includes a strongly — clade comprising the two western Asian genera C nd. Thopia (100% TAC; Fig. 1B). Both Chamaes and Thuspeinanta are annuals bearing very narrow nutlets and short stamens. The monotypic Chamaesphacos is characterized by spiny leaf margins, a long corolla tube with a short and flat upper lip and anterior lip deflexed, and ARRE nutlets (Harley et ). Chamaesphacos has previously been ñumqisaed with Craniotome, Anisomeles, Achyrosper- ` and C unia based on the shared presence a short, flat, and glabrous upper corolla lip ME 1876). The two species of Thuspeinanta are characterized by being annual and having bracteoles that recurve in fruit, calyx lobes that are inflated in fruit, and confluent anther-thecae (Harley et al, 2004) Thuspeinanta has previously been classified with Acrotome, Marrubium, and Sideritis tribe Marrubieae Vis. (Bentham, 1876; Briquet, 1895-1897). In our molecular phylogeny, Thuspei- nanta is paraphyletic with respect to Chamaesphacos and may hold a derived position within clade B of the Stachys s.l. clade (Fig. 1B). All included members of Sideritis are confined to clade B (Fig. 1B). Both Sideritis and Stachys are large non-monophyletic genera within subfamily Lamioi- deae (Fig. 1B), and both show an extensive morp logical, karyotypic, and ecological diversity that overlap (Harley et al., 2004). Sideritis (ca. 140 spp.), which is found from Macaronesia to western China with a circum-Mediterranean center of distribution, is characterized by having verticillasters in terminal spikes, corolla tube shorter than calyx, posterior corolla lip almost flat, and confluent anther thecae (the latter feature is also seen in Thuspeinanta; Harley et al, 2004) In their study of the origin of Macaronesian Sideritis, Barber et al. (2002) assu the genus Sideritis to be monophyletic, but following Lindqvist and Albert (2002), we show here that Sideritis as currently circumscribed is paraphyletic, and that phylogenetic Ms of Sideritis are complex. Furthermore, e of the sectional subdivi- sions of Sideritis mapa 1891-1895) or Stachys (Bhattacharjee 1980) are monophyletic in our phylogenetic sialjoce (Fig. 1B). T" d und no Maca features e "- E d in the corolla tube. Moves, this feature does not distinguish tribe Stachydeae from most other lamioid groupings (see Issues in Lamioid Character Evolution—Stamen Length, below). However, there are a few morphological features that characterize the majority of Stachydeae. These include: calyx often Annals of the Missouri Botanical Garden campanulate or weakly 2-lipped with lobes often spiny and throat often hairy, and corolla often strongly 2- lipped. This morphologically and ecologically diverse assemblage, comprising at least 11 genera, clearly needs further investigation. GENUS PARAPHLOMIS The remainder of Lamioideae constitutes a mono- phyletic group (94% JAC; Fig. 1C) comprising some well-supported genera. However, many genera are intercalated within one another, perhaps confused taxonomically by homoplastic morphological traits (as mirrored, e.g., in Stachydeae by Stachys and Sideritis). The condition of having the nutlets apically truncate may constitute a synapomorphy of this group, but there are reversals to apically rounded nutlets within Paraphlomis and all of the following tribes. The genus Paraphlomis (Prain) Prain together with the Phlomis clade form a trichotomy with respect to all remaining taxa (Fig. 1C). Paraphlomis, as currently circum- scribed, includes about 20 species that occur mostly : 1 Zl LEE P a ue Bh al tek East Asia. Paraphlomis has previously been reduced to a section within Phlomis, including the three mis oblongifolia (Blume) Prain, and P. javanica (Blume) Prain (Prain, 1901). Although our analyses do place two accessions of Paraphlomis in the vicinity of Phlomis, the phylogenetic position of Paraphlomis is still uncertain and no higher-level classification is suggested at this time. TRIBE PHLOMIDEAE Phlomis comprises more than 100 species distributed throughout western Eurasia. Infrageneric relationships of Phlomis were recently investigated using the trnI-F region and rps/6 intron (Mathiesen, 2006; Mathiesen et al., unpubl.). Despite considerable morphological and results supported a split of the genus into two separate groups, which can be recognized as separate genera. Our findings here, based on a more limited sampling of Phlomis species, corroborate a split of the genus into two species groups: Phlomis s. str. and Phlomoides Moench s.l. (clades C and D, respectively, Pi ides, the non-type group, includes g Eremostachys (five to 60 spp.), the small subtropical to tropical East Asian genus Notochaete (two spp), and the monotypic West Asian genus Pseuder- emostachys (clade D, Fig. 1C). The division of Phlomis Fig. 1C). the west Eurician species into two groups is supported by several traits, including habit, leaf characters, corolla morphology, cytological data (Azizian & Cutler, 1982; Azizian & — — Moore, 1982), and pericarp structure (Ryding, 2008), 3 ra 1 + B sk s aL + P 1 J QUEUE DL] > 1 ESA al., 1986; Kamelin & Makhmedov, 1990a, b; Ryding, 2008). Moreover, two centers of diversity can recognized: (1) south and east Anatolia and northwest- em Iran, where all but one species belong to the Phlomis group, and (2) Central Asian parts of the former USSR to eastern parts of China, where all species of the Phlomoides group occur (Azizian & Moore, 1982). A close relationship between Phlomis and Eremo- stachys has previously been suggested. Consequently, several species of Eremostachys were transferred to P. ides, including the only species of Eremostachys in the current phylogeny, while other species were transferred to. Paraeremostachys Adylov, Kamelin & Makhm. (Adylov et al., 1986; Kamelin & Makhmedov, 1990a, b). However, as mentioned by Hedge (1990), the name Paraeremostachys is illegitimate; the type of this name is also the type of Eremostachys. Both Phlomoides and Paraeremostachys are treated as synonyms by Harley et al. (2004). Until molecular data are available for more species of Eremostachys, no nomenclatural changes are p . However, we still recognize these genera as part of the Phlomis group and classify this clade as tribe Phlomideae Mathiesen (see Appendix 1). Although not included here, based on strong morphological similarities and phylogenetic analyses based on cpDNA data (Mathiesen et al. unpubl.), the monotypic genus Lamiophlomis Kudó should also be included in this tribe. TRIBE LEONUREAE The four temperate Eurasian genera Chaiturus, Lagochilus, Leonurus, and Panzerina group with high support (95% JAC; Fig. 1C) and are moderately supported as sister to a large polytomy consisting of all remaining taxa. Based on these results, we suggest that Chaiturus, Lagochilus, Leonurus, and Panzerina be classified as tribe Leonureae Dumort. (see Appendix 1). Furthermore, in a phylogenetic analysis of the trnL-F region alone (results not shown), the small genus Lagopsis (Bunge ex Benth.) Bunge groups within the Chaiturus-Leonurus-Panzerina clade and should also be included in Leonureae. Short stamens that are included in the corolla tube, palmate leaf venation, and Leonurus, Chaiturus, and Panzerina have been associated in traditional classifi- cations, their close relationship to Lagochilus and Lagopsis has not Previously been suggested. Lagopsis Volume 97, Number 2 2010 Scheen et al. Phylogenetics of Lamioideae was classified in a separate tribe from that of the other four genera by Takhtajan (1997), and Mabberley (1997) regarded Lagopsis as synonym to Marrubium. A monophyletic and strongly supported (100% JAC) Lagochilus is recovered as sister to a clade including the remaining four genera (Fig. 1C). Morphologically, Lagochilus (ca. 40 spp.) is the most distinct genus of the four, with spiny bracteoles longer than calyces, spines usually present in the leaf axils, and a densely villous, 2-lobed, | g J p — n lip (H 1 y et al, 2004). Three small genera, Lagopsis (four spp.), Panzerina (two to seven spp.) and the monotypic Chaiturus, are nested within a paraphyletic Leonurus (ca. 25 spp.). These four genera group in all trees and differ from Lagochilus in having shorter bracteoles, no spines in leaf axils, and a short posterior lip of the corolla (Harley et al., 2004). Chaiturus and Panzerina have been variously associated with Leonurus in traditional classifications (Dumortier, 1827; Reichenbach, 1830-1832; End- licher, 1836-1840; Bentham, 1876; Briquet, 1895- 1897; Wu & Li, 1982; Harley et al., 2004). Included or excluded, Chaiturus and Panzerina have always been recognized as divergent in several features from Leonurus s. str. and classified separately at some level. Chaiturus differs from Leonurus in the structure of the calyx, the arrangement of stamens, leaf shape, and chromosome number (Harley et al., 2004). Panzerina differs from Leonurus in the size, color, and shape of the corolla and the surface morphology nutlets (Harley et al., 2004). Chaiturus and Panzerina also differ from Leonurus ecologically and biogeogra- phically. Chaiturus marrubiastrum (L.) Spenn. is a ruderal species in the European-Mediterranean re- gon, whereas the Panzerina species are endemic to semi-deserts of Central Asia (Harley et al., 2004). Lagopsis, which is widely distributed throughout morphology, and by being densely white-lanate (Harley et al., 2004). on the paraphyly of Leonurus, as well as the e and karyotypic discontinuity within the If , we sita 5 1 L NS established based on plesiomorphic characters. More T should be added prior to a more thorough evaluation of generic status of groups within this clade. A LARGE POLYTOMY Sister to tribe Leonureae is a weakly supported og consisting of all remaining taxa (58% JAC; ig. 10). This clade is native to Old World temperate, b. cal, or tropieal areas, although a few species en been introduced elsewhere (e.g., the widespread arrubium vulgare L. and Leonotis nepetifolia (L.) R- Br.). This large group of taxa is separated into three groups and the monotypic genus Roylea Wall. ex Benth., which together form a polytomy (Fig. 1C). Roylea, and the likewise monotypic Eriophyton Benth., occur at high altitudes in the Himalayas. Tribes Lamieae Coss. & Germ., Marrubieae, and Leucadeae Scheen & Ryding all include species from temperate western Eurasia with extensions into subtropical to tropical zones. Given their uncertain phylogenetic placements in our analyses, we have not classified Roylea and Eriophyton at the tribal level. TRIBE LAMIEAE Our results strongly support a clade comprising the three genera Lamium (ca. 35 spp.), Lamiastrum (one to four spp.), and Wiedemannia (two spp.) (99% JAC; Fig. 1C), which we have chosen to classify as tribe Lamieae (see Appendix 1). Lamieae has a temperate Eurasian distribution with center of diversity in western Asia (the Irano-Turanian region; Mennema, 1989). Synapomorphies of the group include hairy anthers, an abruptly widening corolla tube, and often pubescent corollas with a long and hooded upper lip. A close ium—Lamiastrum relationship has been suggested in most traditional classifications and was therefore expected. The two annual Wiedemannia species have also been taxonomically associated with Lamium (Endlicher, 1836-1840; Bentham, 1876). While most authors agree on a close relationship between Lamium, Lamiastrum, and Wiedemannia, classifications have varied as to the autonomy of the latter two genera (see, e.g., Dumortier, 1827; Reich- enbach, 1830-1832; Endlicher, 1836-1840; Cosson & German, 1845; Bentham, 1876; Luerssen, 1879— Harley et al., 2004). The separation of Lamiastrum has been based on differences in the shape and color of the corolla, whereas Wiedemannia is characterized by a 2-lipped calyx (Harley et al., 2004). In the most recent treatment of Lamiaceae (Harley et al., 2004), both Lamiastrum and Wiedemannia are treated as synonyms of Lamium, although it is also stated that the very distinct Lamiastrum may be better treated as a separate genus, and that most authors treat Wiedemannia as a genus. The monotypic Himalayan Eriophyton, which agrees with most Lamium in having hairy anthers, is sister to tribe Lamieae in all analyses. However, this relationship is poorly supported (56% JAC; Fig. 1C). Other Asian lamioid genera that could not be examined here, but nevertheless might be relevant to Lamieae phylogeny include Ajugoides Makino, Matsumurella Makino, Loxocalyx Hemsl., and Alajja Ikonn. A comprehensive 210 Annals of the Missouri Botanical Garden phylogenetic study of the group will be published elsewhere (Bendiksby et al., unpubl.). TRIBE MARRUBIEAE Species of Ballota, Marrubium, and Moluccella form a well-supported monophyletic group (84% JAC; Fig. 1C). Ballota integrifolia Benth., which is endem- ic to Cyprus, is sister to all other taxa. Together with the European species B. frutescens (L.) Woods, B. integrifolia has been circumscribed as belonging to section Acanthoprasium Benth. (Patzak, 1959). The key characters for section Acanthoprasium are woody habit and the presence of long and spinose bracteoles (Patzak, 1959; Harley et al., 2004). All other species of Ballota are herbs or subshrubs with herbaceous bracteoles. It may be that B. integrifolia deserves to be recognized as a separate genus based on its eed and morphological distinctness from the other Ballot ies: | Ë £. ESOS s he included in th > z taxonomic changes are suggested at this time. The three species of Moluccella form a highly supported group (99% JAC; Fig. 1C). Moluccella is found in rocky and disturbed regions from southern Europe to central Asia. Moluccella aucheri (Boiss.) Scheen was recently transferred from Otostegia to Aa E JO 1 1 E 1 E.2 c characters (Scheen & Albert, 2007, 2009). The monotypie genus Sulaimania Hedge & Rech. f. was separated from Moluccella based on its perennial and subshrubby habit, unexpanded fruiting calyx limb, and different overall a in the current phylogeny. The unexpanded calyx limb ¡ anomalous in Moluccella; however, iman ned to superficially resemble M. aucheri (Hedge & Lamond, T" tet LG 1982). In the original rcumscri e species (as M. ioi Prain), Prain (1890) describes it : EE d M. aucheri with a calyx like that of M. spinosa L., only smaller. Further ies are needed to verify monophyletic group (99% JAC) that is sister to a well-supported group (100% JAC "a ra and Ballota (Fig. 1C). ) consisting oí ost species of form a well-su : ; ed clade with Marrubium (100% JAC; a a close a i JAG Fig. 10), thus confirm the vegetative parts used to distinguish members of the two genera is the position of the stamens, i.e., whethe included in the corolla tube as in Marrubium or shortly ed 30 species rth Africa, with one species (B. africana (L.) Benth.) being endemic to South Africa and Namibia. The current molecular phylogeny 1 1 BI] at nib. clearly le genus y However, the five species of Ballota that form a well- supported subclade (99% JAC; Fig. 1C) are all members of the large section Beringeria (Neck.) Benth. sensu Briquet (1895-1897). The genus Marrubium includes approximately 40 species that are distributed from Europe through Pakistan to the Himalayas and in North Africa, mainly in rather dry places. Based on the current molecular phylogeny, it is not possible to say whether or not Marrubium is monophyletic as currently circumscribed. Three of the included species form a strongly supported group (100% JAC; Fig. 1C), whereas the fourth species is unresolved with respect to Ba Although the status of Marrubium and Ballota remains encom and Moluccella (see Appendix 1). TRIBE LEUCADEAE As part of the large polytomy, species of the six genera Acrotome, Isoleucas, Leonotis, Leucas, Otoste- gia, and Rydingia form a well-supported group recognized here as tribe Leucadeae (100% JAC; Fig. 1C; see Appendix 1). Based on a phylogenetic analysis of many more representatives of Leucadeae, several taxonomic changes have recently been suggested (Scheen & Albert, 2007, 2009). The genus Otostegia was recently recircumscribed and the number of species was reduced from 17 to 11, all with an African to Arabian distribution occurring dry, often montane areas and semideserts (Scheen & Albert, 2007, 2009). Species of Otostegia lack spines at ihe losf ouk: amal b herhaceous bracteoles and white flowers (Sebald, 1973; Rechinger, 1982; Ryding, 1998 Scheen & rt, , 2009). 418 Of the excluded six Species, one species was t somala (Patzak) Scheen) based on molecular data " izell f, 13 5 I : luding minute bracteoles, small, bnt round leaves, a 5-lobed calyx, and most parts of the plants being densely white tomentose (Sebald, 1973; Scheen & Albert, 2007) nother species was transferred to Moluccella (M. aucheri; see tribe Marrubieae, above). Finally, four species were transferred to the new genus Rydingia (Scheen & Albert, 2007, 2009). Rydingia differs from Volume 97, Number 2 Scheen et al. 211 2010 Phylogenetics of Lamioideae the remaining species of Otostegia in having spinesat is possible to suggest some patterns of character the leaf axils, spinose and persistent bracteoles, yellow flowers, and few-flowered verticillasters (Sebald, 1973; ee. SEN dup: Tn we d recircum- of Rydiagia; all three gorra are sll kano monophyletic groups (Fig. 1C). However, althou Rydingia is highly supported (100% JAC) as sister to all other species of the Leucas s.l. “se —— and Isoleucas are nested within Leucas (Fig. The genus Leucas is one of the As genera of subfamily Lamioideae with about 100 species occur- ring on dry or disturbed ground in tropical to southern (Harley et al., 2004). M either Africa (including the Arabian Peninsula) or Asia (excluding the Arabian Peninsula), although a few species are more widely distributed (e.g., L. aspera (Willd.) Link and L. martinicensis (Jacq.) R. Br.; Singh, 2001) Asian and African species of Leucas form separate groups with the primarily Asian species being supported as a monophyletic group (88% JAC), whereas the African species are not (Fig. 1C; Scheen & Albert, 2009). The African species of Leucas are paraphyletic with respect to the African genera Acrotome an hematin, » as well as tbe Africa species of Otostegia. Th of a previous A based phylogeny, but — Acrotome and Leonotis form monophyleti based on the morphological data Faken, 1998), they do not form monophyletic groups based on molecular data (Fig. 1C; Scheen & Albert, 2009). The nine species of Leonotis occur on hilly slopes and rocky or disturbed ground in tropical and southern Africa and are easily recognized by the bright orange or red corollas of their flowers and the short lower corolla lip that withers at anthesis (Ryding, 1998; Iwarsson & Harvey, 2003). The six species of Acrotome occur in dry places in south re and southern Africa (Harley et al., 2004). Acrotome is separated from Leucas and Leonotis based on short stamens that are included in the corolla tube, a hairy style, and the lack of a bearded margin of the Posterior corolla lip (Ryding, 1998; Harley et al., 2004). The non-monophyly of Leonotis seems partic- ularly strange given the suite of characters (related to bird pollination) shared by all members of the genus. Preli liminarily, we suggest that cpDNA capture via hybridization could account for the relationships seen between particular species of Leonotis and ISSUES IN LAMIOID CHARACTER EVOLUTION With the extensive sampling across subfamily and the resulting molecular phylogeny, it evolution within the subfamily. A few monotypic or on RISEN Rot a Tan and > epresented by UNG Vi tiie peal: Theiekors ilo ssa results do not paint a complete picture. Despite these limitations, it is clear that several en w— that were — = iis for specific groups (e.g., Bentham; aman are not synapomorphies — to these ee "a have | l times. M have thymoid dine. bu tribe Srendene: has of inflorescence occur, e.g, in tribe :Gtachydess; Ballota, and Marrubium (Harley et al., 2004). Lamioid labiates vary in habit from annual herbs to subshrubs, shrubs, and rarely even small trees (Harley et al., 2004). Woodiness has evolved repeatedly from herbaceous ancestors in several asterid groups, e.g., in Apiaceae subfam. Apioideae (Calvifio et al., 2006) and in the family Gentianaceae (Struwe & Albert, 2002). In subfamily Lamioideae, the reverse has also occurred: manthosphace stemoneae), has clearly evolved from woody ancestors. Many lamioid genera (e.g. Leucas, Phlomis, Pogostemon) include both herbs and shrubs or subshrubs, suggesting that overall habit in Lamioideae is a highly homoplastic trait. In a few genera, the calyx is expanded into a dilated limb, e.g., Moluccella and Otostegia, and in a few genera the calyx is strongly accrescent in fruit, e.g, Colebrookea, P Dunn, and P (Harley et al., 2004). Indeed, several striking patterns of parallelism emerge from the curent phylogeny, as discussed egere and ndm. Fleshy fruits. A well-known case of parallelism within lamioid labiates is the development of a fleshy fruit. Because most labiates have dry fruits, it was once thought that fleshy fruits had evolved only once, ee genera with fleshy fruits were circumscribed as tribe Prasieae (Bentham, 1848) i Prasioideae (Briquet, 1895-1897). However, recent studies of fruit pericarp structure and molecular relationships of lamioid labiates have shown that fleshy fruit is a homoplastic trait (Ryding, 1994c; Deb a Ae A Behr eit has x hiates- mod e Hawaiian labiates (Stenogyne and Phyllo- i and in two genera of the emmateae (Gomphostemma and Bostry- ). Not only have there been three indepen- in origins of fleshy —-— but the current molecular phylogeny also suggests there has been at least one 212 Annals of the Missouri Botanical Garden reversal from a fleshy fruit in the common ancestor of Bostrychanth € nopsis G h t dry fruit in the genus Chelonopsis. In monocots, fleshy fruits have evolved and been lost repeatedly, and a strong tendency for fleshy fruits to evolve in the shade and be lost in open habitats has been demonstrated (Givnish et al., 2005). In Lamioideae, a shady habit not seem to be linked to presence of a fleshy fruit. Fleshy-fruited Prasium, for example, occurs in dry, open places (Harley et al., 2004). Many other examples of parallel evolution of fleshy fruits from dry-fruited t i (Potter et al., 2007), Rubiaceae (Bremer & Eriksson, 1992; Rova et al., 2002), and Solanaceae (Knapp, 2002). t. e.z..inR , €.B. Stamen length. Having short stamens that are included in the corolla tube, rather than exserted, is a character that has been used historically to distinguish several genera: Marrubium from Ballota, Acrotome from Leucas and Leonotis, and Sideritis from Stachys. The shared presence of short stamens led Bentham and Briquet to place Marrubium, Acrotome, and Thuspeinanta in tribe Marrubieae (Bentham, 1876; Briquet, 1895-1897), although this view has not been supported by later authors (e.g., Sebald, 1980; Ryding, 1998). Most genera of Lamioideae are described as having stamens that are not or only shortly exserted from the corolla (Harley et al., 2004). However, a few genera have stamens that are long and clearly exserted from the corolla. This trait may be considered a synapo- morphy for the clade consisting of Comanthosphace, Leucosceptrum, and Rostrinucula, but it is also found in Pogostemon (Harley et al., 2004; see Pogostemo- neae, above) Thus, long-exserted stamens have evolved at least twice within the lamioid labiates but are restricted to tribe Pogostemoneae (Fig. 1A). The differences in stamen position and length are most likely related to differences in pollination syndrome. Indumentum. Many labiates have densely hairy corollas, most often on the outside as in Lamium, Moluccella, Leucas, and Phlomis, but also sometimes on the inside of the corolla as in Lagochilus (Harley et al., 2004). Although it is easy to distinguish between a glabrous and a densely hairy floral part, it is more difficult to quantify the degree of indumentum between the two extremes. Even so, type and amount of indumentum often vary enough to be used in keys. The presence versus absence of branched hairs was used in the key to subfamily Lamioideae (Harley et al., 2004) and also to distinguish the monotypic genus Isoleucas (Schwartz, 1939). However, with the recent transfer of Otostegia somala (Patzak) Sebald to Isoleucas, presence of branched hairs is no longer a diagnostic character for the genus (Scheen & Albert, 2007, 2009). Although presence of branched hairs is sometimes shared among closely related taxa, e.g., Comanthosphace, Leucosceptrum, and Rostrinucula, it is a character that has evolved several times within subfamily Lamioideae, e.g., in Ballota, Gompho- stemma, Isoleucas, and Pogostemon. Several genera of subfamily Lamioideae are charac- terized by having a bearded margin of the posterior corolla lip, but this feature is only found in Phlomideae and Leucadeae. In the genus Phlomis, the presence L. f a: E-J n z 11mnoarte the segregation of the Phlomoides s.l. (including Notochaete and at least some of Eremostachys) from Phlomis s. str. (Mathiesen, 2006; see tribe Phlomideae, above). In tribe Leucadeae, the bearded corolla margin is present in all genera except the derived genus Acrotome. Thus, it appears there has been a reversal of the trait in the lineage leading to Acrotome (Scheen & Albert, 2009). The lack of the characteristic bearded corolla margin was one of the morphological characters supporting the transfer of Otostegia aucheri Boiss. to Moluccella and thereby the segregation from Otostegia (Scheen & Albert, 2007). Whether or not different indumentum H char- 1V I characters. However, presence of a bearded margin of the posterior corolla lip may be an example of a phylogenetically informative character that may be taken as a synapomorphy for two different groups. It seems to have evolved twice with at least one reversal of the trait (Fig. 1C). Spinose bracteoles. Most genera of subfamily Lamioi- deae have herbaceous bracteoles, but a few genera are characterized by having spinose or spinescent bracte- oles, e.g., Galeopsis, Lagochilus, Leonotis, and Moluccella (Harley et al, 2004; Fig. IB, C) Based on the relationships uncovered in the current phylogeny, this is another trait that has evolved several times indepen- dently. Furthermore, this character can be continuous, Nevertheless, the presence of spinose bracteoles does seem to hold a phylogenetic signal at the generic level. In several cases, species with spinose bracteoles do not group with their congeners with herbaceous bracteoles. The presence of spinose bracteoles is one of the morphological characters that support the transfer of Otostegia aucheri to Moluccella and the segregation of the newly described genus Rydingia from Otostegia (Scheen & Albert, 2007, 2009; see Fig. 1C and tribe Leucadeae, above). Also, in Ballota, presence versus absence of spinose bracteoles coincides with the molecular relationships uncovered in the current EXA RSS PARAS ARA AL ee Se urus i G TED ES o eee = on * OLEATE we IRA ATAN A A e Volume 97, Number 2 2010 Scheen et al. 213 Phylogenetics of Lamioideae phylogeny and may warrant the segregation of B. integrifolia and B. frutescens from the remaining species of Ballota (see Fig. 1C and tribe Marrubieae, above). In all of these cases, presence of spinose bracteoles is corroborated by other n characters that support the generic segregations Calyx fibers. Ryding (2007) studied the amount of fibers in calyces of Lamiaceae and found particularly high quantities in the subfamilies Lamioideae and lila. Although the character is very homoplastic, it is interesting to note that the variation in amount of calyx fibers appears to be rather strongly correlated to the topology of the current cladistic hypothesis (Fig. 1). The amount of fibers is generally ery L Leucadeae (Fig. 1C); monte intermediate in the clade of Betonica, leops an tachydeae (Fig. 1B); and generally very i in the tribes that split off in the basal part of the phylogeny (Fig. 1A). der (2007) suggested that the shared presence of suggests that high amounts of c evolved independently in these two subfamilies. THE NEW CLASSIFICATION VERSUS HISTORICAL CLASSIFICATIONS are proposing a new suprageneric classification of aneit Lamioideae with nine tri ( Appendix 1). Three tribes are new and the remaining six tribes are recircumscribed to correspond to monophyletic groups in the current molecular phy- logeny (Fig. 1). Several classifications of subfamily Lamioideae have been published in the past (e.g., Bentham, 1876; Briquet, 1895-1897). In the latest revision of the entire family (Harley et al., 2004), no suprageneric groups were recognized within subfamily Lamioideae. Neither of the historical classifications corresponds well to the current phylogeny, nor do they correspond well to the currently ized subfam- ilies (sensu Harley et al., 2004). However, even if none of the groups in Bentham's (1876) and Briquet's (1895-1897) classifications represent monophyletic groups based on the current molecular phylogeny, a few remarks on how the new classification deviates from the historical ones are warranted. There were no subfamilies in Bentham’s classifica- tion; thus, most of the recognized as subfamily Lamioideae were placed in tribe Lamieae (as Stachydeae; Bentham, 1876; name ee Casna | 1... Jn Prasieae, which included the fleshy-fruited genera (Bentham, 1876). Also, the two lamioid genera Pogo- stemon and Colebrookea and the nepetoid genus Teenie Nook: ios ui ie rupa ka ninae (Pogostemoneae; name corrected according to Sanders & Cantino, 1984) under tribe Mentheae (as Satureineae; Bentham, 1876; name corrected according to Sanders & Cantino, 1984). Briquet’s (1895-1897) classification was heavily influenced by Bentham's (1876) classification. The main difference between these two rne was FN s dame: of a "p subfamily I soos to Sanders & Cantino 1984), which s“ RI s Harley et al., a Funbenane, L of tribe, ie. as E and transferred to died» Lamioideae (sensu Briquet, 1895-1897) and Prasieae was raised to the rank of subfamily, i.e., as Prasioideae. In both historical classifications, tribe Lamieae (sensu Bentham, 1876) and subfamily Lamioideae (sensu Briquet 1895-1897) were further divided into the three subtribes Melittidinae, Marrubiinae Endl., and Lamiinae Endl., ve latter re the vast majority of g subfamily Lamioideae (Bentham, 1876; Briquet; 1895- 1897). Thus, the most striking difference between the new classification proposed here (see Appendix 1) and these two historical inci (onthan, dies i E Briquet, un 1897)1 g y included in subtri lit ] groups that are renal at the tribal evel Literature Cited Abe Ah M. S. & P. D. Cantino. 1987. 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Struw CAVA Abat A aie Conii ianaceae: Systematics and N atural History- Cambridge University Press, Cam- Giel CA eee —_— Taberet, P., L. ly, ing a VT P. Mele. Bel 17. 1105-1 p . P. 466 in A. Takhtajan, Plants. Columbia A 216 Annals of the Missouri Botanical Garden — hi & R. G. Olmstead. 1997. Phylogeny of Verbenaceae inferred from rbcL nces. P. A. Reeves & R. G. rred from Wallander, E. & A. Albert. 2000. Phylogeny and classifi based on rpsl6 and trnl-F sequence data. Amer. J. Bot. 87: 1827-1 Wu, C. Y. & H. Li. 1982. On the evolution and distribution of the E . Yunnan. 4: € Wunderlich, R. 1967. Ein Vorschlag irlichen Gliederung der Labiaten auf Grund - Polonia. a. aka und des reifen Samens. Oesterr. 114: 383-483. APPENDIX 1. À new tribal classification of subfami amily Lamioideae includes nine iicet three vs zA are new and five of which are recircumscri mscription of -— Synandreae follows a vomit. published study M - 29. Asterisks (*) ere genera that are La lassified to other cladistic re results or based on morphological similaritica. All tribes n groups based on molecular data. To id ptum redundancy, monogeneric tribes have not been cepted; ibus, only duin that include more than one genus have n recogni as tri M a few genera that were included in the and correspond to EMI clades A still s inis - incertae sedis. NE tures characters shared i all many of the clin are r for an ibo: However, ide morphological characters not necessarily represent synapomorphies for the Lo but rather Mis that are useful for identification. I. Lamioideae Harley, ep ps T 765. 2003. TYPE: Lamium L., Sp. Pl. 2: 53. Non-molecular features: style nutlets mucilaginous; pollen tricolpate and 2-celled when shed: seeds albuminous; em © spatulate. — taxa: *Ajugoides Makino, cs Ikonn., Beto- oe n Wall., Eriophyton Loxocal nobasic; Stachyops & Rech. f., as Tat mateae, Synandreae, Stachy- . Lamieae, Marrubieae, and Leuc. Note: Ajugvides, A lajja, Hypogomphia, Loxocal: Matsumur- ella, Messochydiun, Paralamium, i Sta- chyopsis, chyopsis, p and Sulaimania are included met Lamioideae Sad, iu UM T e e & Prantl, Nat. Pflan- zenfam. IV, 3a: 208. Dec. TYPE: P. Pogostemon Desf., Mém. Mus. Hist. x 2: 154. 1815. Non-molecular features: none readi t: bracts often y ery broad; salla clin secs 2-lipped, posterior lip a iria stamens often long-exse rted, filaments often bearded; nutlets often small; pericarp often lacking a sclerenchyma re. Included taxa: Achyrospermum Blume, sd R. Br., *Coleb Sm., Comanthosphace S. Moore, Craniotome Rchb., tinola Prain. i gr Pogostemon Desf., Rostri e: Colebrookea is included in tribe Pogostemon e on morphological similarities: weakly 2-lipped ini short posterior lip; small nutlets Eurysolen is — with the other members of t vibe Pogostemoneae molecular phylogeny based on the trnL-F region cal not shown). 2. Gomphostemmateae Scheen & Lindqvist, trib. nov. TYPE: Gomphostemma Wall. ex Benth., Edwards's Bot. Reg. 15: t. 1292. 1830. — on saepe ex cyma laxa longipedunculata nstans. Corolla plerumque grandis, tubo ad basim angusto alas valde dilatato, labio posteriore en vix cucullato. Nuculae carnosae vel siccae ac valde fi Non-molecular features: — often lax, long- pedunculate cymes; corolla y large, with be narrow at base but bin cdm in the distal part; posterior lip we scarcely hooded; nutlets fleshy or dry and " fibro ncluded inde: Bostrychanthera Benth., Chelonopsis Miq., rica Wall. ex Benth. 3. Symandreae Raf., in Fl. Tellur. 3: 84, Nov.-Dec as “Synandrines.” TYPE: Synandra Nutt., Amer. Pl. [Nuttall] 2: 29. 1818. E E Non-molecular features: inflorescence racemoid; Homes gpeeoil, Included taxa: Brazoria Engelm. & A. Gray, *Macbridea Elliot ex Nutt., pes Benth., Synandra Nutt., Warnocki, W. Turne Note: The inclusion of Macbridea is based on molecular phylogeny (Scheen et + 2008) an morphological characteristics: inflorescenc d flow- ers sessile; corolla broad; stamens villous. ws revious 4. Stachydeae Dumort., Fl. Be Belg. Ds 44. 1827. TYPE: Stachys L., Sp. Pl. 2: 580. 1 Non-molecular features: none readily apparent that could identify all or most n E^ diverse clade. ce the following characteri paratively frequen calyx often campanu E. or usar apa -lipped, calyx | t spiny, calyx throat often hairy; corolla often strongly 2- lipped. Included taxa: hrenk ex Fisch. & C. A. Mey., e (A. Gray) Hiller, Melinis L., Phlomi- doschema Vved., Phyllostegia , Sideritis L., Stachys L. » Stenogyne ps nom. cons., non Stenogyne Cass. [Asteraceae]), Suzukia Kudó, Pipiena T. 5. Phlomideae Mathiesen, trib. nov. TYPE: Phlomis L., Sp. PL 2: 584. 1753. Trichomata ramosa plantae partes varias plerumque edd Flos caly rai lobis saepe in apicem — 2 abrupte con saepe barbata ac dense pubescente. Non-molecular features: calyx lobes often abruptly mamawa ted nite cee ae expanded at margins; la extus SE LE NN EEN Volume 97, Number 2 2010 Scheen et al. 217 Phylogenetics ol L amioid A En e P often bearded Po det pubescent outside; ranched hairs usually pres grece taxa: s Bunge, *Lamiophlomis Kudó, Notochaete Benth. onc L., Phlomoides Moench, a mostachys Popo d Note: La. pihak is included based on morphologi- lobes abruptly narrowed to a spinescent apex, and corolla bearded and densely pube- scent. Also, Lam iophlomis pe bee Phlomoides i in = 6. Leonureae Dumort., Fl. == Dt 46. 1827. TYPE: Leonurus L., Sp. . 1753 Non-molecular features: + palmate leaf venation; leaves often palmately lobed; stamens s short. Included taxa: Chaiturus Willd., Lagochilus Bunge Benth., Leonurus L., Pain Soják, *Lagopsis op c ex Benth.) Bunge. Note: Lagopsis is included in tribe Leonureae bed $ on anions Also. f tribe Leonureae in a molecular ues qe on MT region (results not shown). 7. Lamieae Coss. & Germ., Fl. Descr. Anal. - 311, ama 1845, as Lamicidene” TYPE: Lamium L., Sp. Pl. 2 579. 1753. Non-molecular features: corolla often densely pub- escent outside, posterior lip long, hooded, and often arched, tube — abruptly widening; lateral lobes of the lower lip mostly a tooth or acute at the apex; anthers t hai Included taxa: Lamium L. irm Lamiastrum Heist. ex Fabr. and Wiedemannia Fisch. & C. A. Mey.) 8. Marrubieae Vis. “Marrubiaceae.” 582. 1753 Non-molecular features: calyx , Fl. Dalmat. 2: 214. 1847, as TYPE: Marrubium L., Sp. Pl. 2: en with rad lobes, Included taxa: Ballota L. 9. Lanendese Scheen & Riding, tb. now. TYPE: Lenses U: Br., Prod. Fl. Nov. Holland. 504. Flos calyce plerumque manifeste zygomorpho, lobis lobula . 1t sr* i harhato — features: m sal disney zygomor- cas margin, with few exceptions (Acrotome Benth. ex — Included taxa: Acrotome Bei a Endl., dd Schwartz, Leonotis rs "s BR. Br, Benth., Rydingia Scheen & erum die. & ipeum 2007). GENERA INCERTAE SEDIS WITHIN LAMIOIDEAE uer : ; Galeopsis, and Paraphlomis ic clades in the ar ascribing them groups. However, > follo in lassified ol od Alaja, Hypogom- phia, Loxocalyx . Matsumurella, Metastach Metastachydium, Paralamium, Poeudomarrubiuzn, Stachyopsis, and Note: An early draft of this paper was as included in A.-C. Scheen's Ph.D. thesis (Scheen, S which w was pinte " a this early de draft, we also atada a | tribe Betoniceae "se Betonica. It was never our REVISION OF THE ASIAN GENUS P. C. van Welzen? KOILODEPAS (EUPHORBIACEAE)! ABSTRACT assk. (Euphorbiaceae) is a genus of nine accepted species ranging from India (K. calycinum Bedd.) to Koilodepas Hi Southwest China, Indochina, Southeast Asia, West Malesia, and New Guinea (K. homaliifolium Airy Shaw). Two spec widespread on the leader Asian mainland and in weste from China to Thailand (K. hainanense (Merr.) Croizat), kia = ag are endemic to Borneo, and a new species is K. glandulige erum Pax & K. Hoffm. is lectotypified. Typical for the species ie Los presence of Welzen & Muzzaz. m Then ipis tcc groups of small st node; and staminate flowers with a broad, short miese flaments - | dress athen < laevigatum excepted). The species are difficult. to distingu ies are bantamense Hassk. and K. longifolium d L IE others (K. brevipes Merr., K. laev ound on Sumatra only (K. Mic esia t, globose e with the typically ss ish morphologi androphor or V te € of the al leaves (green or brown), the typ AM free ES vs. s. entire), the base of the leaf bl blade micis vs. pe Jl sulcate ones), and especially in the mi il united, loose vs. tight around ovary, enlarging in fruit vs. not enlarging i in fruit, and degree in which stigmas aah apically). words: Coelodepas » Euphorbiaceae, Koilodepas, Southeast Asia, taxonomy. Hasskarl (1855) described the genus Koilodepas -, referring to the stamens as the source for the name, although he did not further clarify the name. Backer (1936: 132) explained the name (as “Coelo- depas”) as a combination of the Greek words “koilon” (cavity, here meaning chamber) and “depas” (cup): the stamens form a cup, whereby each filament forms a separate chamber hiding the anthers in bud. The structure of the androecium is indeed characteristic, the four to eight stamens are placed in a circle on a short and broad androphore, the loose filaments are sulcate and narrow apically y. separating the two anther thecae basally (thecae divergent). The only exception is K. laevigatum Airy Shaw with threadlike filaments and parallel thecae. Two years later, Hasskarl (1857) started the confusion around the generic name, when he suddenly referred to Coelodepas Hassk., an orthographic variant on Koilodepas. The name op. depas is the older and, therefore, correct original spelling for the generic name, even though a NH of later authors used Coelode Index () under both generic names. Croizat (1942) even indicated that because of the (incorrect) general use of C > the name should be listed in the nomina generica bobine. Airy Shaw described most species in Koilodepas, although several other species were first published in other, originally monotypic genera. Blume introduced the genus Calpi lume, and later Gagnepain (1925) described Nephrostylus Gagnep.; th are taxonomic synonyms of Koilodepas Koilodepas is a small Asian genus (nine species accepted herein) ranging from India to southern China, then south to the western half of the Malay Archipelago and New Guinea. Webster (1994) and Radcliffe-Smith (2001) classified Koilodepas in the subfamily Acalyphoideae (Euphorbiaceae s. str.), the tribe Epiprineae (based on the sepals valvate, petals absent, stamens usually inflexed in bud, disc absent, styles multifid, fruits dehiscent, and seeds with the cotyledons larger than the radicle), and the subtribe Epiprinae (bisexual inflorescences). on two molecular markers, r and trnL-F, Koilodepas groups together with Cephalomappa Baill. as sister group, and both are sister to Cephalocroton Hochst. (Wurdack et al., 2005: clade A4); both nodes have high bootstrap support. Webster (1994) and Radcliffe- Smith (2001) place Cephalomappa in a different subtribe DREE EN still within the Epipri- neae, but the molec ta suggest unification of the ibes. However, weas Epiprinae genera are still Licking exemplars in the backbone phylogeny of the I thank the directors of A, BK, BKF, BM, BO, K, L, and P for loans of the; Muzzazinah is thanked for providing the basis for diagnosis, Hanneke Jelles for her beautiful * Netherlands Centre RA Leiden, The Netherlands. welzenGnhn.lei, denuniv.nl doi: 10.3417/2007149 insti tutes. this S with her M.Sc. cul P Frits tt is thanked for his Latin Ben Kieft for scanni ing the for for Naturalis, mue Herbarium Nederland, Leiden Lsvenieh, P.O. Box 9514, 2300 Ann. Missouri Bor. Garp. 97: 218-234. PUBLISHED oN 9 JuLy 2010. Volume 97, Number 2 2010 van Welzen 219 Revision of Koilodepas Euphorbiaceae s. str. (Wurdack et al., 2005: fig. 4), and thus it is premature to synonymize both ma Airy Shaw (1960) divided Koilodepas into two sections, section Hyalodepas Airy Shaw with ale flowers with broad calyx wie pu strongly enlarge in t oilodepas with hardly enlarging oligos. or these iios narrow. Section Hyalodepas comprised three species, K. calycinum Bedd., K. hainanense (Merr.) Croizat, and K. pectina- tum Airy Shaw (Airy Shaw, 1969), which was added later. The latter species blurs the distinction between the sections, because a continuous range in sizes now exists between the species with broadly enlarging K : section Koilodepas. Another reason why 1 prefer to unite both sections is that two character states of the same character are used to define the two sections (broadly enlarging sepals vs. non-enlarging or nar- rowly enlarging). One of the two states is plesio- morphic (the non-enlarging sepals, also present in related genera) and cannot be used to characterize a group, because this character state can never indicate the monophyly of the section. One species complex within Koilodepas was espe- cially difficult to resolve. Airy Shaw had previously struggled with these species as exemplified in his different treatments of 1960 and 1963. In later regional revisions, Airy Shaw stopped referring to this species complex, which involved the following nine names: : ntamense Hassk., K. hainanense, K. ferrugineum Hook. f., K. frutes (Blume) Airy Shaw, K. glanduligerum Pax & K. Hoffm., K. longifolium Hook. f., K. subcordatum Gage, K wallichianum Benth., and Nephrostylus poilanei Gagnep. Within this complex, the leaves are mainly elliptic-oblong, but leaf size varies from small to large, base shape and indumentum color vary, and the blade margins are entire to serrulate. The stipules are also diverse, ranging from entire to ones swith dong marginal beth e pectinate). E s " "n e E can x : high, diosas the y so ti tightly as as bo. appear absent, or the calyx can abe low, extending to - half the length of the ovary. The calyx enlarges in bur. » xo. > 1 - : ibo or less the same size. The three shapes of the pistillate calyx provide the solution of the complex and distinguish the species. The loosely draped, high win Viat enlarges i in fruit is typical for K. hoinanense ( with hc fK hainanense are mainly diiré or with a few teeth ial The tightly fitting urceolate, non-enlarging calyx is typical for K. bantamense (with K. ferrugineum, K. , and K. wallichianum now recognized as synonyms); the stipules are mainly entire and small. Finally, K. longifolium has a short, determinate calyx dat docs, mek coluqn shd süpake dei ka dan and K. longifolium are further separated by two other characters: K. bantamense usually has broad glandular apices of the teeth along the blade margin, while those of K. longifolium are generally smaller; and the two species have different witch brooms in the inflores- K. bantamense di cences (see iscussion). CHARACTERS IMPORTANT FOR IDENTIFICATION STIPULES The most important distinguishing character related to the stipules is the i ich varies between entire to pectinate. More or less entire margins are found in Koilodepas bantamense and K. homaliifolium Airy Shaw (Fig. 1A, C), while strongly pectinate margins are present in K. pectinatum (Fig. 1E). The teeth in K. pectinatum are perpendicular to the stipule and some even carry smaller perpendicular teeth themselves. Other species show more or less interme- diate forms, with usually a few teeth, but these usually point upward (Fig. 1C). The distinction is hampered by the old dea “nee are -— persistent and start to similar in n appearance to the PEN However, the leath of f the old stipules (Fig. 1B). COLOR OF DRIED LEAVES Generally, each species dries either brown or green. A few species, like Koilodepas hainanense and K ifolium, are variable between brogwh green and io xia Ui uic 4 brownish, but even in those P specimens dry bru BASE OF LEAF BLADE Most species have a flat leaf blade, although the margins may be somewhat revolute. Typical for Koilodepas brevipes is that the blade base is strongly convex at both sides of the midrib (Fig. IF, 6). especially the basal margin, which is — revolute. This character is easy to 0 broad. leaves, but more difficult to see in tees with a narrow, cuneate GLANDS OF LEAF MARGIN The leaf blades usually have serrulate leaf margins, with the teeth ending in glands. These glands can be a Annals of the Missouri Botanical Garden Figure l. A-E. Stipules a SE - —A. Koilodepas bantamense Hassk.: young stipule. —B. Koilodepas bantamense: old stipule with frayed Koilodepas homaliifolium a ee Shaw. —D. Koilodepas beai Hook. f. —E. Koilodepas pectinatum Airy Shaw. F, ra Leaf base of K. brevipes Merr. with a convexity on both sides of the midrib. —F. View from adaxial surface. —G. View ial surface; four extrafloral nectaries visible. H, I. Leaf margins, ial surface. —H. Koilode, i ‘pas ifolium: teeth with an apical glandular zone. A Pickles S 3527 (D): C Sumbing SAN 91753 (L); F drawn SF 40668 (L); I drawn from K. J. PM RET broad zone along the rounded apex of the teeth (Fig. 1D. or they can be small as in Koilodepas longifolium (Fig. 1H). STAMENS The number of stamens is variable. Koilodepas brevipes and K. cordisepalum Welzen & Muzzaz. have a higher numbers of stamens (five to eight), while the longifolium: teeth with short Pe n. (barcode drawn from K. J. k r Sinclair SF 40668 (L); E wn from 0326 (L); G drawn fi pinus rom Kostermans 13949 (L); a drawn from J. Sinclair other species have four to six stamens. Stamen type is more useful as a distinguishing character. Typical for the genus are sulcate filaments that are arranged in a circle on the androphore. Te filaments uper to the apex, where the broad ae to verge and open inwardly via then almost horizontal slits (Fig. 2A). Koilodepas laevigatum is the only exception, with threadlike filaments and a narrow connective with parallel thecae (Fig. 2B). | | | Volume 97, Number 2 van W. 221 2010 Revi — : Figure 2. A, B. Stamen i olium Hook. f.: general type with broad free types of Koilodepas Hassk. —A. Koilodepas longif. q Pau dickies thecae. —B. Koilodepas laevigatum Airy Shaw: free part of filament ament threadlike, thecae parallel. nt sti i — C. Koilodepas laevigatum: sepals basally connate only. —D. comoletel hainanense (Merr.) Croizat: c lobes loosely veri ely, one sepal drawn tely, others zu to oe ovary. m Koil bantamense .: calyx tightly — ed covering latter : - Koil enlarged calyx in fruit — e caducous). G H. Style and stigma e a tigmas hardly won ae qapya : style present; stigma ap apices less often split; a i p wn from Nap A 409 (Ly B dra from Krispinus SAN 120047 (L); C drawn from O D drawn from Nguyen Nehia Tin 016812 17 (D, a kane n. (barcode L 0016252 [Ll F drawn from Lassan n SAN 63541 (L); G drawn from Singh, Talip & ordin SAN 48964 (Ly H drawn from Othman, Yii et al. SAN 48861 (D. 222 Annals of the Missouri Botanical Garden PISTILLATE CALYX parts and inflorescences. Stipules triangular to elliptic, The pistillate calyx provides the best characters for identification. Unfortunately, many specimens only show spikes "i sanie fem. oas, the pres- ence of fi will enlarge or not. oo eae E e.g., Koilodepas brevipes), basally connate (e.g., K. laeviga- tum, Fig. 2C), or highly connate (e.g., K. bantamense; Fig. 2E). The calyx can cover only the basal half of the ovary (Fig. 2C) or it can completely hide the ovary, either loosely folded around it (Fig. 2D) or fitting very gay (Fig. E "n species yan show ex in fruit. The calyx dies. idi in fruit, ok only slightly in some species (K. , K. laevigatum, K. longifolium). In. most species, the calyx strongly enlarges (K. brevipes, K. calycinum, K. cor s hainanense, and K. pectinatum; Fig. 2F); this character is unknown for the New Guinean K. homaliifolium. STYLE AND STIGMA The style is the part on top of the ovary where the stigmas are still united, thus the part before the split. The style can be absent or present, depending on the species. The stigma apex is generally marked by a relatively deep bifurcation, as well as several smaller reations. The number of splits varies by species; it can be several to many times. When the number of ne is low, the individual stigmas are still visible (Koilode (Koilode. pas brevipes, K. cordisepalum, K. homaliifolium, K laevigatum [Fig. 2H], K. longifolium); when the apices are frayed multiple times and fanlike, the individual stigmas are not easily identifiable (K. bantamense [Fig. 2G], K. calycinum, K. hainanense, K. pectinatum). Taxonomic TREATMENT Koilodepas Hassk., Verslagen Meded. Afd. Natuurk. Kon. Akad. Wetensch. 4: 139. 1856. Conceveiba Aubl. sect. Coelodepas (Hassk.) Kuntze in T. Post & Kuntze, Lex. I 138. 1903, orth. var. Koilodepas Hassk. sect. Koilodepas Airy Shaw, Kew Bull. 14: 383. 1960. TYPE: Koilodepas bantamense Hassk. Calpigyne Me Mus. Bot. 2: 193. 1856. TYPE: Calpigyne et Hassk.). Nhs Gage. l. Soc. Bot. France 72: 467. 1925. 'ephrostylus poilanei Gagnep. (= Koilodepas longifolium Hook. f.). Hassk. sect. Hyalodepas Airy Shaw, Kew Bull. 14: 383. 1960. TYPE: Ko Koilodepas calycinum Bedd. a ee m (Koilodepas bantamense), monoecious; indument simple hairs, single or in stellate groups, often denser on younger late caducous, margin entire to (partly) erose to pectinate with even branching teeth, sometimes basal-marginal e nectaries, externally stellate groups of hairs, but internally with simple hairs. Leaves alternate to distichous, simple; petiole short, usually completely pulvinate, tomentose; blades usually elliptic or oblong- spi. Semele, Bern is esos, drying green or brown k ly ciii the margin iie to serrulate with teeth ending in small or glands, apex acuminate to cuspidate, adaxial surface smooth, generally glabrous, abaxial surface smooth, glabrous to o pubescent on veins and midrib only, extrafloral nectaries generally near the petiole junction, additional nectaries often nearby and often along the margin up to the apex, domatia absent; venation penninerved, slightly raised adaxially, distinctly ially, nerves looping and connected near the margin, tertiary veins often scalariform, others reticulate. Inflorescences spicate (ramiflorous, in K. bantamense and ba. nse ulous, completely stami- nate or lower flowers pistillate and upper ones staminate, the staminate part breaking off at fruit set; staminate flowers in dense clusters of generally 10 or more flowers per node, pistillate flowers solitary per node es ea afew staminate ones); rachis tomentose. Flowers nomor- phic; bracts present and, especially with the ee flowers, bracteoles also present, both with an often erose margin, outside » Ade milis g hairs and inside simple ones, ext L basally; petals and lec aboen. Staminate flowers small; ; pedicel very short, to 0.9 mm, widening apically, with few hairs; calyx generally 2- to 4-lobed, lobes valvate, stellate androphore that apically broadens, 4 to 8, ina circle, the filaments either sulcate in the lower 2/3 and narrowing apically with thecae divergent, or filaments threadlike (K. laevigatum) and anthers with parallel thecae, anthers subapically dorsi- fixed, opening introrse wi pistillode absent to ones; pedicels short, apically As sis. pubescent, completely and tightly with the calyx seemingly absent, (in some species, the calyx enlarging to cover the fruit), externally stellate bundles hairs, simple hairs iine ovary (ocular, villose, 1 ovule pe apically several times bifid FONS individually identi- fiable) to multifid and fanlike (individual stigmas not € iii iii. ———— IQ Volume 97, Number 2 van Welzen 223 2010 Revision of Koilodepas visible), the upper surface with long, branching stigmatic Guinea, d all oth inly A rn md papillae, tomentose beneath. Peach D one of Sumatra. (capsules), dehiscing completely septicidally and partial- ly loculicidally in the upper half, externally tomentose (somewhat scurfy), internally a few stellate hairs at the base; the wall woody; columella very sturdy, broadly obtriangular with large septal remnants. Seeds obovoid, somewhat flattened and keeled on the inside, smooth, die ien somewhat marbled, Ml triangular, | ] , flat The genus comprises nine species: and Sumatra (one extending to Java), one in New KEY TO THE SPECIES OF KOILODEPAS 1N SOUTHERN ASIA AND MALESIA Discussion. Hasskarl (1855, 1856) first used the Greek version of the genus name, which he: Jaler ehad (185131 1858) to a more Latinized form, . Koilodepas is the older variant and, therefore, is used in this revision. umen (1942) indicated the type e. the a This inaceuraté, because Hasskarl published a ide gin und Bie casis dr v oe t i specifica" are otherwise satisfied by Article 42.1 of the International Code of Botanical Nomenclature (McNeill et al., 2006). la. Leaf blades large, 13.5-34 X 3-13 cm, drying green, a Sa aaa tro pie ; free part of filaments threadlike, 1.3—2.4 mm long, Bing Ehe A CA 7. K. lb. Leaf blades small to large, 3.5-33 X 1.3-11.2 cm, drying greenish or brownish, margin (entire to) serrulate (to secondarily entire in die leaves) free part of filaments 0.4-1. ie mm long, of: which lower 2/3 sulcate, upper part thinner, anthers with divergent thecae; pistillate calyx enlarging 2a. Stipules oblong-ovate, 10-13 perpendicular to n part, teeth with secondary pe Pee Eee. 1 2 ee n Stipules es triangular, 1.8-10 X 0.6—1.5 mm, calyx "gine or not enlarging i in fruit; all areas. .5-3 mm (excluding MM pectinate in fruit; all areas. with up to 6-mm-long teeth, ER ak SIQUID eU i K. pectinatum A S š hb b LI o 3a. Leaf b th stror nlarging in fruit; Borneo 3b. Leaf blades at base flat: epe calyx lobes *........ oo p O A A A ao E K. brevipes au. S... enveloping ovary -— enlarging not enlarging i in = all areas. Tue Aa. illate c t ding in a sma "o d; stigmas no Ming cane Ss viible ck 2 20 So an cee ee a el T Pistillate calys enveloping ovary Fue ae — very d so and n a ier nmg? stigmas separately visible or not, due to strong apical splitting. 5a. Leaves drying green; pistillode 041 xs mm long; style (united part of m 0.8-1.6 mm long; stigmas 4—5.5 5 mm long, spically splitting, but ig "S 4. K cordisepalum 5b. I dor : long; stigmas 2-3.2 to stigma lobes densely "E et Samiha, few times and stigmas separately iy visibles al areas (but ur M z E ema er O erat se or with at most 1 or 2 upright teeth: urcco fruit ( , c "ES gh) d Fenil stigmas not separately visible; fruits 16-18 mm ode S sd era ye matra, Java, Pistillate calyx loose unknown for New Guinea K. homaliij gmas separately visible or not; fruits 12-16 mm wide (unknown India, China, Vietnam, Thailand, New r ew Guinea. à : us dn Ta. Stipules 4.3-9 X ings arg etimes erose : muto eio m nei : * bellas. calyx S — e 9» ^ $. $ e. visible; New Guinea ....-- t6 rt Tb. Stipules 1.8-8 X 0.6-1.5 mm, margin en ne a lobes connate in lower third; stigmas Thailand. 8a. Leaves drying gree nish, blade elliptic an — zm X oue € uie s —€— blade (ovate to) eae 8b. ves brownish to eke £ hainanense Es x. RP 9.9. s w to 10; China, Y 224 Annals of the Missouri Botanical Garden 1. Koi bantamense Hassk., Verslagen — 0.6—1.8 mm; pedicels 0.7—1.8(-22 in fruit) mm; calyx oilodepas Meded. Afd. Natuurk. Kon. Akad. Wetensch. 4: 140. 1855. TYPE: Indonesia. Java: originally collected in Bantam, type from cultivated tree in Bogor Botanical Garden, s.d., J. C. Hasskarl s.n. (holotype, L! [barcode L 0016250]). Figures 1A, B, 2E, G. frutescens Blume, Mus. Bot. 193. 1856. ds pyxis frutescens PSR ind. J. Arnold Arbor. 23: 49, 1942. K frutescens (Blume) Airy Shaw, Kew Bull. 14: 385. 1960. TYPE: PENSA Borneo: E Pamatton, s.d., P. W. (lectotype, designated by Croizat, 1942: 49, L! barok L 0016252), photo A!). i ichianum a. Hooker's mi PI. ~ t 1288. 1879, as Coelode, . Syn. ysia. Penang Hills, s.d., C. Porter s.n. (Hb. Koilodepas fe neum Hook. f., Fl. Brit. India 5: 420. 1887 syn. nov. TYPE: Malaysia. Malacca, W. Gri KD 5017 (holotype, K!; isotype, L! [barcode L Shrubs to trees to 27 m high, to 50 cm DBH; flowering branches 1.5-4 mm diam. Outer bark smooth, white to patchy gray and gray-green to gray- brown to honey-colored, papery, sometimes flaking, soft; inner bark pink to reddish brown to brown, thin, brittle-fibrous; wood medium hard, sapwood cream to yellow, heartwood yellow to orange. Stipules triangu- lar, 2-8 X 0.6-1.5 mm, margin often somewhat erose or with at most 1 or 2 upright teeth, mainly on one side. Leaves with the petioles 3-16 mm, round to flattened above; blades ovate-oblong to elliptic- oblong, 5.8-33 X 1.7-11.2 cm, length:width ratio 2.7—5.3:1, drying (greenish brown to) brown, base truncate to cuneate, flat, margin coarsely serrulate (to entire), flat to slightly recurved, teeth ending in a glandular region, apex acute to cuspidate, adaxial surface dull dark green, abaxial surface dull green; glabrous to pubescent along the basal midrib, secondary nerves 11 to 15 per side, often somewhat bullate between nerves. Inflorescences to 10.5 cm, yellowish green to pale brown, with the flowers white in bud to gray-yellow when dehi Sta flowers 1.2-2.4 mm basally; pedicels 0.9 mm; calyx 1-1.2 mm high, 3- or 4-lobed; lobes triangular, 0.7-1.2 X 0.8-1.4 mm; stamens 4 or 5, phore 0.70.8 mm high, filaments 0.7-1 mm, sulcate, anthers 0.2-0.3 X 0.3-0.5 mm, thecae divergent, yellow; pistillode absent or to ca. 0.2 mm. Pistillate flowers 2.5-3.5 mm diam.; bracts triangular, 2-7 X 1.2-2.3 mm, margin often with round extrafloral nectaries, often united with the bracteoles; bracteoles similar to bracts, much smaller, 1.8-2.5 x tightly urceolate and adnate to ovary, 2—3.3 mm high, 7- or , lobes inconspicuous, externally usuall with extrafloral nectaries on calyx tube, splitting into reflexed (to horizontal) lobes, in fruit the calyx not markedly increasing in size, to 3(-5) mm here TN 3-locula, 2-3 X 1.5-2.7 mm, style stigmas 1.5-2.5 mm, yellow, deeply da pas lobe split several times, spreading and fanlike, se compact, individual stigmas not visible. Fruits oung, 1.2 mm thick; eh I 6-10 x 1-8.5 X 7.2-9 X 6-8.2 mm Distribution, habitat, and phenology. Koilodepas bantamense is present in Thailand (southwestern and peninsular parts) and Laos; in Malesia it is found in the Malay Peninsula, Sumatra, Java, and Borneo. It is found in primary ergreen forest (Thailand), primary rainforest, M sometimes also in secondary forest, scrub, and overgrown rubber plantations on yellow-red loam above a granite or sandstone between 50 and 400 m. The species flowers from January to August and fruits in May, June, October, and November. Vernacular names. Sumatra, Lampung Province: kayoe toelan. Borneo, Sarawak: luti (Kayan language). Economic uses. The wood is used for wood carving, knife handles, and sheaths. 4.5—7.3 mm. Seeds Discussion. Koilodepas bantamense is a variable species and is very similar to K. longifolium and K. nanense. All three species often have generally elliptic-oblong leaves with an entire to coarsely serrulate margin. Specimens previously stored under antamense, ferrugineum, K. anum, and party under K. longifolium have pistillate flowers with a narrowly urceolate calyx (with or without glands) that does not enlarge in fruit. The stigmas are short and branch into d fans. The stipules generally have an entire calyces that are loosely fo around the ovary and that enlarge in fruit; the stipules also show more teeth. e calyx of the pistillate flowers of K. longifolium (including K. glanduligerum and K. subcordatum) reaches only to the mid-portion of the ovary and slightly enlarges in fruit; the stigmas are less often divided and generally have a longer unbranched basal portion; and the stipules usually have distinct teeth. The distribution of K. hainanense only slightly overlaps with that of K. bantamense in southwestern - However, K. bantamense and K. longifolium Volume 97, Number 2 2010 van Welzen Revision of Koilodepas largely overlap in distribution. Luckily, there is one more character that generally separates these two species: K. longifolium has very small glands on the marginal teeth of the leaf blades, while K. bantamense generally has glands that broadly cover the rounded apex of the marginal teeth. Dried material known as K. ferrugineum (only the type specimen) has a very dark brown indumentum and tends to be pubescent. The specimens referred to K. wallichianum have relatively large leaves with a truncate blade base, but this is otherwise the only differing character. The name K. wallichianum is treated as a synonym here, because a comparable variability in the shape of the leaf base is also seen in K. bantamense. Koilodepas bantamense and K. longifolium often have witch brooms that develop in the inflorescences, which differ by the species. In particular in K. bantamense, the bracts, bracteoles, and calices are enlarged, with only a few bracts within the calices, while in K. longifolium the bracts and bracteoles are normal, the calices are slender and on relatively long pedicels, but inside each calyx there are far-extending, spikelike struc- tures consisting only of bracts. Airy Shaw (1981: 311) indicates that the “witches’ broom” inflorescences are the result of mite attacks (Lérzing 16329, L). The names Koilodepas bantamense and Calpigyne frutescens were traditionally and previously treated as separate species, principally because different bota- nists reviewed different specimens and considered the ras of different islands: Java (Backer & Bakhuizen van den Brink f., 1963), Sumatra, and Borneo (Airy ae 1975, 1981), respectively. In specimens identi- as K. bantamense and C. escens, the typical Le in common are the strongly urceolate pistillate calyx, which coheres to the young ovary t dehisces when the fruit develops; the barely serrate leaves, especially in the lower half; the short stipules, less than 8 mm; and fewer stamens, four or five versus eight elsewhere in the genus. Blume (1856) did not gx the specimens he in the protologue for Calpigyne frutescens, only that they were from Sulawesi (Ce lebes) and Borneo. According to Miquel (1859), the Sulawesi collections were made by Forsten and the Borneo ones by hals. However, the Sulawesi specimens could not be retraced (they were probably a very different taxon, because Koilodepas bantamense is not known for this island), and Croizat (1942) selected a Korthals Specimen as lectotype from the material present in L. a (1942) indicated that his combination Ptychopyxis es was a nomen novum (and it Was subsequently treated as a new name in Koi by Airy sets [1960, 1975). "However, e » y refer (1856) LEUR rer ws iiy ue though he omitted to acknowledge Blume as author of the basionym. dditional specimens examined. INDONESIA. Jawa : F. W. Junghuhn 98 (L); Preanger, Palabuhan Ratu, S, H. Koorders 11754 (1), Jawa Timur: Bogor, cultivated at al n o sn. (L [barcode L 0034800], Mr Brien A 36 (L), Hortus Bogor- iensis IX.C.36a (L), Hi m XII.B.VII.145 (L). us nsis XILB.IX.39 (L). Kalimantan Selatan: 0382 (L River (Lae Sauraya) area, ca. 15 k of ong River, 2°55'N, a STE, W. 2 E 0. O. de Vid & B Wilde-Duyfjes 203 cd Sam c s (oer EZfw)90 (TY l E. de H. O. Forbes 1532 (D. C A. Lörzing 5615 (L); Cane co js water lintang, J. A. Lórzing 16329 (L) MALAYSIA. " Sembilan: Compart. 8, Gunung Angsi, H. S. Loh FRI 17343 (L). Sabah: Tawau, Tinagat Forest Reserve, J. Singh, A. Talip & Nordin SAN 48984. Sarawak: Kenaban River, Upper Plieran, 2738'N, 114^35'E, G. H. Pickles S 3520 (L), G. H. Pickles S 3527 (L). Terengganu: Ulu Sungai Trengan, P P. F. Cockburn FRI 8426 (L). idley 4426 anom, Prov., Haad Yai Distr., Ko Hong Hill, J. F. Maxwell 85-448 (L); Surat Thani Prov., Kaw Samui, N. Put 843 (L). South- western: Prachuap Khiri Khan Prov., Thap Sakae, Huay Yang Natl. Park, 11736'30"N, 99^33'80"E, D. J. Middleton et al. 2541 (L); Prachuap Khiri Khan Saphan, Huay Yang Natl. Park, 11°27'N, 99°25'E, D. E Middleton et al. 2603 (L). 2. — — Merr., Moon J. Sci. 30: PE: Malaysia 80. ds pas North lines, Senge July 1924, D. D. Wood 1291 (holotype, UC; isotype, K!). Figure IF, G. Koilodepas Airy — Kew Bull. hon — Merr. v 1960, syn — ‘(Airy he) Airy s aps Addit. spi - 138. 1975. TYPE: [Indonesia. Gunung So. en 1956, L. L. Forman 442 (holotype, K!; i nein: to 20 cm DBH; flowering branches 2-3 mm diam.; outer bark smooth, white to light brown; inner white to pale gray: sapwood white to yellowish white, Stipules triangular, 3.7-10 X 0.7-1.2 mm, margin often erose, generally with a round, black, shiny gland basally on one side. Leaves with the petiole 3-7 mm, round to channeled above; blade elliptic to oblong (or ovate), 8-32.5 X 2-11 em, length:width ratio 2.7-5:1, drying brown, base truncate to rounded (to cuneate), poculi- form (convex), margin coarsely serrulate with glandu- Annals of the Missouri Botanical Garden lar teeth, strongly recurved at base, apex caudate, — abaxial surface subglabrous to somewhat venation, nerves 13 to 15 per side, — halla between the nerves. Inflorescences to 10.5 em long, greenish brown. Staminate s 1.3— 1.7 mm diam., green to pale white-yellow to yellow to yellowish gray to white, fragrant with the smell of lemon; bracts triangular, 0.6-2.2 X 1—2.2 mm, margin often with teeth, at base with round, shiny extrafloral taries; pedicels 0.3-0.8 mm; calyx 1.3-2.2 mm high, with 3 or 4 lobes, the latter 0.6-1 X 0.7-1 mm; stamens 6 to 8, androphore 0.6-1.5 mm, filaments 0.7-0.9 mm, sulcate, anthers ca. 0.3 X 0.3-0.4 mm, thecae divergent; pistillode 0.30.7 mm. Pistillate flowers ca. 2.2 mm diam.; bracts triangular, 2-3.5 X 1-2 mm, margin serrate, with basal glands; bracteoles similar to bracts, smaller, 1-1.5 X pedicel ca. 0.3 mm, lengthening in fruit to 16 mm; calyx with 6, 8, or 10 free or basally connate lobes, the latter triangular, 1.5-1.8 X 0.7-0.8 mm when young, extending in fruit up to 12 X 2 mm, basally and often fway along margin with round, shiny extrafloral nectaries, less conspicuous when young, but distinct in fruit; ovary 3(4)-locular, 1.8-2 X 1—1.3 mm, style 1-3 mn, stigma 1.8-3 mm, the apex gan te twice to several times, ak with 2 or 3 main lobes, stigmas individually visible. Fruits lobed regmata, 14—18 x 11 mm, red to reddish black to golden brown; wall ca. 0.8 mm thick; columella 7-8 X 8-9 mm. Seeds ca. T X 6.56.8 X Distribution, habitat, and phenology. Koilodepas brevipes is endemic to Borneo in primary or disturbed forest, on flat to undulating terrain or ridges, and along roadsides on dark red-brown to yellowish black soil, sandy loam, or sandstone at altitudes up to 330 m. The species flowers in January, March, April, July, and August to November; and fruits in March, August, October, and December. V ular names. Borneo, Sabah: ulas; Kaliman- tan Timur: kaju gading. Discussion. Airy Shaw (1960) published Koilode- pas stenosepalum, which he later transferred as K. brevipes var. stenosepalum (Airy Shaw, 1975). Howey- er, I could not detect — differences between K. brevipes var. brevipes and K. brevipes var. steno- sepalum. The calyx lobes of the pistillate flower are short in flower and become longer and slender in fruit. Koi brevipes var. stenosepalum was noted by Airy Shaw (1975) to have longer, more slender — t other than the basal connection between th sepals, which is present in K. El var. brevipes be less distinct in variety stenosepalum, the plants represent the same taxon. The most typica for K. brevipes is the poculiform base of the leaf blade, as well as the pistillate sepals, which are almost and extending in length in fruit. There seems to be no difference between the two varieties, and K. brevipes var. stenosepalum is synonymized here. Additional specimens examined. INDONESIA. Kaliman- tan Tengah: Headwaters of Sungai Kahayan, 5 km NW of an logging cam » Sikatan Wana Raya concession, 035'5 1325 E J S & Tukirin et al. 707 (L); Upper Katingan Rivet ca. eee km WNW of Tumbang ase Camp, ca. 96 km W of Batu Badinding, 1°15’S, 112°40’E, J. P. e ee e Upper Katingan e ca. Ll. km WNW a Samba, K.T.C. loggi ar Central Base , Ca. 55 km W of Batu Badinding, 1° “15S, 11240, J. m "Mars 4427 (L); Ulu Barito, P.T ca. Km 20, K. Sidiyasa PBU603 (L); ; KTC Tumbang Sah, Km 96 Kotio River, 1° e S, 113°10’E, H. Wiriadinata 3518 (D. nu ur: Gunung qe Amdjah 365 (L); Berau Inhutan m 16, trayek D. 920 (L); c Ritan, T 32503 (L); B , along transect L, 1°50'N, 117°08'E, PJ J. A. Kefler et al. Berau 857 (L); Bulungan, Sebakis River region, A. J. G. H. Kostermans 9317 be Central Kutei, Belajan River, near Long Kostermans 10326 iR . Kostermans 21079 (L); Nunukan Meijer 1913 (L); ca. 15 km NE of camp of P. T Kut C., Taban Murata et al. B- 939 (L); Batu Penalong, (L); Long Le'es, Kecamatan I: 1169 (L). MALAYSIA. Sabah: Mostyn, Ulu elem Ahmad SAN 208212 (L), Elmer 21 512 (L); Tawau, Merotai Besar, A. Gi SAN 31331 (L); Kalabakan, Bukit Tuku, mi. 8, Luasong Rd., F. En = 95856 56 (L); Kalabakan, Ulu Sungai Sepaku Forest Rese ; ig Sigin & Ismail SAN 60275 (L); Lahad Datu, Bukit Silam, H. T. ——* api 57289 (L); Tawau, Sub-compart. 4, compart. 5 rmah T.C. Concession, Kalabakan, 30 mi. WNW of Tawau, x H. = m 4106 (L). Sarawak: Kuching, Selang Forest Rese . Paie S 8463 (L); 4th Division Miri, Suai, Block 15, €—— E Co. area, I. Paie S 39175 (L); 3rd miss s iine u Sungai Arip, Bukit Iju, Sibat ak oo 656 (L); Ath s D Nyabau catchment area, Sad ak Luang S 24520 (Ly Kuching, Sasha L. P. Zehnder S 9570 (L). 3. Koilodepas calycinum Bedd., Fl. Sylv. S. India: 207 (manual), Ju 320 (part 2). 1873 “Coelodepas.” : India. Tinnevelly Hille Forests/Ghats, 2000 ft., s.d., R. H. Beddome 7329 (holotype, BM!; isotypes, K!, MH not seen). Small trees, to 6 m high; flowering branches 1.5- 2 mm diam. Bark and wood unknown. Stipules triangular, 1.8-3.5 X 0.6-1 mm, margin with teeth to 1 mm, often a round, black, shiny gland basally on one side. Leaves with the petiole 2-5 mm, somewhat flattened above; blade elliptic (to obovate), 3.5-15.5 Volume 97, Number 2 2010 van Welzen Revision of Koilodepas X 1.3-5 cm, length:width ratio 2.7-3.1:1, drying green, base rounded, margin regularly crenulate to serrulate with glandular teeth, flat, apex acuminate to cuspidate, with cusp rounded, abaxial surface gla- brous, nerves 9 or 10 per side. Inflorescences to 10 cm. Staminate flowers [not seen, described from sketch on K type] minute; pedicel very short; calyx 3- or 4- lobed; stamens 4 or 5 on a short androphore, filaments suleate, thecae divergent; pistillode not depicted. Pistillate flowers with the bracts triangular, ca. 2.2 X 1 mm, margin entire, bracteoles not seen; pedicels 6— 7 mm in fruit; calyx ca. 2.5 mm high, enlarging to 14 mm in fruit, connate in the basal third, somewhat pubescent on both sides, lobes triangular in fruit, 2— as X 3—4 mm, extrafloral nectaries present espe- cially on the connate portion; ovary 2- or 3-locular, style absent, stigmas 2-2.5 mm, flat, spreading, stigmas not separately visible. Fruits lobed regmata, 13-16.7 X ca. 9 mm; wall ca. 0.8 mm thick; columella ca. 6 X 6 mm. Seeds ca. 6.5 X 6.2 X 5.8 mm. Distribution, habitat, and phenology. Koilodepas calycinum is endemic in southern India (Tamil Nadu State), where it is found fruiting in May at altitudes between 670 and 830 m. Economic uses. Good timber. ce specimens examined. INDIA. s. loc., R. Wight 2677 (L); Tinnevelly Hills, Beddome s.n. (BM). 4. Koilodepas cordisepalum Welzen & Muzzaz., sp. nov. TYPE: Indonesia. Sumatra: Atjeh Prov., Middle Alas River (Lae Sauraya) area, ca. 15 km N of Gelombang, S of Bengkong River, 80 m, ca. 2°55'N, 97°57'E, 25 July 1985, W. J. J. 0. de Wilde £ B. E. E. de Wilde-Duyfjes 20339 (holotype, L!). Folia viridia in sicco, margine grosse serrulata, nervi ee quaternariisque in paginis ambabus bene visibili- ` Flos staminatus: stamina 5 ad 7, basi Flos Pistillatus: calyx usque ad 3.2 mm altus (in fructu usque ad 55.18 mm accrescens), lobis 6 basi connatis triangularibus 8 aam longis 1-1.5 mm latis (in fructu usque ad ca. m ongis latisque accrescentibus); stylus 0.8-1.6 mm WT 4—5.5 mm longis. Shrubs or trees, to 12 m high, to 30 em DBH. Stipules triangular, 2.5-5.5 X 0.7-1 mm, margin slightly erose, basally generally a round, black, shiny gland on one side. Leaves with the petioles 2-9 mm, round; blade ovate to elliptic to oblong, 8.5-22 X 2.4-10 cm, length:width ratio 2.2-3.5:1, drying green, base rou flat, margin somewhat recurved, Cheney serrulate with glandular teeth, apex caudate; abaxial surface slightly pubescent on midrib, venation distinet, also quaternary veinlets, nerves 10 to 13 per side, slightly bullate between the nerves. /nflores- cences to 10 cm, pale gray-green to pale creamy brownish green; flowers fragrant. Staminate 1.1-1.5 mm diam., (dirty) creamy white; bracts triangular, ca. 2.2 X 1.5-2.2 mm, margin entire, with a round, shiny extrafloral nectary at base, bracteoles not seen; pedicels 0.3-0.7 mm; calyx 1.3-2 mm high, with 3 or 4 lobes, latter 0.4-0.8 X 0.8-1 mm; stamens 5 to 7, androphore 0.7-1.5 mm, filaments 0.4-1 mm, sulcate, anthers ca. 0.3 X 0.6-0.7 mm, thecae divergent, yellow; pistillode 0.8-1 mm, 1- or 2-lobed. Pistillate flowers 3.6-3.7 mm diam., greenish cream; bracts triangular, 2-3.3 X 0.6-2 mm, margin entire, basally with 1 or 2 glands; bracteoles smaller, 1.2-1.3 X 0.3-1 mm; pedicels 0.8-1 mm, lengthening in fruit to 5 mm; calyx basally united, to 3.2 mm high (enlarging in fruit to ca. 18 mm), lobes 6, triangular, 2.3-2.8 X 1-1.5 mm (enlarging in fruit to ca. 8 X 8 mm), extrafloral nectaries absent; ovary 3-locular, ca. 1.5 X 1 mm, style 0.8-1.6 mm, stigma 4—5.5 mm, pale (greenish) yellow to pale purplish white, the apex split into 2 major branches, each with 3 lobes, stigmas individually visible. Fruits lobed regmata, only young one seen, ca. 10 X 6 mm, dull brownish green or yellowish green; wall ca. 0.8 mm thick; columella ca. 6 X 4-45 mm. Seeds ca. 6 X 6 X 5.3 mm. Distribution, habitat, and phenology. Koilodepas cordisepalum is endemic in Sumatra (Province Aceh, Gunung Leuser Nature Reserve), where it is found in (logged) primary hill forest and riverine forest, on sandstone, alluvial, or yellow-red loamy (rich in lime) 1 Ann th `. La yla UY "ar. AÑ SOLL DCiwccr TV oem and August and fruits in May and July. IUCN Red List category. | Koilodepas cordisepalum is considered Vulnerable (VU Bla) according to IUCN Red List criteria (IUCN, 2001). The species is deemed vulnerable because it is only present in a few locations in the i northern Sumatra. The park clearance for road-building and oil palm plantations, with the forested area diminishing in size and quality each year (De Wilde, pers. comm.). Discussion. Airy Shaw (1981: 311) previously indicated that material from Sumatra (de Wilde & de Wilde-Duyfjes 12463) might be a new species, but due to lack of sufficient material, he referred the specimen to Koilodepas cf. hainanense on the basis of the enlarging pistillate sepals and green color of the dry leaves. However, the type of K. hainanense (W. Y. Chun 1092, A!) has leaves that dry brown and woe 2 PE k h H üa 3 9 mm bu Thus, the specimens from Sumatra are indeed an identifiable new species. Other typical characters 228 Annals of the Missouri Botanical Garden for this new species are the coarsely serrulate leaf ^ absent; pedicels 0.1—0.4 mm; calyx 1-1.2 mm high, margin and slightly bullate venation; the five to seven stamens that are connate at base; the pistillate calyx that is 3.2 mm high and enlarges up to 18 mm in fruit, and of which the six lobes are 2.3-2.8 X 1-1.5 mm and enlarge to a length of ca. 8 mm; and the long style (0.8—1.6 mm) and stigmas (4—5.5 mm). In morphology, the species closely resembles K. calycinum from India and K. hainanense from Thailand to southwest China. a NS. INDONESIA. Sumatra. Aceh: Gunung Leu- ure Reserve, Ketambe, valley of Lau Alas, near den die tna ME NW of Kutatjane, W. J. J. O. de Wilde & B. E. E. de Mig ndi ad a SR Nature Reserve, Sungai Kloët, along Kru poo dc 305'N, 97°25' E, W. J. J. o de Wilde & B. E. Wilde-Duyfjes 19626 (L); vic. Pucuk Lembang, 3°05'N, ie W. J. J. O. de Wilde & B. E. E. Lae Batu Batu, near abandoned village of Belingtang, 2°43'N, 97°54’E, W. LL 0. de Wilde & B. E. E. de Wilde-Duyfjes 20623 (L). 5. Koilodepas hainanense m Croizat, J. Ar- nold Arbor. 23: 51. 1942, “Coelodepas.” Basionym: Calpigyne Missis Merr., J. Arnold Arbor. 6: 135. [30 July] 1925. TYPE: China. Hainan: Nam Fung [Nam Fong/Namfeng], 21 Mar. 1920, W. Y. Chun 1092 (holotype, A!; isotype, A!). Fiji 2D, 3G-I. Nephrostylus poilanei Gagnep., Bull. Soc. Bot. France 72: 467. [Aug.] 1925, syn. nov. TYPE: Vietnam. Annam Prov., Ca-na, 8 Mar. 1923, E. Poilane 5694 (holotype, Pl; isotype, P!). Tree(let)s, to 15 m high, to 4 cm DBH; flowering branches 1.5-2.3 mm thick. Bark smooth, gray-brown. ro triangular, 3.5-8 X 1-1.5 mm, margin slightly erose, with some up to l-mm-long teeth, glands absent. with the petiole 0.5-1.2 mm somewhat flattened above; blade elliptic-oblong (o ovate to obovate), 6.5-22.5 X 2.1-7.5 em width ratio 3—3.5:1, drying brownish green to some- times green, obtuse to rounded, flat, margin flat, finely serrulate with glandular teeth to (secondarily) almost entire, apex acuminate, adaxial surface dark green, abaxial surface slightly pubescent on major venation, slightly paler than adaxially, nerves 10 to 18 per side. Inflorescences up to more than 10 cm; flowers lemon-yellow, scent strong, unpleasant. Sta- minale rs 1-1.5 mm in diam.; bracts ovate to triangular, ca. 1.7 X 2.2 mm, margin entire, glands with 3 or 4 lobes, latter 0.7—1 X ca. 0.7 mm; stamens 4 or 6, androphore ca. 0.3 mm, filaments ca. 0.6 mm, sulcate, anthers ca. 0.3 X 0.6 mm, thecae divergent, pet pistillode ca. 0.3 mm, broad. Pistillate flowers mm diam.; bracts long-triangular, 5—5.3 X ca. argin entire to glandular-toothed; bracteoles Ta pe broad-triangular, 2—3.5 š pedicels short to up to 18 mm in fruit; calyx Lens united, up to 3.5 mm high (enlarging in fruit to ca. 19 mm), lobes 8 to 10 (enlarging in fruit to 18 X 6 mm), folded around ovary, with extrafloral nectaries in mainly the united part; ovary 3-locular, ca. 2 X 1.5—2 mm, style absent, stigmas 2-3.2 mm, flat and spreading, top broad and hardly split to split into 2 major branches and each branch split several times less deep, fanlike, individual stigmas not visible. Fruits lobed regmata, 12-15 X 10-11 mm, green with orange tinge to brown-green; wall ca. 0.8 mm thick; columella 6-8 X 5—7 mm. Seeds ca. 6 X 6 X 5 mm. Distribution, habitat, and phenology. ^ Koilodepas land, and is locally fairly common in (disturbed) ex evergreen forest, often along rocky shores of reams on sandy soil above a granite bedrock at i n. to 320 m; the species flowers in March and June and fruits in March, April, May, and August. Vernacular name. China: pak tsa shu. Discussion. Airy Shaw synonymized Nephrostylus poilanei with Koilodepas longifolium (1960), but later changed his mind (1963) and placed both Calpigyne hainanensis and N. poilanei within the synonymy of K. wallichianum [= K. longifolium herein]. Herein, K. hainanense is considered a distinct species and includes the synonym N. poilanei. The two epithets were published in the same year, but Merrill's name (C. hainanensis) was published a few months before agnepain's name (N. poilanei; see above). Therefore, Croizat's new combination of Merrill's name is the correct name. Koilodepas hainanense differs from K. bantamense and K. longifolium in that the pistillate calyx enlarges with fruit maturity. See the discussion under K. bantamense for further differences among these species. Additional specimens examined. CHINA. Hainan: Ching Mai ia n LE Ling, Tung Pin Tin village, C. I. Lei 536 T D. South-eastern: Trat Prov., Koh Chang n] Mayom Waterfall, 12°00'N, 102°40'E, C. F. usekom & T. Santisuk 3188 (L); Trat Prov., Koh Kut Mani, hills around Ao Yai Bay, 12°00'N, 102740" E, C. F. Krachan, Kaeng Krachan Krachan Natl. Volume 97, Number 2 2010 ITI HJ UR ⁄ SAT | LT HT] < Z 2277 4l] 22727771] C x LÀ 72 f iP E 177 — 1 mm Figure 3. A-F. Koilodepas longifolium Hook. f. —A. Habit. —B. Leaf blade margin with abeat a -9 visible. —C. Stami IDs £ bud, with 2n p 1 3 pi St E E f flower. k kutay apina (Merr.) Croizat. —G. Fruit. —H. Columella after dehiscence. — Seed. A a 8 Kostermans & Anta 717 (1); B-F drawn from Rahim A 409 (Ly; G-1 drawn from van Beusekom & Santisuk 3185 (1). Annals of the Missouri Botanical Garden Park, trail to Dd 12*50'24"N, 99^18'E, D. J. Middleton et al. 3342 (L). V Nha, Km 19 HCM hers m western, e hia. Thin 010812.1 7 (L). D m Phan-rang, 11/14 in 1909, C. d'Alleizette s. 6. Koilodepas homaliifolium Airy Shaw, Kew Bull. 36: 609. 1981. TYPE: [Papua New Guinea.] Terr. of New Guinea, Central Distr. Port Moresby sub-distr., Kuriva Forestry Area, near Veimauri River, 6 May 1971, H. Streimann & A. Kairo LAE 51550 (holotype, K!; isotype, L!). Figure 1C, I. Trees, to 24 m high, bole to 18 m, straight, to 38 cm DBH; crown spreading; flowering twigs ca. 3 mm in diam. Outer bark brown to dark gray, papery, flaky; middle and inner bark red, layered; wood very hard and heavy, sapwood straw-colored, heartwood yellow- ish straw colored. Stipules oblong-ovate, 4.3-9 X 1— 1.5 mm, margin entire but apically sometimes erose, glands not observed. Leaves with young flush drying reddish; petioles 3-8 mm, channeled above; blade NM 10.5-23 X 4.1-8.3 cm, length:width 2.6-3.3:1, drying brown, base emarginate to biad in margin laxly serrulate, teeth round- ed, glandular, apex acute to acuminate, adaxial surface dark green, abaxial surface somewhat pubes- cent when young, especially on venation, green, nerves 1l to 15 per side. Inflorescences to 16 cm; flowers gray to yellow. Staminate flowers ca. 1 mm diam.; bracts triangular, ca. 1.8 X 1.8 mm, margin probably entire (not well visible in scarce material), extrafloral nectaries not seen; pedicel at most ca. 0.3 mm; calyx 3-lobed, lobes almost completely free, elliptic, ca. 1 X 0.7 mm, apex rounded; stame androphore ca. 0.3 mm, filaments 0. 5-0.7 mm, sulcate, anthers ca. 0.3 X 0.5 mm, thecae divergent; pistillode present. Pistillate flowers ca. 4.2 mm diam sessile; bracts triangular, ca. 2.5 X 0.8 mm; feuite- oles minute; calyx 6-lobed, ca. 2.1 mm high, lobes acute; ovary 3-locular, ca. 2 X 1.5 mm; style ca. 0.5 mm, stigmas ca. 2.5 mm, apex d individual stigmas visible. Fruits and seeds unknow ion, habitat, a. ean Koilodepas eae is endemic in Papua New Guinea (Central Province) in the understory of lowland rainforest at ca. 70 m; the species flowers in February and May. Discussion. Airy Shaw (1980: 122) already no- ticed that the single specimen then known from New Guinea constituted a new species. More material confirmed his view. Typical for the Species are the long, narrow, mainly entire stipules, the leaves drying brown, the almost free pistillate calyx lobes, and the stigmas that can be individually seen. It is the only species of Koilodepas from New Guinea and is probably related to the west Malesian species with a non-enlarging pistillate calyx with almost free lobes (e.g., K. laevigatum and K. longifolium). Additional specimens examined. PAPUA NEW GUINEA. Central: Mt. Lawes, 200 ft., 9°30'S, 147°10’E, K. J. White NGF 10732 (L). ds E laevigatum Airy Shaw, Kew Bull. : 83. 1969. TYPE: Malaysia. po 4th img Bukit Mersing, Anap, . 1964, ibat ak Luang S 21928 i Kt Lr _L!). Figure 2B, C, H. Koilodepas longifolium Hook. f. var. integrifolium Airy Shaw, TYPE: [Malaysia. Sabah:] eo, Bongkoka Kadas, 135 ft., 27 Apr. 1932, P. Orolfo 1821 (holotype, K!; isotype, L! [incorrectly as P. Keeper 1821]). (Small) trees, to 15 m high, bole to 5 m high, straight, to 28 cm DBH; flowering branches 2-3 mm thick. Outer bark smooth to much grooved to flaky, gray or grayish white to white-brown, thin or papery; inner bark pale green to orange-yellow to reddish yellow to ochre, hard; sapwood pale white to yellowish orange. Stipules triangular, 2-4 X 1-1.7 mm, margin erose, late caducous, glands absent. Leaves with the petiole 6-11 mm, channeled above; blade elliptic to oblong (to ovate), 13.5—34 X 3-13 cm, length:width ratio 3.3—4.5:1, drying green, base broadly cuneate, margin irregularly entire, seldom with one or a few teeth near the apex, flat, apex acuminate to cuspidate, abaxial surface glabrous, nerves ca. 12 per side. Inflorescences to 7 cm. Staminate flowers 1-1.3 mm diam. (excluding stamens), pale greenish to whitish to pale pes bracts ovate, ca. 2 X 1.6 mm, margin slightly erose, basal marginal gland on one side; E ca. 0.3 mm; calyx 1.2—1.4 mm high, glabrous, with 2 or 4 lobes, lobes triangular, ca. 0.6 X 0.6— 2 mm s 4 or 5, androphore ca. 0.9 m ico ¡liesdliko, 1.3-2.4 mm, ow des ovate, ca. 0.4 X 0.2-0.3 mm, thecae parallel, E pistillode ca. 0.3 mm. Pistillate diam. (excluding stigma), green to yada oes to white; bracts ovate, 2.3-2.5 X 2-23 mm, margin erose; bracteoles like bracts, triangular, 1.7-1.8 X 0.7-0.8 mm; pedicel ca. 2 mm, extending to 12 mm in fruit; calyx with 8 to 12 lobes, basally connate, lobes triangular, 0.7-2 X 0.5-1.7 mm, usually glands on united part and on lobe apices; ovary ca. 2.3 X 3 mm, 3-locular, light green with ochreous brown hairs to pink, style 0.5-1 mm, stigmas 3.3-6 mm, lower half folded, upper half deeply bilobed, stigmas individu- ally visible. Fruits lobed regmata, 15-18 X 10- ll mm, pale gray and white (immature) to pale volume 97, Number 2 2010 van Welzen Revision of Koilodepas 231 yellowish; calyx + recurved; wall ca. 1.5 mm thick; columella 9-10 X 8-9 mm. Seeds 8-10 X 8-10 X 6.5-8.7 mm. Distribution, habitat, and phenology. Koilodepas laevigatum is endemic to Borneo (Sabah, Sarawak, Kalimantan Timur), where it is found in dipterocarp forest and secondary forest, generally on hills on sandy soil, sandstone with shale, basalt, and conglomerated clay-stone and sandstone at altitudes up to 750 m; the species flowers in February to May and de to October, and fruits in May and August. Malaysia, Sabah: akar, kilas M. E (kay) (Kedayan) (Keith, 1938, 1952, as “Aporosa | brevipetiolata”); puti [?pati] (Dusun Rongos); kilas (Bajau Lobok); rongrongkoi (Malay); kelis-kelis (Dusun Kinabatangan). Sarawak: puti (Iban) (Airy Shaw, 1960). Discussion. Koilodepas laevigatum is one of the species of Koilodepas found on Borneo, which is a hot spot for this genus. When flowering, K. laevigatum can be distinguished from other species of Koilodepas by the different type of stamen (threadlike filaments, el thecae) and the pistillate calyx that does not enlarge in fruit. Vegetatively, the leaf blades are generally larger than those of the other Bornean species, and they dry green instead of generally brown. Additional ie examined. INDONESIA. Kaliman- = T. P Sungai Mentaya, Kab. otawaringin Nine. 1°29'S, 112°31'E, E. R. Latupeirrissa " (L). Kalimantan Inhutani area, Km es plot 4, Ambriansyah et al. Berau 837 (L); E Buntung, 1°50'N, 117°15'E, R. Geesink 9344 (L); i" ung ng, ca. 70 km S of Tanjung Redeb, Berau, ; 30’N, 117°20'E, M. Kato, M. Okamoto & K. us M MALAYSIA. Sabah: arta HS. Bod Timur: Berau ai Menanggul, al SA SAN H 1 7587 (L); pas Marudu, Kampung Palu Sumbu, A. Gibot SAN 100030 (L); Pandewan, Sungai Pamentarian, F. [1 SAN 120047 (L); Sandakan, Sepilok Forest E Jalan Hujong Tanjong, W. Meijer SAN 141519 (D: tian, Kalabakan, K. Muroh SAN 75304 (L); Sandakan, Sepilok Forest Reserve, Compart. 13, D. J. Nicholson SAN 776 (L); Danum Valley, C. Gk Ridsdale 1965 (L); K ol SAN 51113. 13 i Beaufort Sungai Jelalong, Sungai Ebau, n "ded ]ision, Kapi pit, path to Bukit Mabong, Ulu Selada, Melinau, aie S 24270 vi Tau Range, Bukit Mersing, J. W. Purseglove P.5195 8. RU NM Bd: f., Fl. Brit. India 5: 420. 1887. TYPE: Malaysia. Perak, Larut, Aug. 1884, King’s collector 6502 (holotype, K!). Figures 1D, H, 2A, 3A-F. Pflanzenr. IV, 147. vii: i20, ip 420 191 a ^ E: Garden Jungle, H. N. Ridley 6481 flectetspe, designated here, E re Th 7 Gage, Rec. Bot. Surv. India 9: 239. 1922, as “Coelodepas subcordatus.” TYPE: Malaysia. Malay Peninsula, Penang, Bukit Penara, Oct. 1887, c Curtis 1271 (lectotype, designated by Airy Shaw, 1960: K). Small trees, to 12 m high, to 18 cm DBH; flowering branches 1.5-2.3 mm thick. Outer bark white to light brown, smooth, slightly papery; inner bark pink, thin; wood yellow. Stipules triangular, 3.7-8 X 1- 1.2 mm, late caducous, margin with several upright teeth {to entire or somewhat erose), basal . Leaves with petiole 3-20 mm, round; blade elliptic to elliptic- oblong, 8.5-27 X 2.7-8.2 cm, length: :width ratio 3.1— 3.2:1, drying brown, base rounded to cuneate, margin coarsely serrulate (to Ms flat to slightly recurved, teeth. ending in a small and narrow gland, apex acuminate to cuspidate, sometimes mucronulate, adaxial surface medium to very dark green, shiny, abaxial surface glabrous to pubescent along midrib and basal nerves (Borneo), paler green, nerves 9 to 15 per side, sometimes somewhat bullate between nerves. Inflorescences to 12 em, dark yellow, some- brown pubescent, branching, with flowers consisting of calyx cups, each containing a short spike of bracts. Flowers pale green with a silvery tinge to cream to yellow. flowers 0.8-1.3 mm diam.; bracts broadly ovate, 0.7- extrafloral nectaries; pedicels 0.2-0.8 mm; calyx with , lobes entire or bilobed, sometimes split and seemingly 3 or 4 free sepals, 0.9-1.2 mm high, teeth triangular, 0.5-0.6 X 0.4-0.8 mm, all acute; stamens 4 or 5(or 6), androphore 0.2-0.4 mm high. filaments 0.5-0.6 mm, wi wa anthers ca. 0.3 X au. l 0.4 mm P Pistillate flowers 1. 73 n mm diam.; bracts ‘ieee 2.5-4.7 X 0.7-1 mm, sometimes glandular, margin s es similar to bracts, 1.2-2.5 X 0.4-0.9 mm; pedicel 0.8-2.3(-11 in fruit) mm; calyx only enveloping lower half of ovary, 0.6-1 mm high, extrafloral e ide. 17-2 X 182 mm, style 0-0.8 mm. stigmas 1.5-2.1 mm, deeply bilobed apically for 1- 22 mm, each lobe split somewhat, stigmas individ- ually visible. Fruits lobed regmata, 12-14 X 8.5 Annals of the Missouri Botanical Garden 10 mm, dark yellow to brown; wall 0.8-1 mm thick; columella broadly obtriangular, 6—6.5 X 4—6 mm, with a few caducous stellate hairs basally. Seeds 6.5—7 X 7-7.5 X 5.2-6 mm A habitat, and phenology. | Koilodepas longifolium is present in ae Lg (Y nn the Malay Peninsula (incl Province, Bangka ed d Baan (Sabah, js, Sarawak), where it can be found in primary mixed lowland dipterocarp forest and kerangas forest on sandstone, diorite scree, granitic sand, sandy clay, or clay loam at altitudes between 6 and 330 m; it flowers in January to October and December and fruits in January, June, July, and September. Small black ants create "earth" nests among the fruits. Vernacular names. Peninsular Malaysia: seman- tum. Borneo, Sabah: kilas (Brunei Benuni); Sarawak: bantas (Iban). Discussion. Kollodepas MNA is character- ized by th teeth of the leaf margin, the short pistillate calyx (only enveloping the lower half of the ovary) with non-enlarging lobes, and the stipules with teeth that point upward. The species concept within the K. banta K. haina- nense-K. longifolium complex (see discussion under K. bantamense) appeared to be difficult and m many identifications were incorrect. A similar problem occurred with the syntypes used to describe K. igerum and K. subcordatum; t they too were mixed collections, which necessitated the selection of lectotypes. Koilodepas subcordatum was lectotypified by Airy Shaw (1960: 387), but K. glanduligerum still requires lectotypification. Of the three specimens cited my Pax and Hoffmann (1914: 270), one specimen (H. N. Ridley s.n., Malay 1 Bukit Mosis cni: not be located and the ot Les 422 K) appears to represent K. biben. The remaining specimen, H. N. Ridley 6481 (K) is e designated as lectotype here. 6, Ad specimens examined. BRUNEI. Belait: Labi, ai Rampayoh, 4°22'N, 114°28’E, M. J. E. oe e > (L); Andalau Forest Reserve, part. 6, Ç. Wood, B. T Smythies & P. S. Ashton SAN iow di INDONES IA. Sumatra. Rise Tandjong Pinang, Teijsmann s.n. (L [barcodes peesi a L 0034878)). o Selatan: Bangka, Gunung Mangkol, A. J. G. H. Kostermans & Anta 717 (L). MALAYSIA. Jee Kluang Forest Boas PF RI 7537 (L); Gunung "Pant Forest Reserve. Compart. 64 Fast, Reserve. K. M. (L). Perak: Dindings. South Pangkor . M. Burkill & M. Shah HMB 179 (L); Dindings, South P. Forest Reserve, H. M. ill & M. hah as Pulau Piu: Pangkore, C. Curtis 1374 (K, paratype of K. s )- : Kalatuan, A. Rahim A 409 (L) e Cunung Santubong, P. S. Ashton S 21494 (L); 4th Di Miri Distr., Niah River, Ulu Sungai Sekaloh, E. Wright $ s 291 17 (L); Baraza, Marudi Forest Reserve, A. Yaci 5 8292 (L). SINGAPORE. Nee Soon, Hardial 352 (L); Upper MacRitchie Reservoir area, J. F. Maxwell 81-113 ia mes Chu Kang Rd., 15 Apr. 1901 & 9 Oct. 1901, H. N. R. (K); Botanic Gardens” Jungle, Jan. 1915, H. N. ake e D ee Gardens’ Jungle, J. Sinclair SF 40668 (D. ILAND. Peninsular: Pattani, Yala, N. Put 3696 (L). 9. Koilodepas pectinatum Airy Shaw, Kew Bull. E: Malaysia. Sabah: Lahad ilabukan pe Reserve, Kennedy Bay, 15 Oct. 1963, H. nanggul SAN 39941 (holotype, K!; sean Fig- ures 1E, 2F. (Shrubs to) small trees, to 17 m high, bole to 11 cm high, to 8 cm DBH, girth 45 cm; flowering branches 2-3.5 mm thick. Outer bark smooth, whitish to gray to black, papery; inner bark pale yellow to yellowish ed 5-3 mm (excluding teeth), pectinate with up to 6-mm-long teeth, teeth perpendicular to main part, with secondary perpendicular teeth. Leaves with petiole 3-15 mm, round to reniform near blade; blade oblong, 7-28 X 2.4—10.7 cm, length:width ratio 2.6— 3.8:1, drying brown, base rounded, margin serrulate with glandular teeth, apex acuminate to caudate, abaxial surface subglabrous to rather pubescent, most often on venation, nerves 10 to 14 per side, often bullate between nerves. Inflorescences to 12.5 cm, airy, pale green. Flowers white to yellowish green to reddish to brownish green. Staminate flowers ca. 1 mm diam.; bracts ovate to triangular, 1.7-2 X 1.8 mm, at sometimes with small bracteoles or extrafloral nectaries, margin with raised glands; pedicel ca. 0.3-0.8 mm; calyx 3-lobed, lobes easily detaching, ca. 1 mm high; stamens 4, androphore 2-0.4 mm high, filaments ca. 0.7 mm, sulcate, anthers ca. 0.3 .9 mm, thecae divergent; pistillode absent. Pistillate flowers with bracts ovate to triangular, ca. 5 X 2.5 mm, margin with raised glands; bracteoles similar to bracts, ca. 3 X 2 mm; sepals (6 to)10, free, ovate, 3-3.3 X 1.2-1.3 mm, enlarged in fruit up to ca. 3 X 1.5 cm, purple, margin with raised glands; ovary 3-locular, style 1- J mm, stigmas 2.7-3 mm . deeply bifid, apices multifid, yellow, fanlike, individual stigmas not visible. Fruits regmata, 1.3-2 X 1.1-1.3 cm, green- ish to brownish; columella ca. 9 mm. Seeds obovoid, 8-10 X 8-9 Xx 7-7.5 mm Distribution, habitat, and Phenology. | Koilodepas pectinatum is seemingly rare in the Malay Peninsula (one specimen: Stone & Sidek 12616) and mainly “Volume 97, Number 2 2010 van Welzen Revision of Koilodepas endemic in Borneo (Sabah, northeast Kalimantan), where it is present in primary lowland dipterocarp forest, secondary forest, logged-over forest, open areas along logging roads, and along rivers at altitudes between 50 and 850 m; occasionally it is found on limestone. The species flowers in March, April, June through October, and December and fruits in February, March, and July through December. Discussion. Of the species in the genus Koilode- pas, K. pectinatum is the easiest to recognize because of the pectinate stipules. Other species have stipules with teeth, but these teeth point upward; in K. pectinatum the teeth are patent, perpendicular to the main axis of the stipule, and often possess smaller, also patent teeth. Additional specimens examined. INDONESIA. Kali- mantan Tengah: Katin km Upper ca WNW of Tumbang Samba, ag 1715'S, 112740 E, J. P. Mogea 4314 deba imur: Sepaku, 4 (L). Tel, pS d l, aes 117°E, eec ez Arifin A432 T 7 (D: G unung - Buntung, 1950'N, E o Geesink 9333 (L). MALAYSIA. Kelantan: Gua n pe & M. Sidek 12616 (L). Sabah: Toni] Ulu Su in iu Reserve, abawan, ogg Kalabakan, Hia F. Eee s >. SAN “017: 753 D: em Hiap logged Tembuku, F. Krispinus & Sumbing SAN 91 770 ( w Lahad spa Danum Valley, Coupe 1991, J. & Donggoj gop SAN 133305 (L); Lamag, Rail 689 ( Sungai al. SAN 116822 [5 Beluran, Sungai Melinau, A. Rahim et al. SAN 99807 (L); Sandakan, Ullu Sigin et al. SAN 100273 (L); Sandakan, , Sigin et al. SAN 107195 (L); Ted Kampung 29277 (L (L); RÀ Forest Reserve, D. = ansus SAN 67476 (L); T. Bukit Tinker: Karam D. Sundaling et al. 6 (Tong e EXCLUDED SPECIES vue hosei Merr., Philipp. J. Sci. 11: 66. 1916, as “Coelodepas.” TYPE: [Malaysia Borneo:] Sarawak, Baram fus: Entoyut River, 13 Nov. 1894, C. Hose 465 (holotype. K not seen; isotype, L!). [= Claoxylon hosei Per) Airy Shaw]. Airy Shaw (1960: 391) already noted that the type specimen of Coelodepas hosei is a pistillate specimen ion genus Claoxylon A. Juss. vessel the two genera can easily be separated. The dried leaves of are smooth, while those of Claoxylon generally feel. rough. The roughness is caused by — "e that protrude — ceram yi are absent in Koilodepas: Literature Cited Airy Shaw, H. K. 1960. Notes on Malaysian Euphorbiaceae. 14: 353-396. Bull., A Ser. 8: 1-243. — T 1981. The Euphorbiaceae of Sumatra. Kew Bull. 36: Wacker. C A. 1936. Verklarend woordenboek der we- O namen van de in N en Neder- h-Indié in het wild groeiende en in tuinen en parken an varens en planten. N.V.P. Noordhoff, roningen. & R. C. Bakhuizen van den Brink f. 1963. Flora of Java 1. N.V , Groningen. Blume, C. L. 1856. Museum Botanicum Lugduno-Batavum 2. E. J. Brill, Leiden. TA On certain 75" Bot. France 72: 48-470. Hasskarl, J. K. 1855. Brief van den Heer Hasskarl aan den sec der Natuurkundige A Afdeeling van de Konink- like Akademie van Wet te Amsterdam. V. Meded. Afd. Natuurk. Kon. Akad. Wetensch. 4: ae 856. Brief van den H e e secretaris ll abad ASdecting van de lyke Akademie van Weternschappen. Bot. Zeitung esa 14: 801—803. ——. 1857. Genera aliquot nova horti botanici bogor- iensis. Flora 14: 529—535. — — —, 1858. Hortus Bogoriensis Descriptus 1. F. Günst, Amsterdam. : Hooker, J. D. 1887. The Flora of British India 5. L. Reeve & Co., London. pres 2001. IUCN Red List Categories -— c rm 1. Prepared by the IUCN "^ iv. IUCN. c Switzerland, and Cambridge, United Kabouw, P. P. C. van Welzen, P. Baas & B. J. van Heuven. crystals in Claoxylon (Euphorbiaceae) and with notes on leaf anatomy. Bot. orth Borneo Plant , 125 Annals of the Missouri Botanical Garden McNeill, J., F. R. Barrie, H. M. Burdet, V. Demoulin, D. L. Hawksworth, K. Marhold, D. H. Nicolson, J. Pra: E ` Skog, J. H. Wiersema & N. J. Turland ella. ernational anical Nomenclature pea ienna Code). Regnum Veg Miquel, F. A. W. 1859. Flora I b ine em 1(2). C. G. van der Post, Amsterd Pax, K. & P. Hoffmann. 1914. Euphorbiaceae—Acalypheae— Mercurialinae. In A. abe (edito D Das Pflanzenreich IV, 147, vii. Wilhelm Engelmann, Berlin Radcliffe-Smith, A. 2001. Genera Euphorbiacearum. Royal Botanic Gardens, Kew, Richmond. Webster, G. L. 1994. Synopsis of the genera and supragene- ric taxa of Euphorbiaceae. Ann. Missouri Bot. Gard. 81: 33-144. Wurdack, K. J. P. Hoffmann & M. W. Chase. 2005. agad phylogenetic analysis of uniovulate Euphorbia- T A et sensu stricto) using ne rbcL and trnL-F DNA sequences. Amer. J. Bot 1397— ORIGIN, DIVERSIFICATION, AND Steven J. Wagstaff? mid Dawson,’ CLASSIFICATION OF THE Stephanus Venter,’ Jéréme Munzinger,' AUSTRALASIAN GENUS Pa tsa Dory Sane nd ina L. Lemson? DRACOPHYLLUM (RICHEEAE, ERICACEAE)! ABSTRACT The genus Dracophyllum Labill. (Ericaceae ) ha ted distribution in Australasia, but hes th test level of species richness and morphological veri d New d We investigated evolutionary processes that contribute to this sp ia in Pies e chien by c compari sequences from members of f Dracophyllum, its close its close relatives Richea Labill. Ericaceae. We ah e = = for the chloroplast-encoded genes matK and rbcL. Parsimony, Bayesian, and maximum likelih y The results were largely congruent and, when analyzed in — provided greater resolution. In - eyes, tribe Richeese formed a monophyletic group that diverged during the Eocene Early Miocene (at least 16.5 Ma) ae resulted in two disjunct lineages. This date nih roughly to the onset of aridificati ste! Caledonia, and New Zealand. The relationships of the Tasmanian endemic, D. milliganii Hook. f., remain an enigma. It was ambiguously placed as sister to Sphenotoma or to the Dracophyllum-Richea clade. We recovered two disti nct lineages, traditi ized as Richea sect. Cystanthe (R. Br.) Benth. and Richea sect ted within Dracophyllum. The Lord Howe Island endemic, D. Sitzgeraldii F. Moell., oom as sister >... um Australian Pe = Y Our evidence suggests that the New at 1 n Tos M: + p. riy DH S I ON E y a :3 T ^" > Bal iu island hipel l ly within the ree to six million years. This radiation accompanied f the N and episodes « p during the Pleistocene. Because S is e and Richea is e: the taxonomic circumscription of these genera requires revision. i rm, Australia, biogeography, classification, diversification, Dracophyllum, : . angi Epacridaceae, epacrids, Ericaceae, island floras, Lord Howe nb matK, molecular clock, molecular ATT molecular sequence data, molecular systematics, New Cal phylogeny, plant evolution, rbcL, Richea speciation, species richness, Sphenotoma, Tasmania A A —— hence are often considered to be hot spots of biodiversity (Myers et al., 2000; Emerson, to a combination of hic isolation, ination geograp 2002; Leigh et al, 2007). Darwin 0859 diverse climate, and vari opography, oceanic islands host some of the world's unique floras and Warne, ‘This research was supported in by a National Geographic Society's Committee for Research and Exploration grant 7774-05 to S.J.W. and by the N New MR Foundation for Research, Science and Technology through the Defining sod Zealand's Land Biota Outcome Based Inv estment (O BD. The authors thank many individuals f for their — qes ihi, including those from Australia: Jay giar, Ray Moore, Michelle Issen, me a and Brendon Neilly (Canberra, N New: South Wales); lan Histo and T, Andrew Perkins (Queensland); Muhammad Phil Sack rd "py New Zealan s ee ia ad hyllum from the Chatham, Three ior and subantarctic » Earli dans of LP Dt n eem the insightful comments of Greg Jordan, Daphne Lee r, Thomas Buckley, Walt Judd, Kathy Kron, and Ulf Swensen. p Alen Hei L kos, Beso : arch, PO. Box 40, Lincoln 7640, New Zealand. Author for correspondence: B on U : ical bie qued Consultant, P.0. Box 63, Trinity Beach, Queensland. 4879, Queensl e ra s "s , IRD, UMN A AMAP, Laboratoire de Botanique et dÉenlogie Végétale Appliquées, Herbarium NOU, F- IRD, UMR AMAP, Mompelier F: y Cai P.0. Box 6811, Cairns 4870, Australia. ° Australian T Tropical Herbarium, James Cook ae Cairns Campus, a i iversi ia, Pri Hobart, Tasmania 7001, Australia. School of Plant Science, sees d Tasmania, Pia Bag 55, m ETUR Usta 100 las nae » Western Australia 6027, Australia. .. doi: 10.3417/2008130 Ann. Missourt Bot. GARD. 97: 235-258. PUBLISHED ON 9 JULY 2010. Annals of the Missouri Botanical Garden observed that a high proportion of the species on islands were endemics, and some of the groups that had colonized isolated islands had diversified in mainland settings. He proposed that large remote islands allowed more ory evolutionary innova- tion, and th ection was more severe. a factors, such as e: age of these island archipelagos, their geographic area, and topographic diversity, would have also contributed to promote diversification. MacArthur and Wilson (1967) t species diversity on islands reflects a delicate interaction between immigration, speciation, and extinction. Here, we reconstruct phylogenetic patterns and use this as a work to ume evolutionary processes that contribute to a disparity i species richness between continental and island species of Dracophyllum Labill. (Ericaceae). The genus Dracophyllum reaches its greatest level of species richness and morphological diversity in the island archipelagos of New Zealand and to a lesser extent in New Caledonia, but has close relatives on mainland Australia and Tasmania (Oliver, 1929, 1952; Venter, 2008) (Fig. 1). About 51 species of Dracophyllum are currently recognized, and these vary from low-growing cushion plants to trees up to 14 m tall (Fig. 2A-H). They are characteristic shrubs of upland forests and heathlands in mainland — (e.g. Powell, 1992; Brown & Streiber, 999: Streiber et al., 1999), Tasmania (e. E^ Rodway, — Curtis, 1963; Buchanan et al., , Lo Howe Island (Oliver, 1917), New Cilada (Virot, 1975; Venter, 2004), and New Zealand (Allan, 1961; Venter, 2002) and are commonly known as drago leaf or grass tree because of their distinctive spiky growth form. Three subgenera of Dracophyllum were recognized by Oliver (1929, 1952) (Fig. 2A-H). Twenty-nine species have been recognized in Dracophyllum subg. Oreothamnus (F. Muell.) W. R. B. Oliv. (Fig. 2F-H); all are endemic to New Zealand with the exception of D. minimum F. Muell. of Tasmania (Fig. 2H). About 21 species are placed in Dracophyllum subg. Dracophyllum (Fig. 2A-D); of these, seven endemic to New Zealand, eight to New Caledonia, four to mainland Australia, one to Tasmania, and one to Lord Howe Island. A third subgenus, Cordophyllum W. R. B. Oliv., comprises a single species, D. involucratum Brongn. & Gris, which is endemic to New Caledonia (Fig. 2E). Systematists have long recognized a close relation- ship between Dracophyllum and two morphologically AR Australian genera, Richea Labill. and Sphe- ma R. Br. ex Sweet, and, in recognition of this ins la place these three genera in the Australasian tribe Richeeae. The genus Richea while Sphenotoma (Fig. 2N—P) includes six described pecies that are restricted to Western Australia (Powell et al., 1996, 1997; Paczkowska & Chapman, 2000). Unique morphological (Powell et al., 1996) and molecular traits (Crayn & Quinn, 2000; Kron et al., 2002) shared by these three genera indicate that they once shared a co Dn mmon ancestor whose descendants form a single lineage. While tribe Richeeae forms a well-defined monophyletic group (Powell et al., 1996; Crayn & Quinn, 2000; Kron et al., 2002), the phylogenetic relationships among Dracophyllum, Ri- chea, and Sphenotoma are less clear due to the sparse sampling in previous studies. ian epacrids were formerly placed in the family Epacridaceae. However, recent phylogenetic studies (Powell et al., 1996; Stace et al., 1997; Crayn & Quinn, 2000; Kron et al, 2002) revealed that the epacrids form a well-supported monophyletic group nested within the Ericaceae. As a consequence, they have all been transferred to the family Ericaceae, and 4 LE ° ] g... + LE ster the Styphelioideae Sweet. The Styphelioideae include about 35 genera and 420 species found throughout the a ni : | ade d abundant in southwestern and southeastern regions of mainland Australia and Tasmania. Outliers extend the range to Tierra del Fuego, Argentina (Lebetanthus Endl.), Hawaii (Styphelia Sm. s.l.), and Southeast Asia si gr R. Br.) (Kron et al., 2002). aceae have an ancient evolutionary history (Collinson & Crane, 1978; Nixon & Crepet, 1993; Jordan & Hill, 1996; Zetter & Hesse, 1996; Jordan et al., 2007, 2010). Remarkably well-preserved fossil- ized flowers related to the extant genus Enkianthus sss, are ees am North American deposits y years ago Mal and these exhibit pata dal vit specialized insect pollination (Nixon & Crepet, 1993). Fossil seeds and pollen resembling those of extant species of Rhododendron L. are described from Early Tertiary deposits in Europe (Collinson & Crane, 1978; Zetter & Hesse, 1996). The appearance of two pollen types in the epacrids suggests that the group had diversified by the mid-Eocene, at which time fossil pollen is observed in both southeastern & Hill, 1996; Jordan et al., 2007). fragments of Styphelioideae, m fragments attributed to Richeeae, rom Early Oligocene sediments in Ea which provides additional evidence for a mid-Tertiary s of the family (Jordan & Hill, 1996). The distinc Volume 97, Number 2 Wagstaff et al. 2010 Origin of Dracophyllum (Ericaceae) B Dracophyllum Richea Sphenotoma 50°S AUCKLAND Is. CAMPBELL Is. Figure 1. Extant distribution of tribe Richeeae. As presently circumscribed, Dracophyllum subg. Dracophyllum (21 2 E in New ' Zealand, New Caledonia, and Australia a a Tasmania and Lord Howe Island); a of Tasmania); Dracophyllum subg. pes sp., D. verticillata) i is endemic to New Caledonia; Richea (11 i is restricted to southeastern Australia (including ); Tasmania Sphenotoma (six spp.) is restricted to southern Western pollen tetrads characteristic of Richea procera (F. in tribe Richeeae by examining the DNA — Muell) F. Muell. and R. sprengelioides (R. Br.) F. data in conjunction with evidence from the fossi e koem in Lar Piem dope Jordan Q ome Ma Gà paihua o e questions: 1996). Small-leaved sclerophyllous ericads, similar to many of the fossils, ae Gud n L Ë the genus Dracophyllum monophyletic, and how à wide range of habitats including cool temperate is it related to Richea and — S o rainforest, dry woodlands, heathlands, and alpine 2. a the current classification reflect og environments, so it is difficult to trace the diversifi- í = did these lineages originate and when did cation of the grou p based on fossil evidence alone. a : The ditis history of Dracophyllum undoubt- ey diverge: i U edly reflects Tieuiaico: dispenal, adaptive radiation, 4. Are the extant species of Dracophyllum ancient > the th of pt unra evolutionary history of Dracophyllum and its relatives Annals of the Missouri Botanical Garden Morphological variation in Dracophyllum, Richea, me Sphenotoma (tribe Richeeae). —A. Dracophyllum — Is land. It is quite common near the summit of Mt. Lidgbird i Mt. Gower where it ~ Cl f th Pied is associated with Cyathea sp. —B. Habit of D. ic ose-up of the flowers of D. ma. poa bg. Diver) Nea C aedon - Close-up of the vins of D. ouaiemense (subg. Dracophyllum), New Caledonia. —E. Infructescence of D. involucratum e 2. fusgealdi is endemic to Lord “Volume 97, Number 2 2010 Wagstaff et al. Origin of Dracophyllum (Ericaceae) recent founder populations that radiated following long-distance dispersal, as has been observed in many other New Zealand taxa? _ 5. What are the underlying reasons for differences in species richness between continental Australia, Tasmania, Lord Howe Island, New Caledonia, and New Zealand? METHODS STUDY GROUP During the 2005 and 2006 field seasons, we conducted four collecting expeditions and obtained material of Dracophyllum, Richea, and Sphenotoma from throughout their range. Further material was obtained from other collectors and herbarium speci- mens. The study group included 78 DNA samples that represented the range of morphological variation and the majority of species within tribe Richeeae (Dracophyllum, 36/51 spp.; Richea, 10/1l spp. Sphenotoma, four/six spp.). Twenty-eight outgroups were selected to provide a diverse representation of Australasian epacrids, as well as more distant members of the Ericaceae. We sequenced Cosmelia rubra R. Br. and Sprengelia incarnata Sm. Sequences for the remainder of the outgroups were obtained from GenBank (). The study group is listed in Appendix 1, along with collection details, herbarium voucher information, and k accession numbers. The complete data sets are available on request from the first author and were deposited in TreeBASE (; accession number = $2437, matrix accession numbers = M4629 to M4631). DNA EXTRACTION, AMPLIFICATION, AND SEQUENCING Total DNA was extracted from fresh leaves, leaves dried using silica gel, or from herbarium specimens, dung a Qiagen DNeasy extraction kit (Qiagen Pty Ltd, - Clifton Hill, Victoria, Australia) and following the manufacturer's recommended protocols. Most extrac- lions were performed at Landcare Research, Lincoln, New Zealand, although a few DNA samples were Prepared at the National Herbarium of New South Wales, and aliquots were sent to Lincoln for subse- quent amplification and sequencing. These amplifica- tion and sequencing techniques generally followed L re y 14. (2000) AE. A E (9009 amplified by polymerase chain reaction (PCR). These gene regions were chosen to provide informative data 1: ff, L. ill 1 vh x TL LE T dad a relatively slow rate, which allows comparisons of more distantly related taxa at higher taxonomic levels, l th tK e l idly than rbcL and is more suitable for comparisons within and among related genera. Standard rbcL primers (Olm- stead et al., 1992) were used as listed in Table 1; 1351R was sometimes also used with difficult material. The majority of the matK primers (Table 1) were designed specifically for this project. One primer, which we labeled Aus50F, was designed (by D.M.C.) for earlier projects in the Eri (Cherry et al., 2001; Quinn et al., 2003). The selection of matK primers that we developed for tribe Richeeae (Table 1) gave us better results than some of the others that we trialed (those reported by previous workers as successful for epacrids). Following amplification, the excess primers and unincorporated nucleotides were removed from the PCR products using a shrimp alkaline phosphatase and exonuclease (SAP/EXO) enzyme digest. The purified DNA samples were labeled with fluorescent dyes (BigDye Chemistry, Applied Biosystems, Foster City, California, U.S.A.) and then sequenced at the Waikato and Massey universities’ DNA sequencing facilities. In all instances, both the forward and reverse DNA strands were sequenced. PHYLOGENETIC ANALYSES The sequences were initially aligned using Clus- talX (Thompson et al., 1997) and gaps were inserted in the data matrix. The resulting alignments were visually inspected and minor changes were made manually to ensure positional homology phylogenetic analyses. The aligned data sets were subjected to phylogenetic analysis using parsimony, Bayesian inference, and maximum likelihood as a M M ue cuo — (subg. flowers Habit of Richea pandanifolia (sect. Dracophylloides), Tasmania. —J. L i Tasmania. —L. Cl of the flowers of R. acerosa (sect. Cystanthe), Tasmania. . Inflorescences of Sphenotoma Dracoph Cordophyllum), New Caledonia. —F. Habit of D. recurvum (subg Oreothamnus ers of D. longifolium (subg. and. —H. Habit of D. minimum (subg. ), New Zealand. —G. Close-up of the ), Tasmania. —1. tescence of R. pandanifolia (sect. Dracophylloides). of the flowers of R. victoriana (sect. ia. —N. Habit of sp., Stirling Range. —P. Close-up of 240 Annals of th Missouri Botanical Garden Table 1. PCR and sequencing primers used for Dracophyllum and related genera. Primers Bases Reference rbcL Olmstead et al. (1992) 5 GGC CGT CGA CAT GTC ACC ACA AAC AGA RAC TAA AGC 346F ATA TTT ACT TCC ATT GTG GGT AAC GTA TTT 895F GCA GTT ATT GAT AGA CAG AAA AAT CAT GGT 1204F TTT GGT GGA GGA ACT TTA GGA CAC CCT TGG GG 346R AAA TAC GTT ACC CAC AAT GGA AGT AAA TAT 895R ACC ATG ATT CTT CTG TCT ATC AAT AAC TGC 1351R TTC ACA AGC TGC GGC TAG TTC AGG ACT CCA 3 CTC GGA GCT CCT TTA GTA AAA GAT TGG GCC GAG matK Cherry et al. (2001), Quinn et al. (2003) Aus50F TAG AAC TAG ATA GAT CTC AGC DracMatK1 ATG GAG GAA TTC AAA AGA TAT This paper 496F ACT CTT CGC TAC TGG GTA AAA This paper 888F TGA TGA ATA AAT GGA AAT ATT This paper 496R TIT TAC CCA GTA GCG AAG AGT This paper 888R AAT ATT TCC ATT TAT TCA TCA This paper 2R AAC TAG TCG GAT GGA GTA G This paper optimality criteria (Huelsenbeck & Ronquist, 2001; Swofford, 2002; Ronquist & Huelsenbeck, 2003 parsimony analysis was conducted using PAUP* with tree bisection-reconnection (TBR) branch-swapping, MULPARS, and random addition (insertions or deletions) were coded separately as Pei characters and included in the parsimony, but the maximum likelihood and Bayesian analyses. Following the method of Simmons and Ochoterena (2000), gaps in the same position were treated as homologous binary characters. Gaps that differed in length, sequence, or position were treated as different characters. We assessed the amount of phylogenetic signal in the data by generating one million random trees and calculating the gl statistic (Hillis, 1991). Congruence of the data matrices was assessed by the incongruence length difference (ILD) test of Farris et al. (1994, 1995) with 100 data partition replicates. In the event that the phylogenetic relationships recov- ses did not correspond to the current classification, we used the topological constrain by bootstrap analyses (Felsenstein, 1985), with 1000 replications excluding uninformative sites: starting trees were obtai by random addition with one replication for each bootst TREE limit of 1000. Clades with > support (BS) or > 95% posterior probability (PP) were considered well support The most appropriate maximum likelihood model and ae cse m the m a and m the Akaike Information Cia (AIC) Inference Criterion (BIC) with model a & Buckley, 2004). These approaches are implemented in Modeltest version 3.06 (Posada & Crandall, 1998). and Baycetist eragin DIVERGENCE TIME ESTIMATES The likelihood ratio (LR) test (test statistic — —2 log LR, where LR is the difference between the unconstrained and the —In likelihood value con- strained by a molecular clock, distributed as the X? distribution, with n — 2 df, and n = the number of taxa) was used to determine whether the data satisfied the assumptions of a molecular clock (Felsenstein, 1988). In the absence of a molecular clock, we used a penalized likelihood with the truncated Newton algorithm to accommodate rate a across lineages (Sanderson, 1997, 2002a). This procedure is implemented in the program r8s allen 2002b) and uses a likelihood model combined with a smoothing parameter estimated by cross-validation to estimate divergence times. We calculated bootstrap confidence limits associ- ated with the divergence dates using a 2 bootstrapping 2003 bootstrap search, and 100 rooted bootstrap trees with maximum likelihood branch lengths were saved using Volume 97, Number 2 2010 Wagstaf 241 agstaff et al. Origin of Dracophyllum (Ericaceae) the ALNEXUS format (without a translation table). This saves trees with branch lengths and taxon labels as an integral part of the tree description. We then used the profile command to summarize confidence intervals to the divergence estimates at designated — . modes in the maximum likelihood tree. A fossil-based cross-validation procedure was used to assess the magnitude of the violations to minimum and maximum age constraints (Sanderson, 2003). We used four calibration points that were based on the fossil record and geological events (e.g., the formation of Lord Howe Island). We placed a fixed age of 90 Ma at the node separating Enkianthus from all other Ericaceae. A minimum age constraint of 40.5 Ma was placed on the node separating Rhododendron and Cassiope D. Don, and a minimum age constraint of 37.8 Ma was placed on the node separating the Styphelioideae from all other Ericaceae. Finally, a maximum age constraint of 7.5 Ma was placed on the node separating the Lord Howe endemic Dracophyl- lum füzgeraldii F. Muell. from the eastern Australian species D. oceanicum E. A. Br. & N. Streiber. This maximum age constraint corresponds to the emer- gence of Lord Howe Island around 7.5 Ma, while the minimum age constraints were based on first appear- ances in the fossil record. The cross-validation approach initially removes each of the minimum or maximum age constraints and then completes a full estimation of divergence times and rates across the tree. If the estimated age is younger than a minimum age or older than a maximum age constraint, then the magnitude of the violation is determined and a running total of these is recorded across the tree. The analysis is repeated across a range of smoothing values using the penalized likelihood method. Two kinds of errors are reported, a fractional value node Per constrained node, and a raw value in terms of absolute time (Sanderson, 2003). We conducted two independent Markov chain Monte Carlo (MCMC) searches using BEAST version 1.4.8 (Yang & Rannala, 1997; Rambaut, 2006-2008; Drum- mond & Rambaut, 2007; Rambaut & Drummond, 2007) with a relaxed uncorrelated log-normal molecular clock model with the AIC settings as priors. The tree prior was set to a Yule speciation process with log-normal than 18s. We set log-normal priors of 90.0 with 95% confidence intervals of 97.7 Ma and 82.9 Ma for the most recent common ancestor (MRCA) of Enkianthus; 40.4 (43.9-37.2 Ma) for the MRCA of 37.7 (40.9-34.7 Ma) for the MRCA of subfamily Styphelioideae; and 7.5 (8.1-6.9 Ma) for the MRCA of —— Dracophyllum ftzgeraldii. The log files were examined ? + using Tracer version 1.4 to optimize priors and to assess effective sample sizes. The Tracer log files are available upon request from the first author. LogCom- biner and TreeAnnotator & Rambaut, 2007) were used to combine and summarize the information in the tree output files; a summary tree with 95% highest posterior density (HPD) confidence using FigTree (Rambaut, 2006-2008; Damad È Rambaut, 2007; Rambaut & Drummond, 2007). LINEAGE THROUGH TIME PLOT We used GENIE version 3.0 (Pybus & Rambaut, 2002a, b) to construct a lineage through time plot to study diversification rates. Under the simplest model (constant speciation rate), the probability of a speciation event occurring at a given time is constant both over time and among species, and a straight line with a slope equal to the per lineage diversification rate is expected (Barraclough & Nee, 2001). However, several evolutionary processes can cause departures from the expectations of a constant diversification rate. An increase in the slope could reflect an i in the net diversification rate (speciation minus the extinction rate), whereas a slowdown in the diversi- fication rate, a flattening of the slope, can be by a decrease in the speciation rate or an increase in the extinction rate. Sampling artifacts can also influence the pattern that is observed. Incomplete sampling tends to underestimate the number of nodes toward the present, which gives the illusion of a slowdown in the diversification rate (Barrac & Nee, 2001). The aligned rbcL data set included 1402 characters (Table 2). Of these, 1042 characters were constant, 188 variable characters were parsimony uninforma- and 172 were informative. A parsimony analysis i [cl] = 0.513 [excluding uninfor- J, retention index [RI] = 0.755). A The ali matK characters (Table 2). Ten indels were inferred, and gaps were created to maintain positional homology in the matK data set. These were always in multiples of three nucleotides and varied in length from six to 12 nucleotides. The gaps were positioned so as not to disrupt the reading frame of the gene. Of the 1533 sequence and gap characters, 840 were constant, 385 variable characters were parsimony uninformative, and 308 were informative. The relationships inferred 242 Annals of the Missouri Botanical Garden Table 2. Summary statistics for the rbcl, and matK data partitions. Uninformative characters were excluded from the consistency index calculation. The gl statistic was calculated from one million randomly generated trees using PAUP* Data partition Total characters Informative characters MPTs Tree length CI RI gl ILD test rbcL 1402 172 11177 700 0.513 0.755 -0.618 — matK 1533 308 432 1452 0526 0.772 .502 — Combined 2935 557 36 2166 0512... 0 5 05372 G.HI CI, consistency index; ILD, incongruence length difference; MPTs, maximum parsimony trees; RI, retention index. by the matK sequences were more resolved than the D. townsonii Cheeseman, and D. traversii Hook. f.) rbcL results. The parsimony analysis recovered 432 formed a second MMC clade (clade B) aih a trees in a single island of 1452 steps (CI = 0.526 96% BS value. The of Dracophyll nns uninformative characters], RI = 0.772). from New Caledonia (clade C) s Dracophyl- The rbcL and matK strict consensus trees are com- lum and subgenus Cordophyllum) were at best weakly pared in Figure 3. Significant g] values (—0.618 and supported (53% BS). However, two subclades, one —0.502, respectively; P = 0.01) indicated that the comprising D. alticola Däniker, D. balansae Virot, D. random distribution of tree lengths was significantly — cosmelioides Pancher ex Brongn. & Gris, D. mac- left skewed, which suggested the rbcL and matK data — keeanum S. Venter, and D. ramosum Pancher ex sets were converging on a small subset of the possible Brongn. & Gris (88% BS), and a second comprising D. parsimony trees (Table 2). Furthermore, the data sets M and D. verticillatum Labill. (91% BS), were congruent (ILD P = 0.11), and so were con- were supported. Richea sect. Cystanthe (R. Br.) Benth. verging on a subset of trees with a similar topology (clade D) formed a fourth well-supported clade (100% (Fig. 3). BS) in the E analysis, but emerged in a Because of the lack of conflict, we combined the different part of the tree from the members of Richea data sets and conducted parsimony, maximum sect. me Benth. (clade F). Three Austra- likelihood, and Bayesian analyses to assess the lian members of subgenus Dracophyllum, D. oceani- robustness of our results to the different assumptions cum, D. secundum R. Br., and D. macranthum E. A associated with these approaches to phylogenetic " & N. Streiber, mile a fifth clade (clade E) inference. However, the phylogenetic position of three (100%), with the Lord Howe Island endemic, D. taxa seemed anomalous and required confirmation. —fitzgeraldii, emer, rging as sister, but with weak BS e sequenced a T" accession of Dracophyllum — (Fig. 4). A sixth clade, Richea sect. Dracophylloides milliganii Hook. f, D. minimum, and D. strictum (clade F), was well supported with a 96% BS value Hook. f. to dnd for possible misidentification, with two subclades within Richea sect. Dracophyl- incorrect labeling, or contamination, and the new oides also supported. Richea alpina Menadue, R. sequences obtained for each taxon matched the continentis B. L. Burtt, R. pandanifolia Hook. f., and original data. R. scoparia Hook. f. received 99% BS, and R. gunnii The combined rbcL, matK, and gap data set Hook. f. and R. victoriana Menadue received 100% included 2935 total characters. Of these, 1882 BS. The Tasmanian endemic Dracophyllum minimum characters were constant, 496 variable characters was also included in clade F, but its relationships to were parsimony uninformative, and 557 were infor- the two subclades of Richea sect. Dracophylloides mative. The combined parsimony analysis provided were not resolved. greater resolution and support for relationships. A Dracophyllum sayeri F. Muell. emerged as sister to heuristic search of the combined data recovered 36 a large clade (100% BS) composed of most species of trees in two islands of 2166 steps (CI = 0.512 Dracophyllum (except D. milliganii) and all of the [excluding uninformative characters], RI = 0.775); a species of Richea, together forming clade G (100% strict consensus tree is shown in Figure BS) (Fig. 4). Clade G is united by a unique 6 bp We identified 10 clades that were wasikunaq bythe duplication in their matK sequences at nucleotide mbined data set labeled clades A—J in Figure 4. positions 543—548. This duplication is not present in cake of Dracophyllum subg. Oreothamnus (with — D. milliganii, Sphenotoma, or any of the other the exception of D. minimum) was supported (86% members of the Ericaceae in our survey. The sister with D. strictum (subgenus Dracophyllum) to this large clade is not clear; D. milliganii, the four emerging as sister (100% BS); together, these taxa — species of Sphenotoma (clade H) (100% BS), and the comprise clade A. The five New Zealand species of Dracophyllum-Richea clade (clade G) form a trichot- Dracophyllum subg. Dracophyllum (D. fiordense W. R. — omy. These three clades comprise tribe Richeeae and B. Oliv., D. menziesii Hook. f., D. latifolium A. Cunn., Pid a monophyletic group (clade I) with 95% BS. f j = : The Richeeae are hi $ YA - Volume 97, Number 2 2010 Wagstaff et al. 243 Origin of Dracophyllum (Ericaceae) rbcL Figure 3. Comparison strict consensus trees of Australasian Ericaceae relationships inferred by the matK sequences were more resolv ghlighted in bold, and bootstrap values > 50% are presented above the branches. matK cerinthoides 100 Arbutus canariensis Pyrola rotundifolia Enkianthus campanulatus from parsimony analysis of rbcL and matK ed than the rbcL sequences. Members of tribe 244 Annals of the Missouri Botanical Garden Oreothamnus - Dracophyllum | Dracophyllum Dracophyllum - Cordophyllum ]] Dracophyllum i Cystanthe j Dracophyllum Tribe Richeeae Dracophylloides - Oreothamnus l Dracophyllum Figure 4. Strict consensus tree from parsimony — of the combined rbeL and matK data sets. A heuristic search of the co ombined data recovered 28 trees in two islands of 215 l steps A 0.512 [excluding uninformative characters]. RI — 0.7 T da 2). Bootstrap values 7 50% are fas peeti nted above the nches. The combined parsimony analysis provided pendent on of either rbcL or matK. Well-supported clades labeled A-J are discussed in the text. Tribe Richeese, de, bi of Dracophyllum, and sections of Richea are shown at right. Tribe Richeeae is nested within the Southern recovered 272 trees of 2176 steps; these were 10 Hemisphere epacrids (clade J), which receive 10076 — steps longer than the maximum parsimony trees of BS in our analysis (Fig. 4). 2166 steps. However, this clade was a nested We used topological constraints to assess the within _Dracophyllum. Constraining the analysis so differences between the current classification and hat a and Dracophyllum emerged as monophy- the results inferred from the combined analysis of rbcL — letic sisters were 25 steps longer than the maximum K sequences. Enforcing a topological con- parsimony trees. Constraining the analysis so that straint so Richea formed a monophyletic group Dracophyllum and Richea were each monophyletic as Volume 97, Number 2 2010 Wagstaff et al. Origin ot Dracophyllum (Ericaceae) well as the three subgenera of Dracophyllum required an additional 51 steps. AIC and BIC selected the general time reversible model (GTR + G + I) with an assumed proportion of invariable sites = 0.3008 and a rate distribution of LAE i fl] = g gamma pp : H with a _ shape parameter — 0.8861 as the best-fit substitution model for the combined analysis of the rbcL and matK sequences. Nucleotide frequencies determined by the AIC test were set as: A = 0.3074, C = 0.1654, G = 0.1871, and T = 0.3401. These settings were used in _ the maximum likelihood and Bayesian inference "wu optimality criterion with these AIC settings resulted in a single tree (—Ln = 16709.592; shown in Fig. 5). . This tree is also largely congruent with the parsimony . . and Bayesian trees (Figs. 4, 6). There appears to be - considerable rate variation across lineages (Fig. 5), which is apparent, for example, in Oli -micrantha R. Br. and Lysinema ciliatum R. Br. with relatively long branches and Arbutus canariensis Duhamel and Cassiope mertensiana (Bong.) G. Don with comparatively short branches. Most of the branches leading to species of llum and 1 are approximately the same length (Fig. 5). which suggests the substitution rates in this part of the tree are approaching clocklike behavior. Nonetheless, the substitution rates across the entire maximum likelihood tree violated a molecular clock assumption, exhibiting significant rate heterogeneity across line- ages (LR test — 2 [16709.592-16959.605] — 500.026, df — 75, P = 0.001). Therefore, we used the penalized likelihood approach of (20022, b) to estimate substitution rates and diver- gence times in the absence of a molecular clock. Tho min; 1 : ¿amia niaced isti hun EL ind ss dd on the maximum likelihood tree (Fig. 5) were across five smoothing values to evaluate the quality of the penalized likelihood model and the parameters _ that were selected for the r8s analysis. The i and raw errors were relatively low across all five smoothing values. Only one violation of the minimum age constraint placed on the Styphelioideae was noted; the estimated age of 37.65 Ma was 0.15 Ma Younger than the fossil-based constraint of 37.80 Ma. .... However, the maximum age constraint of 7.5 Ma was nd e i e a e 100 BS trees presented as mean + SD and range) (Table 3). Th ge for th diation i tribe Richeeae was Early Miocene, about 20.6 * 2.9 Ma (range, 7.2-35.9 Ma). The New Zealand Draco- + 1.0 Ma (range, 2.6-8.8 Ma compared with 5.6 * 0.7 Ma; range, 3.9-7.0 Ma), which dates the origin of both lineages to the Late Miocene. The crown radiation occurred at i he same time in New Zealand and New Caledonia—3.0 * 1.2 Ma (range, 1.1-7.7 Ma and 3.5 + 1.1 Ma; range, 0.7-6.5 Ma), subg. Oreothamnus in 11 + 1.1 Ma (range, 0.0-7.1 Ma). Zero-length collapsed in the r8s analysis, and in M o e 54 si. e actinia ware than those derived from the Bayesian analysis. However, with one i means were still within the 95% confidence intervals of the HPD. The i stem of the New Zealand radiation, interval of the HPD of 6.9-11.2 Ma. We ran two MCMC chains, each for five million -Ln — 167500 + SD of the means, which were 0.374 and 0.511, respectively. Five thousand trees were saved during each run; 5% (250 trees) were excluded as bum-in from each, and the tree files were combined. Figure 6 shows the combined tree files with bars representing the 95% HPD intervals for the correspond to Dracophyllum subg. D. strictum) (clade A) and Dracophyllum subg. 246 Annals of the Missouri Botanical Garden Dracophyllum Dracophyllum ass Dracophyllum cosmei kann kg ei mackeeanum en involucratum Dracophyllum verticillatum Dracophyllum ouaiemense Dracophyllum thiebautii acerosa pronum Dracophyllum scopariu umo05.30 37.8 Ma REI 90.0 Ma 40.5 Ma — Vaccinium uliginosum A Enkianthus campanulatus — 0.005 substitutions/site i Figure ndi 14,0) Broche likelihood tree T Ln = - 16709.592) that i ds largely congruent with the parsimony and Bayesian trees us tir rge ing a jali d lik Li d thi gI ]. : pl Es um (S d 20029). Dracophyllum (clade B). Within subgenus Oreotham- D. patens W. R. B. Oliv., D. rosmarinifolium (G- nus (clade A) is a clade composed of D. ophioliticum Forst) R. Br. and D. acerosum Berggr., which S. Venter, D. pra Hook. f., D. kirkii Berggr., D. received 100% PP support. Relationships among the densum W. R. B D. trimorphum W. R. B. Oliv., New Zealand species of subgenus Dracophyllum Volume 97, Number 2 Wagstaff et al. 247 2010 Origin of Dracophyllum (Ericaceae) 100 d £ Figure 6. Bayesi c 0500 trees MCMC analysis. Well-supported clades labeled A uen Log-normal pri ors of 90.0 with 95% confidence intervals of 97.7 million years and 829 were ser or am 40.4 (43.9-37.2 Ma) for the MRCA of Rhododendron; 37 d 7 Ma) for the _ (8.1-6.9 Ma) for the MRCA of Dracophyllum fitzgeraldii. This iod ind Lord Hove Island around 75 Ma. "iile probability values > 95 min pare each node, and an ionary n is shown at the bottom. The bars represent resent 95% - intervals 248 Annals of the Missouri Botanical Garden Table 3. Divers cuins given as ~ a nee brnebes were pe 3 in te r8s analysis. In some of the strap t rees, was not maximum likelihood are as means with 95% confidence intervals of the HPD. d. The estimates derived from as means + SD with the range in vers sama while the Bayesian estimates are presented No. of bootstrap Node trees in r8s profile Maximum likelihood (Ma) Bayesian (Ma) Stem age for tribe Richeeae 100 33.4 + 3.5 (12.2-44.1) 34.3 (26.9-36.3) Crown radiation in tribe Richeeae 100 20.6 + 2.9 (7.2-35.9) 16.5 (8.7-21.4) Stem age of New Caledonian radiation 47 5.6 + 0.7 (3.9-7.0) 6.7 (4.0-9.7) Crown age of New Caledonian radiation 92 3.5 + 1.1 (0.7-6.5) 5.2 (2.6-7.2) Stem age of New Zealand radiation 95 6.2 + 1.0 (2.6-8.8) 7.4 (6.9-11.2) Crown age of New Zealand radiation 100 3.0 + 1.2 (1.1-7.7) 6.1 (2.3—6.3) Stem age of Dracophyllum subg. in New Zealand 100 1.1 + 1.1 (0.07.1) 1.4 (0.7-3.0) (clade B) are completely resolved by the Bayesian analysis. Dracophyllum traversii emerged as sister to a clade (96% PP) consisting of D. latifolium, townsonii, D. fiordense, and D. mendis with D. latifolium and D. townsonii (9996 PP) and D. fiordense and D. menziesii (100% PP) each sisters. The New Caledonian species of Dracophyllum (clade C) form a well-su ed clade (100% PP) with three well-supported subclades (Fig. 6). Draco- phyllum verticillatum and D. involucratum form a clade (100% PP). Da ouaiemense Virot and D. thiebautii Brongn. & Gris form a second clade (100% PP) that is sister e a clade one of D. alticola, D. cosmelioides, . D. mackee- and D. balansae dod "PP. Dracophyllm ihiebautii was previously considered as a synonym of D. verticillatum by Virot (1975), but is "n recog- nized as a distinct species. Most of the Australian species of Dracophyllum and Richea form a grade at the base of tribe Richeeae; two lineages emerge in succession as sisters to the New Caledonian species of Dracophyllum (Fig. 6). The four species of Richea sect. Cystanthe (clade D) (10096 PP) are again well supported in the Bayesian tree. Similarly, D. oceanicum, D. secundum, and D. mac- ranthum (100% PP) (clade E) and Richea sect. Dracophylloides (plus D. minimum nested within this clade) (100% PP) (clade F) are well supported by both analyses. Richea gunnii and R. victoriana form a clade (100% PP) that is sister to a clade composed of R. pandanifolia, R. scoparia, R. alpina, and R. continentis. In the Bayesian tree, Dracophyllum milliganii emerged as sister to all of the other species of Dracophyllum and Richea (clade G), but there was low PP support for this relationship. The four species of Sphenotoma in our analysis form clade H (100% PP). Within clade H, S. capitata (R. Br.) Lindl. and S. kiere Sond. Menta a e m. PD ied is Sg and S. gracilis (R. E Sweet (100% PP). P Richeeae received greater support (99% PP) in the Bayesian tree (clade I, Fig. 6) than in the parsimony tree (Fig. 4) and again was nested within the Southern Hemisphere epacrids (clade J) (100% PP). The nodes separating the 77 terminals in the r8s analysis are plotted through time in Figure 7A—C. Our sample was fairly complete within tribe Richeeae, but of the genera in subfamily Styphelioideae were only represented by single exemplars, and the relatively flat portion of the plot partly reflects this taxonomic bias (Fig. 7A). Within tribe Richeeae, we estimated that a new species lineage was form approximately every 338,000 years. However, we observed two plateaus in the lineage through time plot, which suggested a departure from this average diversification rate. The earliest punctuation was bserved among the 20 Australian members of tribe Richeeae (e.g., Sphenotoma, Richea, and five species of Dracophyllum) beginning approximately 20.6 Ma and lasting for 13.5 million years (Fig. 7B). This period was marked by a substantial slowdown in the diversification rate and/or an increase in the extinc- tion rate. À second punctuation in the diversification rate beginning around 6.5 Ma and lasting for 33 million years was noted Ë Caledonia (Fig. 7C). This occurred shortly after these island archipelagos were colonized by Dracophyllum and may reflect a slowdown in the diversification rate during establishment. Most of the net diversification in tribe Richeeae has occurred within the last two million years, as indicated by the steep slope in the lineage through time plot during this time period (Fig. 7A-C). Volume 97, Number 2 2010 Wagstaff et al. Origin of Dracophyllum (Ericaceae) DISCUSSION We provide a robust inference of the phylogenetic relationships within tribe Richeeae. Our results indi- cated that only Sphenotoma is monophyletic, whereas Dracop: if- Caledo- nia, and New Zealand partly reflect a taxonomic bias in the manner that genera within the tribe have been _ circumscribed. The disparity would not be so great if the species of Richea were lumped in Dracophyllum. This . taxonomic bias is superimposed on an evolutionary history of long-distance dispersal, diversification, and extinction. There appears to be a biogeographical basis to the patterns of diversification that we recovered. While the greatest levels of species richness and pool diversity in Dracophyllum are found in New Caledonia, the phylogenetic p is greatest in Australia. The Australian species of Dracophyllum are remnants of older lineages, and their present distributions are fragmented and disjunct. In contrast, our results suggest that the New Caledonian and New Zealand species (especially Dracophyllum subg. Oreothamnus) have recently radiated following at least two unique instances of long-distance dispersal from eastern Australia. PHYLOGENY AND CLASSIFICATION OF TRIBE RICHEEAE On its own, the analysis of rbcL does not support monophyly of tribe Richeeae (comprising Dracophyl- lum, Richea, and Sphenotoma). However, it is not in conflict with the matK results, which provide better support for the tribe (Fig. 3). The combined analyses provide stronger support and resolution within the tribe (Figs. 4-6). Our findings confirm earlier molec- ular studies with an expanded sample of the tribe (Crayn & Quinn, 2000; Kron et al., 2002). Additional morphological characters that unite the members of tribe Richeeae include the presence of a single bract that subtends the sepals, sheathing leaves that leave a distinct annular scar, leaf nodes that are tri- or multi- lacunar, and the absence of platelet waxes on the adaxial surface of the leaves (Powell et al., 1996; Crayn et al., 1998; Kron et al., 2002; Venter, 2008). Our results also suggest the current generic circum- . Sriptions do not form monophyletic groups (Fig. 4). The molecular analyses supported monophyly of - Sphenotoma (clade H, Fig. 4). The genus was originally erected by Sweet (1827), but for a time (1869) submerged it in Dracophyllum. _ ma gracilis is the type for the genus. _ Sphenotoma differs from Dracophyllum in having a narrow corolla tube, with the throat almost closed by longitudinal folds at the base of the lobes and the filaments adnate to the corolla tube (Powell et al., 1996) (Fig. 2N-P). Six species are currently recog- nized, but there are probably one to two undescribed species oe & a Of th by Oliver (1929, 1952), only the New Zealand members of subgenus Oreothamnus form a clade in our analyses (clade A, Fig. 4). Dracophyllum subg. Oreothamnus has solitary flowers or a raceme, and the subtending bracts become differentiated according to their position, with the lowermost being the most ns (Fig. 2F, 9. The type for subgenus Or- , D. minimum (Fig. 2H), is distinct from the Ne ew Zealand clade (Fig. 4), contradicting the phe- netic and cladistic morphological analyses of Venter (2008) that supported the traditional placement of D. minimum as a member of subgenus . The morphological similarities could be the product of convergence, as D. minimum (Fig. 2H) and the New Zealand cushion herbs within Dracophyllum subg. Oreothamnus (e.g., D. muscoides Hook. f.) are found in similar alpine habitats, and their distinct cushion morphology is an adaptation (by morpho rud inhabit Pollen idee may also help resolve the correct placement of D. minimum, as McGlone (1972) demonstrated that pollen morphology of the New Zealand members of Dracophyllum subg. nus differs from that of Dracophyllum subg. o phyllum, but unfortunately D. minimum was not included in his survey. Dracophyllum strictum (Dracophyllum subg. Draco- phyllum) emerges as sister to Dracophyllum subg. Oreothamnus (clade A, Fig. 4). It is | caen from the other New Zealand me eee Dracophyllum by its small, narrow E sol anthers and was instead allied by Oliver (1929, 1952) with the Australian and New Caledonian members of subgenus Dracophyllum. The adult leaves of D. strictum are (3.5)5.5-8.5 em X 6-7 mm and the juvenile leaves are 10-11 em X 11-13 mm (Oliver, 1929), approaching those those of subgenus Oreothamnus, especially the heteroblastic juvenile forms. Dracophyllum subg. Dracophyllum is the most widely distributed of the three subgenera and occurs across the full ic range of the genus. However, the distribution is fragmented. Several members of Dracophyllum subg. Dracophyllum are narrow endemics. Dracophyllum sayert emerged at the base of clade G. It is geographically isolated from the other Australian species of Dracophyllum and Richea and is restricted to a few isolated mountaintops in northeast Queensland. Dracophyllum fitzgeraldii is endemic to Lord Howe Island, and D. ouaiemense and L Hn i 250 Annals of the Missouri Botanical Garden D o 60 © o £ u- O ° OQ 40 E pa < 20 80 ME. 60 “50 - 4D ` 30 4 10 present 20 80 70 60 50 40 30 20 10 present 20 80 70 60 50 40 30 20 10 present Relative time (Ma) since root node re 7. Lineage through time plot. A. Seventy-seven lineages were plotted that corresponded to the — in our st ui ‘Gee sample was fairly capias dili tribe Richeeae, but most genera wit thin Veste —— were represented by single exemplar. The rio flat portion of the plot reflects this taxonomic bias m stem li ving rise to tribe Richeeae. —B. Plot of the Australian species of Dracophyllum, Bikes m ps toma shows a broad plateau from 20.6 Ma tha t may represent an increase in the extinction rate relative to the rate of speciation. —C. In Volume 97, Number 2 2010 Wagstaff et al. Origin of Dracophyllum (Ericaceae) D. alticola to a few isolated mountain peaks in New Caledonia. Our results suggest the subgenus is at best paraphyletic, and it is probably ehe (Fig. 4; Es representatives in clades A, B, E). Oliver (1929, 952) recognized four groups based on ex inii B of the panicle, sepals, corolla, and anther position (Fig. 2A—D). A paniculate inflorescence is y morphological character that unites the members of Dracophyllum subg. Dracophyllum, al- though it can be either terminal or lateral. The bracts can be short and broad as in D. strictum or greatly elongated as in D. milliganii and are generally deciduous. The corolla tube can be quite long with inserted stamens or short with the stamens far exserted. The New Caledonian species, Dracophyllum in- ended by small TU (Oliver, 1929, 1952), but in most other respec is quite similar to the other members of Diocigh iln subg. Dracophyllum. There is little sequence variation that distinguishes D. involucratum from the other New Caledonian species of Dracophyllum, so continued recognition as a distinet subgenus is unwarranted, and the homology of its inflorescence structure needs to be investigated in greater detail. It shares the large colorful deciduous bracts and paired bracteoles of the other members of Subgenus Dracophyllum. Its unique inflorescence structure is undoubtedly an autapomorp Both Richea lineages are well uui (clades D, F, Fig. 4) and correspond to the two sections (Richea Sect. Cystanthe and Richea sect. Dracophylloides) recognized from morphological and flavonoid charac- ters (Mueller, 1867-1868; Menadue & Crowden, 2000). Because we found Richea to be pupa o each lineage could mr be recogni a distinct genus. Indeed, proach was E taken by Robert Brown (1810) when he described Cystanthe and Richea based on their unusual cap- shaped corolla (Fig. 2L, M) but distinguished by their inflorescences. Richea sect. Cystanthe has a simple spike (Fig. 2M) and persistent bracts, whereas Richea sect. Dracophylloides has elongate spikes or com- pound panicles and deciduous bracts (Fig. 21-L). The floral characters that were nee by. Been qua " identify Richea are h evolved independently in be different lineages. To overcome the issue of polyphyly, either Draco- phyllum could be enlarged to accommodate Richea (clade G, Fig. 4) or tribe Richeeae (clade I, Fig. 4) could be as a distinct genus. While this ater dee is — the € D. gaps was nus, so it may be necessary to apply t the New Zealand clade (clade A, Fig. 4). Nonetheless, monophyletic groups restricted to New Caledonia and New Zealand as distinct genera, but this would require the circumscription of at least five new Australian genera to resolve the other issues of polyphyly in — and Richea. Unfortunately, = — sulis, so i» possible that any newly ons genus would not be monophyletic. One approach is to adopt a broad circumscription of Dracophyllum that includes Richea. If this approach is followed, tribe Richeeae would then be comprised of two well- supported lineages that have been reproductively isolated for millions of years and an infrageneric t could be used to account for some of the clin Richea) are geographically isolated and onomically distinct. The ambiguous placement of D. milligani poses a conundrum for either approach. It could be recognized as a distinct genus or included in Sphenotoma, but because of its morphological similar- ity to the other species in Dracoph subg. Dracophyllum, we would recommend tentatively in- cluding it there, at least until additional evidence suggests otherwise. The presence of sclereid thicken- ings on on the top and bottom of the cells and two ersal in the members of Draco- bracteoles (with rev phyllum subg. Dracophyllum) is a putative synapo- morphy for Sphenotoma, whereas possible synapomor- eo — Contrast the plot Sis WT Cal IN „y i 1 about 6.2 Ma that lasted for 3.8 Ma. This may repre island archipelagos. Most of the net indicated by the MD UN RU nni LE ut are laa ie Wis I through time n= (D hyll I ] d by a brief plateau beginning Richeeae rita within the last two million years as Annals of the Missouri Botanical Garden phies for Dracophyllum sJ. are leaves with a serrate margin (with reversal in D. sayeri, D. alticola, and ed E E ye E OX XT $ 2002 E ORIGIN AND DIVERSIFICATION OF THE MAJOR AUSTRALIAN LINEAGES OF TRIBE RICHEEAE Sources of error in divergence time estimation have orent received critical attention (Sanderson et al., Renner, 2005). Foremost is oba nin a rolkooi inference of phylogenetic relationships and the proper integration of fossil evidence to calibrate a molecular clock. The issue is the choice of node to which a fossil applies. Moreover, the fossil recond i is is Peal "" incomplete, The first ly a minimum age, and it can be difficult to assess their affinities to extant taxa. Basing divergence time estimates on a single calibration point can be problematic. We pplied bo n multiple fossil dates and the emergence of Lord Howe Island as calibration points and a fossil-based cross- validation procedure, but nonetheless we acknowledge there is substantial uncertainty associated with our estimates. Members of the Ericaceae appear relatively early in the fossil record documented for angiosperms. W rooted our phylogeny on the long branch leading to Enkianthus and set the minimum age of this branch at 90 Ma, which reflects the first appearance of allied fossils during the Late Cretaceous (Nixon & Crepet, 1993). The environmental conditions that existed during the early evolution of the Ericaceae were dramatically different from those of the present day (Raven & Axelrod, 1972; McLoughlin, 2001; Hill, 2004; Hopper & Gioia, 2004; Gibbs, 2006; McGlone, 2006; Ladiges & Cantrill, 2007). The southern continents were united, forming the PEYE » but began to drift apart during Crece Because " "nx n in high hides th o winter al by nearly continuous daylight during dis — summer (Hill, ; McGlone, 2006). The forest vegetation was dumis by diverse angiosperms, araucarias, and ferns. Warm temperate, moist "isa conditions prevailed as the continents continued to shift apart and migrate northward. The landmass that was to form New Zealand retained connections to New Caledonia, possibly until the end of the Eocene, and faced an almost continuous Gondwa- nan coastline consisting of South America, Antarctica, and Australia. Until the Oligocene to Early Miocene, southeastern Australia and New Zealand were clothed in diverse rainforest vegetation, resembling that It li rth Australia, New Guinea, and New Caledonia (McLoughlin, 2001; Hill, 2004; Gibbs, 2006; McGlone, 2006). The divergence estimates depicted in the Bayesian chronogram (Fig. 6) are generally older than those derived from the r8s analysis (Table 3); nonetheless, the mean estimates from both approaches fall within the confidence intervals surrounding the means. The branch leading to ndron diverged during the Early Tertiary about 45.1 Ma. Both fossilized pollen and seeds of Rhododendron are reported from this time period (Collinson & Crane, 1978; Zetter & Hesse, 1996). Our results also suggest that Southern Hemisphere quspa are nested among the Ericaceae 5 Ma, emerging as sister to subfamily E (Kron et 2). Tribes Oxyden- dreae, Lyonieae, and P Ee W are basically Northern Hemisphere groups, whereas tribes Vacci- nieae and Gaultherieae have expanded into both the Northern and Southern hemispheres. The maximum likelihood gajos estimates that we obtained were older than the m age constraints that we placed on these two oa. This is roughly when the land connections from South America to Australia via Antarctica were broken. Perhaps this ancient geolog- ical event is related to the isolation of the Southern Hemisphere oo from the predominately Northern Hemisphere vaccinioids. Diversification in os Styphelioideae (clade J, Fig. 6) was rapid, with lineages presently recog- nized as tribes diverging by the mid-Tertiary (Jordan & Hill, 1996; Jordan et al., 2007, 2010). Fossilized ericaceous pollen was present in New Zealand and Australia by the mid-Eocene. Our results suggest the members of tribe Richeeae (clade I, Fig. 6) diverged from the other epacrids at least 33.4 Ma (Table 3). This date is very close to the age of the earliest fossils of Richeeae—both pollen and macrofossils (Milden- hall, 1980; Jordan & Hill, 1996; Jordan et al., 2007, 2010)—and implies the stem lineage of tribe Richeeae had evolved diagnostic traits of the crown group virtually back to the split between tribe Richeeae and its sister, and the first appearance of the fossils closely followed the evolution of the clade. This is rather surprising given the rarity of the fossils (there are only about five leaves in all of Australia and perhaps 20 in New Zealand older than two million years) (Jordan & Hill, 1996; Jordan et al., 2007). results suggest that the major splits within tribe Richeeae evolved by the Early Miocene at least 16.5 Ma (Table 3). The Western Australian genus Sphenotoma (clade H, Fig. 6) forms a distinct evolutionary lineage, and Dracophyllum and Richea together form a e lineage (except the ambiguous placement of D. milliganii) (clade G, Fig. 6). —. Volume 97, Number 2 2010 Wagstaff et al. Origin of Dracophyllum (Ericaceae) Divergences between the Australian genera Ander- sonia R. Br., Cosmelia R. Br., and Sprengelia Sm. also occurred during the Miocene (Fig. 6). Today, Ander- sonia and Cosmelia are restricted to Waestern Australia, while Sprengelia is restricted to the eastern states including Tasmania. These disjunct lineages may have been geographically isolated by the onset of _ climatic changes that occurred during the Oligocene and progressed through the Miocene (Hill, 2004; Hopper & Gioia, 2004; Crisp et al., 2004; Crisp & Cook, 2007). The final separation of Australia from Antarctica initiated climatic changes that created the central Australian deserts. The gradual expansion of the deserts isolated the mesic high-rainfall forests of southwestern and southeastern Australia with a belt of semiarid vegetation. Increasing aridity during the Miocene saw the fragmentation of the rainforests and their replacement by drier scleromorphic and xero- morphic vegetation (Hill, 2004; Hopper & Gioia, 2004; Crisp et al., 2004; Crisp & Cook, 2007; Byrne et al., 2008). We document a substantial increase in the rate of extinction and/or a slowdown in the diversi- fication rate in Australia beginning approximately 20 Ma (Fig. 7A). DISPERSAL AND ESTABLISHMENT ON ISLAND ARCHIPELAGOS IN THE WEST PACIFIC The divergence estimates suggest that lineages of Dracophyllum independently colonized the Western Pacific archipelagos of Lord Howe Island, New Caledonia, and New Zealand. The progenitor of the Lord Howe endemic species D. fitzgeraldii likely originated in eastern Australia and dispersed to Lord Howe Island (Fig. 6). These findings are similar to those reported for Planchonella Pierre by Swenson et al. (2007). Our results suggest this lineage diverged less than 7.5 Ma, so D. fitzgeraldii must have dispersed shortly after the emergence of the island. It may have existed on th inland prior to this date, but subsequently went extinct. Lord Howe Island is the eroded remnant of a large shield volcano formed during the Late Miocene (Oliver, 1917; Paramonov, 1960; McDougall et al., 1981; McDougall & Duncan, 1988). The period of volcanic activity was relatively brief, lasting less than one million years. A line of reefs, guyots, and banks extends to approximately 1000 km north of Lord Howe Island, and these steep- sided seamounts have a volcanic origin as well. Lord Howe Island lies on the boundary of two major Physiographic features, the Lord Howe Rise and the Tasman Basin. Despite its close proximity to mainland Australia, the flora of Lord Howe Island also share close affinities with Norfolk Island, New Zealand, and .. New Caledonia (Oliver, 1917; Green, 1994). The New Zealand and New Caledonian species of Dracophyllum similarly trace their origins to eastern Australia, having diverged from eastern Australia species at least 7.4 Ma (see Table 3; Figs. 6, 7). The progenitors of these lineages most likely arrived by long-distance dispersal long after these lands had separated from Gondwana. New Caledonia and New Zealand were gradually inundated by rising sea levels Middle to Late Oligocene (Cooper & Cooper, 1995; Lee et al, 2001; Gibbs, 2006; Pelletier, 2006; Grandcolas et al., 2008); much of the extant flora and fauna must therefore have been introduced after the Late Oligocene. Nonetheless, there are a large number of ferns and conifers with a long, con- tinuous fossil record in New Zealand (Cieraad & Lee, 2006), notably the New Zealand kauri, Agathis australis (D. Don) Lindl. (Knapp et al., 2007; Lee et al., 2007), suggesting y ient lineag h survived Oligocene drowning. The recent discovery of a remarkable 20-25 Ma fossil allied to tribe Richeeae (Jordan et al., 2010) significantly predates our minimum age estimates of the extant lineages in New Zealand (Jordan et al., 2010). This fossil, Richeaphyllum waimumuensis G. J. Jord. & Bannister, exhibits anatomical synapomor- phies characteristic of Richeeae, but its affinities within the tribe remain unresolved. This finding suggests the ancestors of Dracophyllum may have been present in New Zealand prior to Oligocene drowning. We evaluated the effect on our divergence estimates of using this 20 Ma fossil as a fixed calibration point for the stem age of Dracophyllum subg. Dracophyllum in New Zealand. The two minimum age constraints were still satisfied, but the maximum age constraint of 7.5 Ma was violated in our 18s analysis. Based on this calibration point, the SEE NOW £ pn l1 JM. gab a Oreotham y "avv nus in New Zealand was 4.2 Ma, the New Zealand and New Caledonian crown dates were 12.7 and 13.2 Ma, respectively, and the New Caledonian stem age was 13.1 Ma. While these dates seem within reason, the crown age for tribe Richeeae was pushed back to 317.2 Ma, the stem age to 402.3 Ma, the epacrids to 502.62 Ma, and the split between Enkianthus and all other Ericaceae to 1331.3 Ma. This latter value predates the origin of land plants. These older values seem unrealistic and are not supported by the fossil record. It is conceivable that the ancestor of D. milliganii was more widely distributed during the i and while its descendants are still found in Australia, they are extinct in New Zealand. This extinct Dracophyllum lineage may have been later replaced by progenitors of the extant New Zealand 254 Annals of the Missouri Botanical Garden lineages. Thi h ld b t with the l , alluvi | pl ins, river terraces, d npe minimum age estimate presented here, but would involve two more recent dispersals to New Zealand and extinction of the earlier lineage. i to and from New Caledonia and New Zealand has occurred in many plant groups (Pole, 1994; Macphail, 1997; Wagstaff & Dawson, 2000; Winkworth et al., 2002; Bartish et al., 2005; Swenson el al, 2007) but Ladiges and Cantrill (2007) suggested that vicariance cannot be justifiably dis- missed in others. There is a correlation between plant distribution and wind pattems in the Southern Hemisphere, and wind has been proposed as one possible vehicle of long-distance dispersal (Muñoz et al., 2004). Dracophyllum has a capsular fruit and produces numerous small seeds within each capsule that could be dispersed by wind, birds, or water. New Caledonia and New Zealand were indepen- dently colonized by species of Dracophyllum at least 5.6 and 6.2 Ma (Table 3; Figs. 6, 7). Because of their geographic isolation, the initial island founder popu- lations were most likely small and may have consisted of only a single individual. Punctuation in the net diversification rate = 7C) may be correlated to these dispe tion, and establishment phases. However, after an hisa colonization and establish- ment phase, diversification in each archipelago was rapid and largely occurred during the Pliocene and Pleistocene some 3-6 Ma (Table 3; Figs. 6, 7). We suggest that inbreeding and strong selection in these small founding populations would have played an important role in the rapid evolution of The conspicuous contrast between levels of morpho- logical and genetic diversity may partly be a reflection of the interplay between these dynamic evolutionary processes (Winkworth et al., 2005). This disparity is particularly evident in New Zealand species of Dracophyllum subg. Oreothamnus. With 29 species, this subgenus is the most species rich in Dracophyllum and includes growth forms ranging from alpine cushion herbs to sizeable trees. However, they have virtually enr matK and rbcL sequences. D low level of species radiation has otcerred within Dracophyllum Oreothamnus. We documented a brief punctua- tion in the net diversification rate beginning about 22 Ma, followed by a rapid radiation about 1.1 Ma (ahes Fige. 5 Tk Thi —— HÍÓ€ — The uplift of the Southern Alps i in New Zealand during the Pliocene and was by cooler climates and expansion of wisi samen’ in the interior of the South Island. This was a time of severe disturbance; the onset of glaciation and erosion during the Pleistocene created a variety of new habitats such MacArthur d: Wilson (1967) stated that species diversity on islands reflects a delicate interaction between immigration, speciation, and extinction. The environmental heterogeneity and biotic diversity in oceanic islands such as New Caledonia and New Zealand may actually contribute to the processes of diversification through increased competition, preda- tion, and the evolution of symbiosis. The impressive and relatively recent species radiation that Dracophyl- has upon its arrival in these island archipelagos certainly supports Darwin’s early obser- vations, whereas the vagaries of a dramatically changing climate isolated their mainland ancestors in Australia. Extinction may have had a_ profound influence by diminishing the extant species diversity. The level of phylogenetic diversity within the Austra- lian lineages far exceeds that found in their island cousins; the present species of Sphenotoma and llum s.l. appear to be some of the remaining relics of a once more widely distributed forest flora in Australia. It remains a challenge to classify the members of tribe Richeeae in a manner that accurately conveys their complex evolutionary history. The data presented in this paper yield a chloroplast DNA (cpDNA) gene tree only. It is likely that relationships of Dracophyllum are further confounded by evolution- ary reticulation, and nuclear data might be more congruent with morphology. This hypothesis could be tested by future research using nuclear genes. Literature Cited Allan, H. H. 1961. Flora of New Zealand, Vol. 1. Government Printer, Wellington, New Zealand. Rydin € M. Killersjó. 2002. Ericales s.l.: 2. New species Alaa a Kes Srl Wo Telopea 8: 393-401. Brown, R. 1810. Prodromus Florae Novae Hollandiae et Insulae Diemen. London. Byme, M., D. K. Yemes. J. M. Kearney, J. Bowler, M. A. Williams, S. Cooper, S. C. Donnellan, J. S. Keogh, R. Leys. J. Melvill, D. J. Murphy, N. Porch & K.-H. Wyrwoll. 2008. Volume 97, Number 2 2010 Wagstaff et al. 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The ology of pollen tetrads and viscin threads in some Tenia, Rhododen- dron-like Ericaceae. Grana 35: 2 AENDIX l. A list of the DNA vouchers for this e Infor- ection Pb. and details, herbarium accession mimber, t number: matK, rbeL. riche divaricata R. Br., Cherry et al. (2001), Crayn et al. (1998), AY005094, U80432. Andersonia sprenge R. Br., eo al. (19993), Crayn et al. 0 AF015631, U 42. Arbutus canariensis Duhamel, Kron (1997), Kron & Chase (1999), U61345, L12597. Archeria comberi Melville, Kron et al. (19993), Crayn et al. (1996), AF015632, U79741. Astroloma | um (Cav.) R. Br. Daraa (2001), Crayn et al. 1998). AY372602, U80433. Brach daph (Sm.) Benth., Kron et al. (1999a), Crayn et al. (1998), AF015633, U . Don, Crayn 117, 1 Oct. 1995, UNSW o GQ392946, rry et al. (2001), acophyllum ., New Zealand, M. 1. 2003, "CHR 570437, GQ392947, GQ392895. Drecapirdium Diniker, New Caledonia, Province Sud, Mt. Hum- boldt. S. Venter 13855 & S. J. Wagstaf 17 May 2005, CHR 585693, arboreum Cockayne New Zealand, M HR 570439A8B, C00, balansae Pancher ex Brongn. & Cris, New J. Garnock-Jones 2481 & V. L. Woo, 10 Dec. 2002, CHR 1, GQ392899. Dracophyllum densum nsum W. R. B. Oliv., New Zealand, South Island, S. Venter 13746, 7 Jan. 1999, CHR 541924, C0392952, ifoli New Zealand, South Island, S. Venter 13753, 15 Jan. - € aa GQ392953, GQ392901. Dracophyllum B. Oliv., New Zealand, South Island, M. Giller s.n., a i CHR qunm GQ392954, füzgeraldii F. & Gris, New Caledonia, Province Sud, S. Venter 13850 & S. J. Wagstaff, 14 May 2005, CHR 585697 GQ392956, ii Berggr., New Zealand, South bliid, Abus Pun, M I. Dawson & P. Novis s.n., 20 Nov. 2003, CHR 570447, GQ392957, GQ392905. Dracophyllum i ., New Zealand, North ium A. Cunn NL or Ford, & S. J. Wagstaff, 10 Feb. 2004, CHR (J. oid & G. Forst.) R. Br. var. longifolium, New Zealand, Stewart Island, S. Venter 13787, 11 Jan. 2000, CHR 541960, CHR 541964, € ener New Caledonia, Province Sud, S. iw 13854 & S. Wagstaff, 18 May 2005, CHR 585692, GQ392960. — & N. Sueiber, Australia, NSW, Lansdowne a E A Brown 97/51, 12 Aug. 1997, i, NSW IIS. 60992 E Stewart bhad S. Venter 13788, 11 Jan. 2000, K UN E GQ3 GQ392910. Dracophyllum milli- Hook. t Australia, Tasmania, Mt. Field National Park, | Steane s.n., 13 Mar. 2005, CHR i — T di 1995, UNSW 22565, Crayn & C. J. uim gas 4 F ies muscoides GQ392912. yllum Hook. f., lew Zealand, South ng P. J. Garnock-Jones 2518, 18 Mar. xd CHR 591982, GQ , 6Q392913. oceanicum E. A. Br. & N. oil Australia, NSW, Jervis Bay, E. A. Broun pr 9 Sep. 1997, NSW 412484, 60392966, Zea- GQ392914. Dracophyllum ophioliticum S. Venter, New land, South Island, S. Venter 13800, 3 Mar. 2000, CHR 541973A-C, GQ392968, GQ392916. mense Virot, New Caledonia, Roches de la Ouaième, J. t Porters Pass, S. J. Wagstaff 2003, CHR 570444, e bord eri F. Muell., A a, Queensland, Ra ok A. Pins 34, 24 sen 1996, GQ392973, GQ392921. Zealand, land, P. J. 20113, CHR zr GQ392974, GQ392922. Dracophyl- Australia, NSW, Kellys Falls, E. A. lum secundi Brown 97/21a, 31 yos 1997, NSW Dx sie 16, GQ392924. 4. Dracoph 7 Hook. f., New Zealand, Annals of the Missouri Botanical Garden North Island, S. Venter 13760, 9 Feb. 1999, CHR kawi; Bon Neu Goladosia, Province Sod. Mi Humboldt, S. Venter 13853 & S. J. Wagstaff, 17 May R Dracophyl- aversii Ls f., New m South bed. Arthur's "aim Sock ” 2478, 3 nulatus G. Nicholson, Kron (1997), Kron ES Chase U61344, L1261. Harrimanella hyp s (L) Co Kron ide Crayn et al. (1998), uos U82766. Leucopogon microphyllus (Cav. R. Br, Cherry et al. (2001), E et al. TM: AY005097, U7974. Leucothoe racemosa A. G al. (1999b), € et s (1998), AF124564, troia Lysinema ciliat E. 999a), Crayn et al. (1998), nM. al. 5640, Br.) L. Watson, Crayn et al. (1998), Crayn et al. (1998), AF539984, U80422. Oligarrhena micrantha R. Br., Cr ayn et al. (1998), Crayn et al. (1998), AF539985, U80423. Pentachondra pumila (J. R. Forst. & G. Forst.) R. Br., Cherry et al. 0n, Crayn et al. (1998), AY005104, L126 nthoides (Labill.) R. Br., Kron et al. (19993), E et d (1996), AF015642, U79743. Pyrola rotundifolia L., Kron (1997), Kron & Chase (1999), U61328, L12622. Rhododendron kaempferi Planch., Powell 2002), Kron (1997), AF440428, AF419832. Richea m (Lindl.) F. Muell, Australia, Tasmania, Mt. Ossa, M. A. Korver 14, 2 Apr. 2004, CHR 572177, 6Q392983, 60392931. Richea in Menadue, Austra lia, Tasmania, egy? Hut, M. A. Korver 5 enl t: Blogg, = ar. 92984, 603929; Burt Ld. Victoria, : T Wagstaff & A. i m v 2005, CHR 580146A&B, CQ392985, nd Richea gunnii Hook. f. Australia, radle Mountain National Park, Waterfall Valley, M. E sn; Apr. nifolia, Australia, Tasmania, Crater Lake, M. A 31 Mar. 2004, CHR 572166A&B, GQ392988, 60392936. ce procera (F. Pg F. Muell., Australia, Tasmania, M. Korver 1 . Korver, 3 Apr. 2004, CHR pr OR. GQ392937. weas scoparia ‘Hook. f., Australia, Tasmania, Crater Lake, . Korver 2, 31 Mar. 2004, CHR 572165A&B, en: GQ392938. Richea sprengelioides (R. Br. F. Muell. Australia, Tasmania, radle Mountain, M. A. Korver 4, 31 Mar. 2004, CHR 572167, GQ392991, GQ392939. Richea victoriana Mena- ue, Australia, Victoria, Mt. Erica, A. Perkins & S. J. ie aii 14 Dec. 2005, CHR 580155A&B, GQ392992, 92940. Rupicola acta Maiden & Betche, et al. (1999a), Crayn et (1998), AF015643, U80427. Skena ` capitata (R. DA Lindl., Australia, I Australia, Crooked Brook Forest, S. J. Wagstaff Lemson s.n., 2 Nov. 2004, CHR 581897A8B, pl GQ392941. Sphenotoma dracophylloides Sond., Australia, Western Australia, a River National ark, E. A. Brown 97/326, P. G. Wilson and N. Lam, 18 Oct. 1997, NSW 416187, pier GQ392942. Sphe- notoma drummondii (Benth.) F. Muell., Australia, Western Australia, Stirling Ranges National Park, Crayn 39a, 2 Oct. 1995, UNSW 22959a, G' 392995, . Sphenotoma gracilis (R. Br.) Sweet, Australia, Western Australia, S. J. Wagstaff & K. Lemson s.n., 2 Nov. 2004, CHR 581898, GQ392996, GQ392944. Sprengelia incar- nata Sm., Australia, Tasmania, Cradle Valley, M. A. Mar. 2004, CHR 572164, GQ392997 viridis Andrews, Che a. (1998), AY005105, U81798. Trochocarpa f.) eap Crayn et al. (1998), U81799. Trochocarpa laurina (Rudge) R. Br., be et al. co) AY005106. "Vein uliginosum Kron (2002), Anderberg et al. (2002), AF419717, AF421107. "y PHYLOGENETIC RELATIONSHIPS Deepthi Yakandawala,5 Cynthia M. Morton," OF THE CHRYSOBALANACEAE 2nd Ghillean T. Prance* INFERRED FROM CHLOROPLAST, NUCLEAR, AND MORPHOLOGICAL DATA! ABSTRACT Chrysobalanaceae, a tropical family containing about 525 species, has often been nested within the 1 Rosaceae pus p! d evidence for recognizing it as a separate e family. In 1963, Pr Prance clear ly p "a 1 71 1 $11 ^" containing 17 genera. However, the family — within the order Malpighiales. B f th i hyl ti h t its monophyly and to investigate the gh esi 2o the oo, as well as its gites to other p Comparative phylogenetic analyses were performed us morphological, rbcL, and ITS sequences. The data sets analyzed independently and in combination. After exploration for hard i incongruencies "— > independent data sa simultaneous analysis of all the data was co resulted in a resolv with several unambiguous morphological synapomorphies. The resulting topology indicated that z family is a well-defined monophyletic group that is sister to Euphronia Mart. & Zucc. (Euphroniaceae). The ibal groupings, however, are paraphyletic. Key words: Chrysobalanaceae, Chrysobalaneae, Couepieae, Hirtelleae, ITS, morphology, Parinarieae, rbcL. The Chrysobalanaceae R. Br. includes 17 genera and at flowers (Licania elaeosperma (Mildbr.) about 525 species. Most of these species occur in the Prance & F. White) scarcely larger than a pinhead, to lowlands of the tropics and subtropics, and the family is — tubular flowers that are longer than 10 cm € Ey -— — in the ned irs age gabunensis (Engl.) Prance). Floral symmetry varies 7 gene almost completely actinomorphic to strongly same in four tribes: cta: which ak Crile: phic. In most genera, the entrance to to the e balanus L., Grangeria Comm. ex Juss., Licania Aubl., and P. an A DC.; Couepieae, which includes dissi five, completely free »e sepals that is Acioa Aubl., Couepia Aubl., and Maranthes Blume; slightly to strongly imbricate. Petals, we Pe S Parinarieae, which includes Bafodeya Prance ex F. always five and inserted on the margin One ae White, Exellodendron Prance, Hunga Prance, Neocarya are mostly ; however, they iN. iioc " (DC.) Prance ex F. White, and Parinari Aubl.; and than half of the species of Licania ide , which includes Atuna Raf. Dactyladenia stamens also varies from two in nd = Welw., Hirtella L., Kostermanthus Prance, and Magni- (Wall. Tea DC. to more than in stipula En ce & White, 1988) (Table 1). All species species EA attics are woody, and most are The ovary is fundamen = bs el m trees or shrubs. The vegetative architecture of the plants carpels, which are united only by i " noy x is relatively uniform. The flower, by contrast, is butin most species only ce is pa de comparatively diverse, although nearly every genus is fruit is basically a dry or xd d xn m id characterized by an underlying uniformity of inflores- The interiors of the fruit Th en s dt cence and floral structure. The flowers are bisexual, the endocarp is variable, often con m is rarely unisexual, and markedly perigynous. The flower mechanism for seedling escape (Prance, size and shape vary within wide limits, from minute & White, 1988). research anced Natural Environment authors thank Walter Judd for helpful discussions. This eh Sd supported by an D puel mm Rech! Council (NERC) Research Fellowship granted to C.M. an she e ais ¿Centre of Plant Di and Systematics, of Plant Sciences, University ng, € i em in a cad of Section Sue cione Museum n Natural History, 4400 Forbes Avenue, Pittsburgh, Pennsylvania U.S.A. A correspon dence: mortoncmQ'v w slg "ou img a Kew, Richmond, Surrey TW9 3AB, United Kingdom. of Botany, University of Peradeniya, Peradeniya, Sri Lanka. doi: 10.3417/2007175 HED oN 9 JuLy 2010. Ann. Missouri Bor. Garb. 97: 259-281. PuBLIS Annals of the Missouri Botanical Garden Table 1. Genera and number of species of tribes of Chrysobalanaceae (from Prance & White, 1988). Tribe/genera No. of species Chrysobalaneae Chrysobalanus 2 i 2 Licania 192 Parastemon 2 Parinarieae Bafodeya 1 Exellodendron 5 Hunga 11 Neocarya 1 Parinari 4 Couepieae Acioa 4 uepia 67 Maranihe: 12 Hirtelleae t 11 Dactyladenia 21 irtella 103 Kostermanthus 2 istipula 11 The family is locally important in the tropics for fruit, construction materials, fuel, charcoal, folk medicine, and shade trees. Several species cultivated. Chrysobalanus icaco L. (coco plum), for example, is tinned and bottled as syrup in Colombia macrophylla Sabine (gingerbread plum) and P. curatellifolia Planch. ex Benth. (mobola plum) are both eaten in Africa. Parinari curatellifolia is used in beer making, and a red dye is extraeted from its young leaves in West Africa. In Brazil, Licania tomentosa (Benth.) Fritsch is widely planted as an avenue tree providing shade and C. icaco is widely used as an ornamental in southern Florida. The taxonomic position of the Chrysobalanaceae has been particularly controversial. The majority of authors of general systems of classifications who treat Chrysobalanaceae as a family distinct from Rosaceae leave it in Rosales. Among other opinions, close affinities have been proposed for the Chrysobalana- ceae with a diversity of taxonomic groups: Dichape- talaceae and Trigoniaceae (Hallier, 1923), Gerania- ceae and Tropaeolaceae (Hauman, 1951), and Connaraceae (Cutzwiller, 1961). Many of these families’ and orders’ circumscriptions have changed in the last few years, and more recently the family has been placed in the rosid clade and sometimes in the order Malpighiales based solely on molecular data (Soltis et al., 2005). Cronquist (1981, 1988) placed Chrysobalanaceae in a much more widely conceived order of Rosales, including 24 families. He acknowledged that the es formed an exceedingly diverse order. How- ever, he thought it was more useful to delimit the order broadly than to fragment it and lose sight of the interrelationships among its parts. In 1989, Dahlgren placed the family into Theales under the superorder Theanae, whereas Thorne, in 1999, placed the family in its own order, Chrysoba- lanales, under the superorder Rosanae. According to Prance and White (1988), the embry- ological differences are great among the Chrysobala- naceae, Rosales, and Theales. During 25 years of studying Chrysobalanaceae, Prance and White found no evidence pointing unequivocally to an evolutionary relationship between the Chrysobalanaceae and any other family. The preliminary attempts to apply mainly morpho- logical data to a cladistic analysis at the family level by Prance and White (1988) were thwarted because of the widespread occurrence of parallelism and because only a few of the many characters used at this time satisfied the requirements for inclusion in a cladistic analysis. Chappill (1992) carried out a cladistic analysis, using the 1988 monograph by Prance and White, to determine the level of parallelism in the family and to see whether or not the Prance and White system was supported. The results of the analysis support a monophyletic family; however, many of the tribal groupings of Prance White were not well supported. Phylogenetic work using molecular data within this family is in its infancy. A large molecular phyloge- netic study using rbcL sequence data (Chase et al., 1993) places the Chrysobalanaceae in the rosid clade, with Trigoniaceae as the sister group. À study using 18S ribosomal RNA (rRNA) sequence data (Soltis et al., 1997) also placed the family in the rosid clade. Both of these studies only used one species of Chrysobalanus and Licania. The combined analysis of rbcL, atpB, and 18S data sets (Soltis et al., 2000) and the analysis of the same three genes plus nad1 B-C (Davis et al, 2005) housed the family in the Malpighiales within the eurosid I clade or, more recently, what has been called the Fabidae (Cantino et al., 2007) or the “fabids” (Judd & Olmstead, 2004). Other recent studies have examined one to three Chrysobalanaceae taxa with two to three genes and have also found the family positioned in the Malpighiales (Davis & Chase, 2004; Tokuoka & Tobe, ; Soltis et al., 2007); however, more taxa from different sources of DNA are needed to confirm this placement. Because of these discrepancies between and within the traditional taxonomy and the phyloge- netic analyses, further studies using phylogenetically Volume 97, Number 2 Yakandawala et al. 261 2010 Phylogenetic Relationships of Chrysobalanaceae more informative characters and more taxa from this Appendix 1 lists the voucher information, specimen family are warranted. numbers, type of material used, and GenBank To test potentially competing hypotheses of family numbers. Fresh (1-2.0 g) or dried (0.1-0.2 g) leaf circumscription and generic relationships in the ^ material was ground into a fine powder and incubated Chrysobalanaceae, i DNA regions that evolve at according to the shortened 2X CTAB procedure of different rates were sequenced and a morphological Doyle and Doyle (1987). Proteins were removed with data set was constructed. The first DNA region was — SEVAG (24:1, chloroform:isoamyl alcohol), followed the chloroplast gene rbcL, and the second was the — by an isopropanol precipitation. Purified DNA was p pan s stored at —80°C. E en x t (1) to test the : s: £ Chrysobalanaceae and their: relationships with the n m Malpighiales (APG II, 2003; Davis & Chase, 2004; The amplification of the rbcL gene was performed Davis et al., 2005; Tra & Tobe, 2006; Soltis et al., either as plete pi ing the fi 1 pri 2007) using an expanded rbcL analysis, and (2) to that matched the first 20 base pairs (1F-ATGTCAC- tigate the internal ic relationships withinthe CACAAACAGAAAC) of the exon and a reverse Chrysobalanaceae using rbcL, ITS sequencing, and — primer. (1460R-TCCTTTTAGTAAAAGATTGGGCC- morphological and anatomical studies. GAG) that matched a downstream control site M (Olmstead et al., 1992) or as two overlapping pieces ATERIALS AND METHODS using three additional internal primers, 636F BOE circ (GCGTTGGAGAGATCGTTTCT), 724R (TCGCATG- TACCYGCAGTTGC), and 1368R (CTTTCCAAATTT- The most recent systematic treatment of Prance and CACAAGCA GCA). When primer mismatch occurred, White (1988) has been followed as the basis for primer combinations changed accordingly. The poly- generic circumscriptions of the family. The genus merase chain reaction (PCR) was performed using Parastemon was not included in the analysis because standard protocols. The Thermal Cycler 480 (Perkin of lack of material. Elmer Ine., Waltham, Massachusetts, U.S.A.) was p to perform 25 cycles of denaturation at 94°C for 1 min., primer annealing at 50°C for 30 sec., Ou : : j and extension at 72°C for 1 min. Slight modifications tgroups varied depending on the analysis per- ,,, optimize the reaction conditions were Seed to be formed and material available. For the larger rbcL for some taxa; that is, the MgCl and bovine analysis, the following species were used: a single serum Ik (BS A) c As ent Mods wdro varied. species of Balanops Baill. (Balanopaceae), Cornus L. p, CEN OlAauick PCR iuo. tee ie Osa = purification kit (QIAGEN Ine., Chatsworth, California, u iaceae), Ochna naceae aoe Comesperma Labill. (Polygalaceae), Spiraea L. (Rosa- emsa ) folloving protocols provided by the ceae), Stylobasium Desf. Soltera sl. Cada F. Muell., Guilfoylia F. Muell., Suriana L. (Surianaceae), OUTGROUP SELECTION ITS GENE AMPLIFICATION (Picrodendraceae); two species of Trigonia Aubl. The amplification of the ITS gene was performed (Trigoniaceae) and Tapura Aubl.; and three species of sing oligonucleotide primers 17SE (ACGAATT- m Thouars (Dichapetalaceae). A subset of CATGGTCCGGTGAAGTGTTCG) a and "s dep the most closely related taxa were used for a smaller ¿q rbcL analysis. For the ITS analysis, however, only by Sun et al. (1994). The PCR was edes Dicha, ronia were used because of standard s; however, the DNA ede amplification problems. Dichapetalum and Tapura depending on the concentration, was diluted 1:10 or were chosen Jor the morphological analysis. These taxa 1:100. The thermal cycler was programmed to were select th L f Chase perform an an initial one cycle of denaturation at et al. (1993) and Litt and Chase (1999), and various 95°C for 2 min. followed by 24 cycles of 95°C for ee 30 sec., 55°C for 30 sec., and 72°C for 1 min. DNA EXTRA 30 sec. This was followed by 10 min. extension at oe 72°C. The same procedures described in the pre- The total genomic DNA was extracted from E ceding section were followed after completion of the _ herbarium, silica id or air-dried leaf samples. PCR. 262 Annals of the Missouri Botanical Garden CYCLE SEQUENCING 2.1 (Ronquis et al, 2005) under the Akaike Cleaned products were then directly sequenced using the ABI PRISM Dye Terminator Cycle Se- quencing Ready Reaction Kit with AmpliTaq DNA polymerase, FS (PerkinElmer Inc.) following the manufacturer’s protocol. Unincorporated dye termina- tors were removed using 3 mol/L sodium acetate and ethanol precipitation as recommended by the manu- facturer. Samples were then loaded into a gel on an ABI 373A am — Sequencer. ner sequenc- Leg 2 E MOTA Inc., lade. Wisconsin, U.S.A.). The alignments were constructed using the CLUSTAL dod All assemblies and initial align- ments underwent subsequent manual editing. MOLECULAR ALIGNMENT The conserved nature of the rbcL gene with no insertions and deletions (indels) made this a fairly simple task. For ITS alignments, the indel Pt method of Simmons and Ochoterena (2000) w adapted, while ignoring autapomorphies. MOLECULAR DATA ANALYSIS Phylogenetic analyses w perf using PAUP* version 4.0b10 (Swofford, 2000). Uninforma- tive characters were excluded from all analyses. Heuristic searches were conducted initially under the unordered and equal weighting criteria of Fitch parsimony (Fitch, 1971) with 100 random swapping and MULPARS in effect, steepest descen on. Ten trees were held in each step. Strict consensus trees were obtained, and branch lengths and tree scores were calculated € ACCTRAN (accelerated transformation o tion). The initial trees found with equal (Fitch) dn were used as the basis for escaled consistency index. Reweighting was continued until the same tree ree length was obtained in two successive rounds. Relative support for individual clades was estimated with the bootstrap method (Felsenstein, 1985). One thousand pseudoreplicates were pe with uninformative , characters excluded. To reduce bootstrap search times, branches were collapsed if their minimum length was zero (“amb-”), and no more than 2000 trees were saved per search. Bayesian analyses were performed using MrBayes 3.1.1 (Ronquist et al., 2005) on the individual molecular and combined molecular, and morpho ical and data sets. The substitution het for each DNA region was selected with MrModeltest Information Criterion (AIC). The parameters for the Bayesian analyses were as follows: nst — 6; rates — gamma; set autoclose = yes; 1000000; prinfewq = 100; ii briens = yes. In the combined i ne analysis (molecular and morphology), a mixed-model approach was used. The combined data were partitioned, and the above model of evolution was used for the molecular data sets. In each case, the first 25% of the trees were re as “burn in” and omitted, and the majority rule consensus tree was obtained in PAUP* from the remaining trees. SELECTION OF MORPHOLOGICAL CHARACTERS The coding method “C” in Kitching et al. (1998) has been adopted in this study. In this independent coding method, every attribute is given a separate character, and inapplicable observations for the absence of the feature are accommodated by using question marks. In the case of filaments, the presence and absence have been coded as a separate character, whereas the length, presence of hairs, and form in bud were coded as three independent characters. Inappli- cable observations for the absence of the feature were denoted with question marks to overcome the problem of overscoring the state's absence when many different characters are perceived as connected to a feature that is absent from some taxa (Maddison, 1993). Potentially useful characters had to be discarded h data for only a few g ilable. Many of the characters are readily coded as binary; however, patterns of morphological variations found in the taxa necessitate the use of unordered multistate characters. When genera are scored as terminal taxa, a large amount of polymorphism can be introduced into the data set because of the highly variable nature of some taxa. In this study, to avoid problems associated with the inclusion of polymorphism in the data set (Nixon & Davies, 1991), subgeneric-level taxa have been included for the genera Licania and Magnistipula. INGROUP SAMPLING All the 17 genera in the Chrysobalanaceae have been coded for their morphological characters. Characters were scored to the extent possible from herbarium specimens taken primarily from the collection at Royal Botanic Gardens, Kew. This information was supplemented with published obser- vations from the literature (Prance, 1963, 1972, 1989; Prance & White, 1988) and personal knowledge of one of the authors (Prance). Characters were selected by reviewing previous work and searching for variations that had not been previously analyzed. Volume 97, Number 2 2010 Yakandawala et al. Chrysobalanaceae PREPARATION OF MORPHOLOGICAL MATERIAL Flowers. Dried herbarium material was revived by boiling in water and then dissected and observed using a dissecting microscope. Leaves/leaf architecture. Leaf venation (primary vein [midvein], secondary, tertiary, and quaternary veins) was coded by clearing leaves and observing their One hundred ninety-seven herbarium leaf samples were used in this study. The materials were obtained from the herbarium at the Royal Botanic Gardens, Kew. Vouchers used in this study are listed in Appendix 2. The protocol for leaf clearing was modified from Radford et al. (1974) for herbarium materials. Terminology in general follows Hickey (1979). MORPHOLOGICAL DATA ANALYSIS The data matrix consisted of a total of 50 characters. The matrix is presented in Table 2, and the list of characters and character states used in the morphological analysis is presented in Appendix 3. Of the 50 characters, 38 are binary (in which 16 of them are coded as simple absence/presence) and 12 are multistate. All analyses were conducted using PAUP* as stated above. RESULTS For the parsimony analyses, the potentially infor- mative phylogenetic characters in each data set, the number of trees, the tree length, the consistency indices, the retention indices, and the number of branches with bootstrap values along with the number of branches with bootstrap values greater than 70% are found in Table 3. For Bayesian analysis, the number of branches with posterior probability values greater than 90% and 95% are found in Table 3. LARGER RBCL The length of the analyzed rbcL gene is 1382 bp in all samples, and no gaps were required for alignment. Approximately 45 bp at the beginning and 17 bp at the end were deleted from the rbcL matrix. There were 984 invariant characters. The final data matrix consisted of 398 variable characters, of which 241 were parsimony informative. Unweighted pairwise sequence divergence among species of Chrysobalana- ceae ranges from 0.2% to 2.9%; that between species of Chrysobalanaceae and the outgroups ranges from 4.5% to 10.5%. Sequence divergence among the outgroups ranges from 1.6% to 19.0%. Mean percentage G + C content is 45.0%. A h LBS h ole then Pink yielded 338 equally most parsimonious trees (MPTs) of 749 steps with a consistency index (CI) of 0.49 and a retention index (RI) of 0.74. Successive weighting produced 139 MPTs of 223.22 steps with a CI of 0.67 and an RI of 0.89, which corresponds to a Fitch length of 753 steps, a CI of 0.49, and an RI of 0.74. The unambiguous _transition:transversion ratio was 318:200 (1.59). Only the Bayesian tree is shown in Figure 1 due to space limitations. All trees recovered well-supported and monophyletic Chrysobalanaceae (100% Fitch equal and successively weighted trees and the Bayesian tree). In addition, all trees resolved Euphronia as sister to Chrysobalanaceae with Dicha- petalum and Tapura (Dichapetalaceae) and Trigonia (Trigoniaceae) as sister to Euphronia. Balanops (Balanopaceae) is placed as the sister taxon to the above grouping. Although the family groupings are poorly resolved on the strict consensus Fitch tree, the successive weighting and the Bayesian tree slightly increased both the resolution and clade support. In the strict consensus Fitch tree, the generic relation- ships are poorly resolved, consisting of only three clades: Couepia-Couepia uber (bootstrap support [BS] 88%); Maranthes-(Grangeria-Magnistip- ula); and Hunga—Neocarya. The successively weight- ed tree is mostly a polytomy with only three major clades present: Hirtella—Hirtella bicornis Mart. & Zucc.-Licania-(Couepia—Couepia robusta [BS 9696]: Maranthes-(Grangeria-Magnistipula) (BS 7296); and Chrysobalanus-(Hunga-Neocarya [BS 9396]. In the Bayesian analysis, the generic relationships are poorly resolved, consisting of a polytomy with four clades: Couepi ia robusta (100%); Dactylade- nia—Trichocarya (71%); Maranthes+{Grangeria—Mag- nistipula [74%]) (98%); and Hunga—Neocarya (58%). SMALLER RBCL In this analysis, there were 1143 invariant characters. The final data matrix consisted of variable characters, of which 118 were parsimony informative. Uninformative characters were excluded from the analysis. Unweighted pairwise sequence divergence among species of Chrysobalanaceae rang- es from 0.2% to 2.9%; that between species of Chrysobalanaceae and the outgroups ranges from 45% to 7.3%. Sequence divergence among the outgroups ranges from 2.3% to 7.0%. Mean percent- age G + C content is 45.0%. A heuristic search under the Fitch criterion yielded 577 equally MPTs of 182 steps with a CI of 0.65 and an RI of 0.73. Successive weighting produced 139 MPTs of 88.81 steps with a CI of 0.89 and an RI of 264 Annals of the Missouri Botanical Garden Table 2. Matrix of morphological characters. See Appendix 3 for character list; ? = missing data or inapplicable eharacter states. E Ë 3 4$ 5 6-1 8. 9:40 HH 412 13 HM Chrysobalanus 1 O 0 6l I I0 Jol O 07-1 0 1 Grangeria E 0 0 Igl1 89 eh 0 Tos 1 1 Licania subg. Moquilea be 6.0% 6.1. 0 OTT O O0 1-90 1 Licania subg. n ü 6 Ol J 0 1 1 FEA o 0 1 Licania subg. Lic BOB mota 1120. 6-1. 0-1 Licania subg. Alicia 1 0 0 0. 0. 1 0 Fer o Ev 0 1 Licania subg. Angelesia iD 0 1:0 I 0 Ld 8 Q c1 isa Licania subg. Leptobalanus 01 0 Ol Ol 0 1 0 bk 0 0.1 0 1 Parastemon I 0 0 (0.0 0.9 Jo q O 0:1 0 1 Bafodeya 0 O0 1 I 0 L 0 1 1 0 0. I [NEN Exellodendron I: O Ü 0r 0 f Q LE 1:0 n. 4 0 1 Hunga 1 O 0(6-Or d.1- 0 Al IL 0 Ü. cf 0 1 Neocarya I. | 1 P 0I 0 E cuu 0. 1 0 2 inari Bro 1 I 9 I 0 EE Ü I 0 1 Acioa pto" 0 gu A 0 Ed 0 0 1 2 2 Couepia E SHE Ob OP Ah I roo ©- T 02 1 Maranthes 1 O 032-00) 0 I 0 1. 3-0 o E 02 1 Atuna i 9 0 qot 0 pol 0 1 0 1 Dactyladenia po) USO TC 9 T9 0 1 802 2 Hirtella Pei (comp vp ps Bode 90 Gb 1 0 1 Koste dl 0 0-0 159 bo - Aj 0. 1 2 2 Mud subg. Magnistipula Lb. 0 0 0 :0- 1 0 1. 1s 0 0...1 0 2 agnistipula subg. Pellegrinie 1.8 0 0D. 8—l1-..0 Lob 5 0. 1 0.2 Magnistipula subg. Tolmiella L. O 0 0.0.1... 0 be 8 0 .1 1 2 Dichapetalum J O D DP. 00 O L J 0 0 0 0 01 Tapura b. 0 0 0 0 0 i € 9 o 0 202 0 Stephanopodium I 9 0 0 00 60 1 1 O 0 0 0 2 0.93, which corresponds to a Fitch length of 182 steps, a CI of 0.65, and an RI of 0.73. The un- ambiguous transition:transversion ratio was 157 to 196:78 to 105 (2.01 to 0.018). Figure 2A shows the successively weighted strict consensus tree, and Figure 2B shows the Bayesian tree. All trees recovered revealed a monophyletic Chrysobalanaceae. The family is well supported (100% bootstrap Fitch equal and successively weighted trees) as a monophyletic group on trees. Although the family groupings are poorly resolved on the strict consensus Fitch tree, the successive weighting increased both the resolution and clade support. Only the clade Licania-Chrysoba- lanus is supported on the equal-weighted tree; on the weighted tree, however, four major clades are supported. The number and distribution of unambig- uous transition:transversion ratios c 105) and successively weighted (157 to 174:78 to 101) trees. On the strict consensus of the successively weighted rbcL tree, four major clades can be ognized. Clade A with Atuna is sister to a poly- tomy consisting of clades B, C, D, Acioa, Bafodeya, Kostermanthus, Neocarya, and Parinari. Clade B is an unresolved polytomy containing Grangeria-Mag- nistipula-Maranthes (BS 69%). Clade C contains an unresolved polytomy of Dactyladenia—Exel ron— Hunga. Clade D is a monophyletic clade bearing Hirtella-Couepia—(Licania—Chrysobalanus [BS 85%]) supported by 84% bootstrap. In the Bayesian analysis, the family is monophy- letic and well supported (10096) The generic hry: epia-Hirtella (60%); Magnistipula [64%]) (96% conflicts between the Bayesian tree and parsimony trees. ITS Boundaries of the coding and spacer regions were estimated by d with of the ITS sequences region in Baldwin (1992). Sequences were easily aligned, with only li being slightly difficult in containing a large indel, and cloning was not - Volume 97, Number 2 Yakandawala et al. 265 - 2010 Phylogenetic Relationships of Chrysobalanaceae Table 2. Continued. 15/16 17318 1 $30 21.32) 3 es MM MD» alanus 21 10 60 1901 |! 5» : PB 9 Grangeria E 00 ? 0 1 Po. lol À | 0a Licania subg. Moquilea or r1: »)? of od 50] 1 06 P * 9 subg. Parinariopsis F 11001 rr 1 P |] 0 Ë l 5 ia subg. Licania o! 1 1 1200 Po 03 0 INM? Licania subg. Afrolicania o X l I L »9 9 0; ] | 0 0 0p 09 Licania subg. Angelesia I p 1/701 r $9 1 I? O0 1.0 0 D 9 9 Licania subg. Leptobalanus or p 1:1 4 poa b 9975.5 ee Parastemon irion Q 0 |» 9.01] Wd.» 9 9» Bafodeya y d c!d 1 a | Í l 1 0 1 Exellodendron U p 0192 7) TP l Q 1] 0: 1 >... Hunga y 9o 019132 3) 11 9] l 0 * |" "7 Neocarya UE oe 159 * | 1! 1 P | 2? ù f Parinari Lol 1701 © d) pr 8| | 8 | Fe Acioa yr 21503 2111 11 1 3 EF ! 3? Couepia UL plo) 20k 51ra # | pP, Maranthes y po ta )peoec1d | 6 b | "7 r riw: 10310101 | j $ j| P) Dactyladenia rrr 027 22r) 1 | 3 8 Hi 1 061 0 q re ©) te ee Kostermanthus r m hi p w opp 63) P ` 3 ^ DO Magnistipula subg. Magnistipula zinaa 2 k jp .....o Ee subg. Pellegriniella UL z 1 02 2 Fp l 01 b 9 1 P 0 Magnistipula subg. Tolmiella r21912 ar ü 1 1! * l1 J! 9 um ro: ? fe rro... 0 1 Tapura U 277» Kk 111? 0! |! $ 5 ] 3 necessary. The length of the ITS region ranges from 763— matrix of 833 MTM Of the 833 779 bp among species of Chrysobalanaceae and from constituting the aligned ITS sequences. 411 were 754-784 bp among the outgroups. The The ingroup length of variable and 234 were parsimony informative. a E ranges from 319-332 bp, that of the 5.8S subunit mative characters were excluded from a 160—162 bp, and that of ITS-2 from 278-290 bp. the 234 parsimony informative characters = The inclusion of gap coding resulted gap coding was not used in the following results. ITS-2 from 277-304 bp. Multi e sequence alignment of Chrysobalanaceae La cee, resulted in a data ‘A heuristic search under the Fitch criterion yielded matrix of 833 characters, of which 168 (20.2%) include 18 MPTs of 751 steps with a CI of 0.57 and an RI of Successive weighting ed two equally at least one accession with a gap (92 of 332 positions produc [27.7%] in ITS-1, 5 of 162 positions [3.1%] in the 5.85 _ parsimonious € 288.3 steps E uk subunit, and ITS- and an RI o 039. ich corresponds to a Fite ii e d n CI of 0.57, and an RI of 0.39. The Chry from 5.8% to Tamilicictuporepsion mtio was 371:281 (1.320). 16.5% in ITS-1, from S to 19.9% in ITS-2, and Figure 3A shows the Did weighted strict from 0.0% to 5:6% in the 5.8S; that between species of consensus, and Figure 3B shows the Bayesian tree. Chrysobal The ITS sequence data, both equal-weighted and W 34.9% in ITS-1, from 36.3% to 79.1% i in n and weighted analysis, indicate a from 0.3% to 7.3% in the 5.8S subunit. Mean naceae (79% bootstrap for the Fitch tree and 100% for i the — weighted tree). Successive n Multiple sequence alignment of Chrysobalanaceae trees are more resol ed and have more support wi snn s fewer trees with a O ccu Annals of the Missouri Botanical Garden Table 2. Continued. 3 3 32 3 354: 35: 36. 37 38 39 40 41 4 hrysobalanus 0- 0 Ü sl is 1 1 1 0^ 0-.0 0 1 Grangeria OZ D. VE 170 1 0 0-. 9 1 ? ? Licania subg. Moquilea 0-0 0 1 Fecr 1 1 o x ? ? ? Licania subg. Parinariopsis 0 It 0 -— bis 1 1 1 Oa? ? ? ? Licania subg. Lic 0,1 0 0 1 1 1 1 Or -01 ? ? ? ? Licania subg. Afrolicania 0. 0 O sit La 0 1 1 0 ? a ? ? Licania subg. Angelesia 0:.0 ir 10 1 1 1 1 0-. 3 2 ? ? Licania subg. 0: 0 Dl Lit 1 1 0 d 1 ? ? P. 0,1 0 0 1 0 1 1 0 0 0 0 0 0 a 1 1 1 1 EE 1 0 EQ 1 ? ? Exellodendron 1 2 1 1 I3 1 1 0: 9 1 ? ? Hunga 1 1 1 1 T uk 1 1 o 0 1 ? ? Neocarya 1 2 I l 1 1 1 1 1 1 2 0 0 Parinari 1 1 1 1 1 1 1 1 1 1 ? 0 1 cioa icr Oe Oa DOE 1 0 0.9 1 1 ? Couepia (Lco G41 Leak 1 OE o 1 1 0 1 Maranthes 1s 2 1 1 Et p 1 1 0. 1 1 1 0 Atuna bro 1 1 I3 1 0 1 1 1 0 ? yladenia T2 oct Lg 1 0 1 1 1 0 ? Hirtella 1 2 0 1 1 H 1 1 0 0 I 0 1 Kostermanthus 1 2 5-a 1 1 1 0 1 ? 0 ? ? Magnistipula subg. Magnistipula 1 2 ai I 1 1 1 1 1 ? 1 0 0 Magnistipula subg. Pellegriniella 1 2 1 1 1 1 1 1 1 ? ? 0 2 Magnistipula subg. Tolmiella is 2 O 33 Eu 1 I 1 2 ? 0 ? Dichapetalum 0- 0c M sb oy 0 0 1 ? ? ? 2 Tapura ia $ Loeb I. 6 0 oan a oe Stephanopodium b. Et A ie 0 0 l1 4d * oj synapomorphies than the equally weighted trees. COMBINED DATA Therefore, the results are discussed based on the d strict consensus tree. A total of 50 unambig- uous pomorphies €— the family using the ad strict consensus tre The family is a (BS 100%) with low internal resolution in the successively weighted strict consensus tree. The internal family clade contains B. Neocarya-Parinari (BS 96%) sister to ps A agnistipula-Maranthes). Clade B has ron—Hunga (BS 52%), which is sister to (Chrysobalanus—Couepia)—Hirtella—Licania [BS 67%)). In the Bayesian analysis, the family is monophy- letic and well supported (100%). The internal family clade contains a polytomy of clade A sister to Dactyladenia-(Kostermanthus-Atuna | |8796]) (93%), Acioa—Couepia—Chrysobal ron—Hi o = between the supported clades of the Bayesian and the parsimony topologies. Following the modified methods outlined by Mason- Gamer and Kellogg (1996), we considered the data sets combinable. In all analyses, the family is uh with 100% bootstrap support. Only in conflict between the rbcL and the ITS es with bootstrap values greater than 75%. In the rbcL parsimonious tree (Fig. 2A), Chrysobalanus— Licania are held together with 85% bootstrap support forming a polytomy with Couepia—Hirtella (BS 84%), whereas in the ITS tree (Fig. 3A) these two taxa are grouped as Chrysobalanus—Couepia sister to Hirtella— Licania (BS 67%) with less than 70% bootstrap support. There are no hard conflicts between these trees; therefore, the incongruence is interpreted as being due to chance and the data sets were combined. Within the Bayesian analysis, one position is in conflict between the rbcL and the ITS topologies with posterior ee greater than 95%. In the rbcL tree, nthes-(Grangeria-Magnistipula [64%]) ru (Fig. c form a f whereas in the ria—(Magnistipula—Maranthes m (75%) ae a clade (Fig. 3B). only conflict is due to the lack of resolution and having Volume 97, Number 2 Yakandawala et al E pss — Phylogenetic of Chrysobalanaceae Table 2. Continued. 4 4 4 & "7" 4 ^ 9» posean 1 0 0 1 1 0 1 0 E Srengrria 1 0 1 1 0 0 1 0 Ei subg. Moquilea pee ün @ 0 1 ° ; Licania subg. Parinariopsis 1 0 0 1 0 0 1 0 Licania subg. Licania 1 0 0 1 0,1 0 1 0 Licania subg. E 1 1 0 1 1 0 1 0 Licania subg. À 1 0 0 1 0 0 1 0 Mitania subg. aseo O b m 1 0 Parastemon 0 1 5 ó 1 0 Bafodeya ? 1 0 1 o 0 1 0 _ Exellodendron ? 0 0 1 e o 1 0 Hunga ? 1 0 1 ü 0 1 0 Neocarya 1 | ó Q ; UIT d 0 Parinari 1 1 1 1 B i 8 0 Acioa 0 1 1 1 > i 1 0 Couepia 1 1 1 1 | 3 3 I Maranthes 0 i s. | 6 ò i 0 Atina 1 1 0 1 0 0 1 0 Dactyladenia 0 1 0 1 é ù 0 Hirtella 1 b 10 1 io 1 N Kostermanthus ? 1 1 o 4.0 1 0 Magnistipula subg. Magnistipula 0 1 1 1 0 0 1 Y Magnistipula subg. Pellegriniella 0 1 0 1 0 0 1 0 Magnistipula subg. Tolmiella 0 1 1 0 1 0 1 0 Dichapetalum ? 1 0 1 o Ó i 0 Tapura ? 1 0 1 o o 1 0 — e P T PM 1— Bafodeya ux in the rbcL topology. Therefore, A heuristic search under the Fitch criterion there are no real hard conflicts between these trees. yielded nine MPTs of 850 The consensus In the Sabine’ molecular data set, only two tree had a CI of 0.56 and an RI of 0.41 (trees not outgroups, Dichapetalum and Euphronia, are in shown). Successive weighting of this tree — common. Difficulty in either amplification or the one equally parsimonious tree of 332.87 steps with a limitation of plant material caused this reduction in CI of 0.66 and an RI of 0.62, which c to the number of outgroupa The total combined dala sot = Fick Jengih TOR © CI of 0.56, and an RI of consisted of 2215 characters, of which 280 characters 0.41. The successively weighted E fu were parsimony informative. tree is more resolved than than the equal-weighted tree, Table 3. Comparison of results from the parsimony analysis of the larger rbcL, rbcL, ITS, and a combination of all data. Bayesian values BS= PP= PP= RI BS 70%' 909 95%" Large rbeL 382/241 139 . a 1382/118 pe. 065 0.73 ITS 833/234 2 mo 051 uw 1 2 5 5 Combined 2265/315 2 033 5 3 ? 3 BS, bootstrap support; CI, RI, ` Ps iwaw iau. ie ka d ime oe eee vers = aS) ed ihe reese one m 70%) were included. | as suelo D t ER = 90 (lie number f branches t n PO ) and post sis, Io Pot qusa = 95% (he number of branches that that contained posterior probabi rior probability ility values — 268 Annals of the Missouri Botanical Garden Cornus eydeana Dichapetalum Dichapetalum crassifolim Dichapetalaceae Tapura Dichapetalum macro. Tapura amazonica Trigonia Trigoniaceae Trigonia nivea Euphronia Euphroniaceae Acios Chrysobalanaceae Bafodeya Chrysobalanus Couepia Couepia robusta Dactyladenia Trichocarya splendens p: Balanops vieillardii N Tetracoccus dioicus Androstachys johnsonii Ochna serrulata Stylobasium Stylobasium australe Guilfoylia monstylis Suriana maritime Cadellia pentasylis Comesperma ericinum Figure l. Bayesian consensus tree from the larger rbcL analysis. Numbers above nodes are posterior probability values. therefore the former is the tree used in the following clade B. Clade A has Neocarya—Parinari (BS 67%) discussion. sister to (Bafodeya-Grangeria)-4Magnistipula-Mar- The family is monophyletic with strong bootstrap anthes [BS 73%]). Clade B has Acioa basal to support (100%). The internal family clade contains Exellodendron-Hunga (BS 99%), which is sister to Atuna, Kostermanthus, clade A, Dactyladenia, and (Chrysobalanus—Couepia)—(Hirtella—Licania). Volume 97, Number 2 Yakandawala et al P ; 269 Phylogenetic Relationships of Chrysobalanaceae a rugosum b __A. The successively weighted strict consensus tree Cl = 0.65, RI = i . from the Chrysobalanaceae (length = 118 steps, ayesian consensus tree with posterior probability v In the Bayesian analysis, the family is monophy- letic with good posterior probability values (100%). The internal family clade contains a polytomy of four clades, part of clade A from above, clade B, Neocarya—Parinari (100%), and Dactyladenia-(Kos- termanthus—Atuna [92%]) (90%). Clade A contains Trigonia eriosperma trees obtained from the rbcL of 139 most parsimonious 0.73). Numbers below nodes are bootstrap values. —B. Magnistipula-Maranthes (BS 100%), Grangeria (94%), and Bafodeya (70%). Clade B has Acioa sister to Exellodendron-Hunga (BS 100%), which is sister to Chrysobalanus-Couepia-(Hirtella-Licania [56%] (85%). There are no conflicts between the supported clades of the Bayesian and the parsimony topologies. 270 Annals of the Missouri Botanical Garden P Euphronia v 52 Dactyladenia B Figu uccessively — strict consensus tree of the tw CI = n a RI = 0 39) hasta from the ITS data from the C Chumik i —B. Bayesian consensus tree with nicis probability values. According to a modified Mason-Gamer and Kellogg (1996) method, the combined molecular and morpho- logical data sets were considered combinable. An independent morphological and molecular analysis Atuna Dichapetalum Euphronia Kostermanthus Dactyladenia Bafodeya Grangeria Magnistipula Maranthes Neocarya Parinari Chrysobalanus Couepia Exellodendron A Licania most parsimonious trees (length = 749 steps, Numbers below nodes are bootstrap values. was completed under parsimony. Although the morphological topology is considerably differen from the combined molecular topology, there is little bootstrap support on the morphological tree. There- p : = : Volume 97, Number 2 2010 Yakandawala et al. 271 Phylogenetic Relationships of Chrysobalanaceae fore, conflicts between the data sets with bootstrap values greater than 75% do not exist. The total combined data set consisted of 2265 characters, of which 315 characters were parsimony informative. A heuristic search under the Fitch criterion yielded 12 MPTs of 985 steps. The consensus tree had a CI of 0.533 and an RI of 0.386. Successive weighting based on this tree produced two equally parsimonious trees of 255.66 steps with a CI of 0.741 and an RI of 0.702, which corresponds to a Fitch length of 987, a CI of 0.532, and an RI of 0.383. One of these trees is shown as a phylogram in Figure 4A. The successively weighted trees are more resolved than the equal- weighted trees and contain higher bootstrap support than the equal-weighted trees. Therefore the following discussion uses the successively weighted tree. Only the outgroup taxon Dichapetalum is common to all three data sets. Euphronia was also included, even though the morphological data have been coded as missing data due to the lack of adequate material. Chrysobalanaceae is monophyletic with strong bootstrap support (10096). Atuna is sister to the remaining taxa. The next clade consists of Koster- manthus, sister to Acioa and Dactyladenia. This clade is sister to two larger clades. The first contains Exellodendron-Hunga (BS 100%) sister to (Chryso- balanus—Couepia)—(Hirtella—Licania) (BS 60%). The second clade has Neocarya—Parinari (BS 70%) sister to (Bafodeya—Grangeria) (Magnis istipula—Maranthes). The pri difference between the combin and e combined molecular tree is the clade containing Kostermanthus In the Bayesian d (Fig. 4B), the d is monophyletic and well supported (100%). internal family clade contains a polytomy of =< clades, clade A, clade B, and Dactyladenia-(Koster- manthus—Atuna [BS 82%]) (BS 65%). Clade A has a weakly supported polytomy of Bafodeya with Gran- geria—(Magnistipula—Maranthes [BS 98%)) (BS 98%), and Neocarya—Parinari (BS 100%). Clade B has Acioa sister to Exellodendron-Hunga (BS 100%), which i is Hirtella—Licania (BS 90%). conflicts between the supported clades of the Bayesian and the parsimony topologies; in fact, they are very similar except for the positions of Atuna and Acioa. Discussion RELATIONSHIPS OF CHRYSOBALANACEAE A recent study using 18S rDNA, rbcL, and atpB sequence data (Soltis et al., 2000) showed that even though Chrysobalanaceae had been closely associated with Rosaceae by previous workers, it is not closely related to the family. Both independent (rbcL) and combined analyses support the sister-group relation- ship of Chry to Trigoniaceae (Chase et al., 1993), to Dichapetalaceae (Soltis et al., 2000), to Balanopaceae (Soltis et al., a - - rane (Litt & Chase, 1999), thi Malpighiales. A relationship between the Chrysobala- naceae, Trigoniaceae, and Dichapetalaceae based on nonmolecular data had been by Hallier (1908, 1921), although few phylogenetically useful morphological features were produced from this study Recently, Litt and Chase (1999) attempted to find logical evidence to support the relationships between Chrysobalanaceae, Trigoniaceae, Dichapeta- laceae, and Euphroniaceae. m and Chase (1999) found no obvious morphological synapomorphies, although there was strong T support for these nip - malpaca peeks "— - the cedar. group tmm of Chrysobalanaceae š and pas The boser rhe sister taxon to a with Dichapetalum and Tapura (Dichapetalaceae) and Trigonia (Trigonia- ceae) sister to Euphronia. Balanops (Balanopaceae) occurs as 5. ihe sister Mw M m above grouping, pits, paracytió stomala, ak zygomorphic flowers, and tenuinucellate ovules. In addition, Chrysobalana- ceae, Dichapetalaceae, and Trigoniaceae have two ovules per carpel. The work of Matthews and Endress (2008) synapomorphies for ok of the families and conclud- ed that the phylogenetic topology for these families still remained unresolved mainly due to a lack of molecular data. Our study found Chrysobalanaceae as a well-supported family, sister to Euphroniaceae, and Trigoniaceae formed a MONOPHYLY OF CHRYSOBALANACEAE A eroatly varied greatiy mibi past mda The genera of the uk naceae traditionally have often been linked with the Rosaceae (Jussieu, 1789; de Candolle, 1825; Meisner, 1837-1838; Hooker, 1865; Focke, 1891) or occasion- studies, and blastogeny taken in 272 Annals of the Missouri Botanical Garden 23 Euphronia Acioa COU 87 13 Dactyladenia HIR Kost hus HIR Bafodeya PAR Grangeria CHR nae Magnistipula HIR Maranthes cou Neocarya PAR Parinari PAR Chrysobalanus CHR Couepia COU Hirtella HIR Licania CHR Exellodendron PAR Hunga PAR a - Atuna HIR igure 4. =A One of the most parsimonious trees arbitrarily selected from the two equally optimal trees from the e li € 7 steps, CI — 0.53, RI — 0.38). Numbers above each branch are branch lengths. Numbers ts! ¿ Volume 97, Number 2 2010 Yakandawala et al. 273 Phylogenetic Relationships of Chrysobalanaceae Figure 4. Continued. conjunction with leaf anatomy and chemistry. Our results show that the Chrysobalanaceae clade is strongly supported by the independent and combined morphological and molecular analyses. The family has three unambiguous morphological synapomorphies, i.e., presence of silica bodies, a receptacle tube (= hypanthium), and a gynobasic style. Individually, these characters occur in various groups of eudicols; however, the combination of these features is distinctive. Other families, the Lamiaceae and Boraginaceae, are currently recognized as having a CHR cou Kostermanthus PAR cou gynobasic style, but these families do not have silica bodies widely present. Although the given features occur sporadically in other families, they are diagnostically significant in this family because the combination of these features is taxonomically restricted. The combination of these features suggests a close phylogenetic relationship between these genera. It is clear from the phylogenetic studies that the gynobasic condition evolved within the family clade. These features also clearly separate Chrysoba- lanaceae from the Rosaceae. 274 Annals of the Missouri Botanical Garden I THE RE OF None of the four traditionally defined tribes are p in the combined or independent analysis. The best-resolved trees came from the a analysis of the combined data set, which included 16 taxa of Chrysobalanaceae and two outgroups. The morphological Mid states were traced onto the combined mo and molec- ular tree using MacClade 4.0 (Maddison & Maddison, 2000) in order to find non-homoplasious characters. This combined analysis contained internal support for most of the major ew which we have named "clade 1," *clade 2," e 3,” “clade 4,” and “clade 5.” Clade 1 consists of Exellodendron and Hunga (100%) from the tribe Parinarieae and has no morphological synapomorphies. This clade is sister to clade 2, which consists of a polytomy of Chrysoba- lanus and Licania of the tribe Chrysobalaneae, Couepia of the Couepieae, and Hirtella of the tribe Hirtelleae. This clade has support (90%) and has one unambiguous synapomorphy of the presence of leaf venation of secondary vein type 1. Clade 1 and clade 2 4 i e 3 has one unambiguous synapomorphy: leaf hs present. The above clades are sister to a polytomy of Bafodeya, clade 4, and clade 5 (57%). Clade 4 contains Neocarya and Parinari (100%), belonging to the Parinarieae with two morphological synapomorphies: the presence of stomatal crypts and 5 (98%) has no known morphological synapomorphies. TYPES OF ANALYSIS Two primary types of analysis were completed: parsimony analysis using successive weighting and Bayesian analysis. The combined molecular and morphological data sets had similar topologies with two of the three major clades in agreement. There were three clades with greater than 70% in the successively weighted tree and five clades with the posterior probability values equal to or greater than 95% in the Bayesian tree. The successively weighted tree provided similar topology with less support than the Bayesian analysis, indicating that within this data set the successively weighted tree is more conservative. Taxonomic CONCLUSIONS Ch y Lol + s lly 1, is monophyletic. Euphronia of the Euphroniaceae is the closest relative to the Chrysobalanaceae. Under the current m these families would be placed in the eurosids (Rosidae, in Cantino et al., 2007) in the order Malpighiales E , 2003; Davis & Chase, 2004; Davis et al., 2005; Tokika & Tobe, 2006; Soltis et al., 2007). None of the four traditionally recognized tibio; Chrysobalaneae, Couepieae, Parinarieae, and Hirtel- leae, are monophyletic. Morphological data indicate hat the genera Licania and Magnistipula are not aa and further work using molecular data needed to confirm these findings and restructure generic limits. This study did find that there probability values and a few morphological characters calera Norphologiest synapomorphies. Future studies will include sila) NA regions and examination of additional morpho- logical characters. Only when more molecular and ological characters are examined can taxonomic mo realignments be formalized Literature Cited Angiosperm Phylogeny Group. 2003. An update of the Angiosperm Phylogeny Group I for the orders and families of flowering plants: APG II 141 ie Baldwin: B. G. . Phylogenetic utility of the internal transcribed de cu nuclear ribosomal DNA in plants: An example from the Compositae. Molec. Phylogen. Evol. 1: 3-16. Candalle, A. y de. 1825. Rosaceae, Chrysobalanaceae. 529. Candalle, A. + P. P. de. 1842. 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Molecular phylogeny of families related to Celas- trales on ET 5' flanking sequenc Phylogen. Evol. 3: 2 2-5 M. W. Chase, k EY Yay, D. C. Albach, A. Backlund, M. van der Bank, K. M. Cameron, S M.D Lledo, J. C PRONTA E C dono, D D. E. Soltis, P. S. Soltis & P. Weston. 2000. Phylogeny x the eudicots: A nearly complete familial analysis based on rbcL gene sequences. Kew Bull. 55: ine Simmons, M. P. & H. Ochoterena. 2000. as characters phylogenetic isis Souk Biol. 49: 276 Annals of the Missouri Botanical Garden Soltis, D. = D. R. Morgan, A. Grable, P. S. Soltis & R. Kuzoff. 1993. Molecular systematics of i ceae ribosomal DNA sequences. Ann. Missou 1-49. » — ——, M. W. Chase, M. E. Mort, D. C. Albach, M. Zanis, V. Savolainen, W. H. Hahn, S. B. Hoot, . Fay, M. Axtell, S. M. Swensen, L. M. Prince, W. J. Kress, K. C. Nixon & J. S. Farris. 2000. Angiosperm rios inferred from 18S rDNA, rbcL and atpB sequences. Bot. J. Li Soc. 133: 38 . K. Endress & M. W. Chase. 2005. Phy ad Evolution of Angiosperms. Sinauer Asso- ciates, K Massachusetts. —.. Gitzendanner & é ks Soltis. 2007. A 567- taxon a set for angiosperms: The challenges posed by Bayesian analyses of large dun sets. Int. J. Pl. Sci. 168: 137-157. APPENDIX 1. Voucher information n the ule ont pa F F. 2009. Angiosperms phylogeny website, , version d 24 March 2010. Sun, Y., D. Z. Skinner, G. H. Liang & S. H. Hulbert. 1994. Phylogenetic analysis of Siphon and related taxa m intern y transcribed spacer of nuclear ribosomal D Appl. Genet. 89: 26-32. Swofford, D. L. 2000. PAUP: Phylogenetic Analysis Using Parsimony, Vers. 4 beta3. Sinauer Associates, Sunderland, Massachusetts. Thorne, R. F. 1999. The classification and a dicia of 2 flowering plum Dicotyledons of the class Angiosperma (s s Magnoliidae, Ranunculidae, Caryophyllidae, Dillenidae, Rosidae, Asteridae, and Lamiidae). Bot. Rev —641. EM T. & H. Tobe. 2006. Phylogenetic analyses of on using plastid and nuclear DNA ences, e. ar reference to the me of Euphorbia- ceae sens. i. J. Pl. Res. 119: 5' rere : Y. S. R. Makes B. T. Tas W. Zhang & C. . 2005. Phylogeny, biogeography, and aud ding al cornelian cherries (Cornus, Cornaceae)—Track- ing Tertiary plant migration. Eiai 59: 1685-1700. 140 = P S = silica, H = herbarium), and GenBank accessi umbers u are deposited at the Royal Botanic Gardens, Kew (K), de Missouri Monica Garden (MO), and in le € wu sq of Morton (*). Taxon Specimen Voucher rbcL ITS Family Balanopaceae Balanops vieillardi Baill. G Litt & Chase, 1999 AF089760 Family Chrysobalanaceae Acioa d E S Rio de Janeiro, Brazil, Prance 30841 (K) MR GQ424453 Atuna racemosa Raf. subsp. racemosa S Bogor, Indonesia, Morton 89 (* Q424454 Bafodeya benna n Elliot) Prance S Guinea, West Africa, Col M. Saiden s.n., een GQ424455 ex F. White 1997 (K) Chrysobalanus icaco L. S Bogor, Indonesia, Morton 64 (*) GQ424476 C. icaco S Dominican Republie, Prance 30833 (K) GQ424456 Couepia obovata Ducke S French Guiana, D. Sabatier & GQ424477 M. F. Prevost 3125 (MO) C. parillo DC. S Reserva Flo cke, Brazil, R. C. GQ424457 Forzza 305 (MO C. robust G Litt & Chase, 1999 AF089757 elena s (Baill.) Prance H Gabon, McPherson 16317 (K) GQ424478 GQ424458 e Ellon m EN Prance S Brazil, Hopkins & m—€— 1209 (K) GQ424479 GQ424459 Crangeria H Madagascar, ma 61 (K) GQ424480 GQ424460 Hirtella ida uud & T G Litt & Chase 0897: H. triandra Sw. S Dominican tendi S. R. Hill 29095 (K) GQ424481 GQ424461 Hunga gerontogea (Schltr.) Prance H w ia, McPherson 6093 (MO) GQ424482. GQ424462 Kostermanthus robustus Prance S Sarawak, oo Morton tree1099 (K) GQ424483 GQ424463 Licania tomentosa (Benth.) Fritsch S Bogor, Indonesia, Morton 97 (*) G M. butayei De Wild. H Zaire, Africa, T. B. Hart 1362 (K) GQ424465 M. conrauana Engl. H Cameroon, Africa, A. J. M. Leeuwenberg 60424485 9572 (K) Maranthes glabra (Oliv.) Prance S Cameroon, Africa, J. J. Bos 7352 (K) GQ424486 | GQ424466 Neocarya macrophylla (Sabine) Prance — S Senegal, Dakar, Goudiaby & Sambou, GQ424487 — GQ424467 ex F. White 1998 Parinari sumatrana (Jack) Benth. S Bogor, Indonesia, Morton 134 (*) GQ424488 — GQ424468 Family Connaraceae Connarus conchocarpus F. Muell. € Ferando et al., 1993 L29495 ESI r LES Volume 97, Number 2 Yakandawala et al. 277 2010 ylogenetic Ph Relationships of Chrysobalanaceae APPENDIX ]. Continued. Taxon Specimen Voucher rbcL ITS Family Cornaceae Cornus eydeana Q. Y. Xiang & G Xiang et al., 2005 AY243874 Y. M. Shui Family Dichapetalaceae Dichapetalum — Chodat G Savolainen et al., 1994 X69733 D. macrocarpum G Litt & Chase, 1999 AF089764 D. rugosum (Vahl) To S Brazil, Spruce 623 (K) 4469 G0424451 apura amazonica Poepp. & Endl. G Litt & Chase, 1 AF089763 T. fischeri Engl. H Lowveld Botanical Garden, South GQ424471 Africa, Prance 30831 (K) Family Euphorbiaceae Androstachys johnsonii Prain G Savolainen et al., 2000 AJ402922 Tetracoccus dioicus G Davis et al., 2005 AY788190 Family Euphroniaceae Euphronia guianensis (R. H. Schomb.) S Bolívar, Venezuela, Berry et al. 60424470 60424452 i 6562 (MO) Family Ochnaceae Ochna serrulata (Hochst.) Walp. G Fay et al., 1997 Z75275 Family Polygalaceae Comesperma ericinum DC. G Fernando et al., 1993 129492 Family Rosaceae Spiraea vanhouttei (Briot) Carrière G Morgan & Soltis, 1993 L11206 Family Stylobasiaceae Stylobasium australe (Hook.) Prance G Fernando et al., 1993 U07679 S. T m Desf. G Soltis et al., 1993 U06828 Cadellia erii F. Muell. Fernando et al., 1993 129491 Guilfoyli n monostylis F. Muell. c Fernando et al., 1993 129494 Š ritima L. G Fernando et al., 1993 U07680 Family Trigoniaceae Trigonia eriosperma (Lam.) Fromm S Rio de Janeiro, Brazil, Prance 30842 (K) 6424472 & E. Santos i from herbarium APPENDIX 2. Taxon and voucher information used in the leaf morphology study. All material used are " I specimens deposited at the Royal Botanic Gardens, Kew (K). Voucher Taxon s o des SS Family Chrysobalanaceae n M schultesii Maguire end Malay, "dien FRI 8202 una “spa as Kosterm. A. racemosa [Indonesia] Malay, Johor FRI eH Guinea, Col. M. Saiden s.n. 1997 Me in (Scott-Elliot) Prance ex F. White on le cio s enezuel 536 k venezuelansus Couepia guianensis Aubl. : C. magnolüfolia Benth. ex Hook. f. Brazil, Cambell DC. 278 Annals of the Missouri Botanical Garden APPENDIX 2. Continued. Taxon Voucher uatrec. Costa Rica, Gerardo Herrera 5375 C. uiti (Mart. & Zucc.) Benth. ex Hook. f. Brazil, 3081 ladenia gilletii (De Wild.) Prance & F. White Gabon, McPherson 03-28-1992 D. letestui (Let ) Prance & F. n, Breteler 1646 D. scabrifolia (Hua) Prance & F. White Guiana, Brown 2627 D. whytei (Stapf) Prance & F. White Sierra Leone, Deighton 5104 ndron ke) Prance Guyana, Jacobs 192. E. coriaceum (Benth.) Prance Guyana, Maas 7601 i ; Mauritius, Bosser 21872 G. porosa Boivin ex Baill. ar, Phillipson 1909 Hirtella bullata Ben Guyana, Henkel 251 H. gracilipes (Hook. f.) Prance Brazil, Harley 21649 H. pilosissima Mart. & Zucc Brazil, Thomas 4 H. minutiflora (Baker f.) Prance H. myrsinoides (Schltr.) Prance L dub Hook. E L. discolor Pi L. bomb Benth. L sclerophylla (Mart. ex Hook. f.) Fritsch L. sprucei (Hook. f.) Fritsch Licania subg. Moquilea (Aubl.) Prance L. arborea Seem L. pawaqta Puesta L. michauxii Prance L. unguiculata Prance B Mozambique, Finley 2178 New Caledonia, North Province, Mackee 19 New Caledonia, North Province. Mackee 17561 New Caledonia, North Province, Mackee 23803 New Caledonia, North Province, Mackee 29322 [Indonesia] pa Cockburn FRI 7966 Brunei, Coode 7 Nicaragua, Moreno E Guiana, Clarke 53. Guiana, Jacobs 198 i Guiana, Mutuhnick 747 uiana, Pipoly 9640 French on Wachendeims 141 Brazil, Almeida 275 Brazil, Dick 139 Venezuela, Aymard 6393 , Sothers 690 Guiana, Cremer. Brazil, Millikein 0 A 1988 French Guyan ana, Hoffman 1183 Brazil, Ferreira 7460 Brazil, Ribeiro 1168 Brazil, Prance 14158 Brazil, Pereira 2839 Guyana, Henkal 5135 Nicaragua, Moreno 22875 Florida, [Brazil] Ducke Reserve, Vicentini A. 746 Volume 97, Number 2 2010 Yakandawala et al. Chrysobalanaceae APPENDIX 2. Continued. Taxon Voucher Licania subg. Parinariopsis Huber L. licanüflora (Sagot) S. F. Blake Brazil, Oldeman, 10 June 1966 Licania subg. Angelesia (Korth.) Prance & F. White L. splendens (Korth.) Prance [Indonesia] Malaysia, Ridley 261 Licania subg. Afrolicania (Mildbr.) F. White & Prance L. elaeosperma (Mildbr.) Prance & F. White Magnistipula Engl. subg. Magnistipula M. butayei De Wild. M. sapinii De Wild. Magnistipula subg. Pellegriniella (Hauman) Prance M. tessmannii (Engl.) Prance Magnistipula subg. Tolmiella F. White Magnistipula e t F. White Maranthes corymbosa M. floribunda (Baker) T "White M. glabra (Oliv.) Prance M. kerstingii (Engl.) Prance ex F. White Neocarya macrophylla (Sabine) d ex F. daten Parastemon urophyllus (Wall. ex A. DC.) A e bl. P. oblongifolia Hook. f. P. sprucei Hook. f. dem Dichapetalaceae um albidium A. Chev. ex Pellegr. C .) Boerl. nopodium Make Baill. in Mart. S. costaricense Prance = estrellense Baill. in Mart. T. capitulifera Baill. T. coriacea J. F. Macbr. T. fischeri T. guianensis Aubl. Cameroon, De Wilde & de Wilde-Duyfjes 1850 Tanzania, Boaler 643 Congo Republic, Lisowski et al. 13220 Gabon, Wilks 1572 Madagascar, Schatz 3329 Philippines, d & Baquiran ISV 489 | 5425 Ivory Coast [Cóte pm Oldeman 857 hapman 4082 , Kosterman [Fiji] Rotuma Island, John 19168 Brazil, Rabelo 3555 lo 3 Malaysia, Kochummen 78747 il, Kawasaki 220 Sierra Leone, Thomas 3173 j 2470 British Guiana, JB 522, 4 Mar. 1953 Brazil, Ferreira et al. 10853 Zaire, Van der Ben 1326 Suriname, Lindeman et al. 566 Annals of the Missouri Botanical Garden APPENDIX 3. W bsa A + ER ] aL morphological analysis of Chrysobalanaceae. The data matrix with 50 binary multistate cuca for xm bod taxa intend in i ki se is given in Table 2 @ the sd Wie (UB and am m agrenca vith the Chappil (1992) matrix. El the tribal descriptions of Prance and White (1988). 1. Lamina glands: Lamina glands occur in almost all species and were scored as absent — 0 or prese of species of Parinari possess two als glands several small or submarginal glands, so this character was scored as present for Parinari. 2. Leaf papillae: Leaf papillae on veins were coded as absent = 0 or present = 1. The majori es of and Couepia do not possess leaf podes da this feature was scored as absent for these genera. 3. Stomatal crypts: The veins on the abaxial surface of specimens are extremely prominent and form a dense p t = 1. nari contain — crypts; this feature was coded as present for the ge 4. Leaf trichomes: Tric lios on leaves were scored as absent — 0 or present — 1. gs hairs = unicellular and simple (Prance, 1972). In Exellodendron, and Maranthes, they are ja, they are either straight r strigose and setose (Pran nce ys White, 1988). uo ‘though the family contains g are not available. This character was coded as absent or present A this study. Only a few species of Magnistipula richomes, therefore m» fest was coded as n Li Aca nia sub: White & Prance, the trichomes are sometimes. present in young — which become glabrous very soon; therefore, this feature was coded as absent. 5. Epidermal cells: Non-mucilaginous — 0; mucilaginous =1 s $i 6. Silica bodies in the ME n membranes are univ silica bodies in the epidermal cells and surnuading the leaf I L a 1972). This feature was scored as absent = or present — 1. s a some arinari, the stipules reach a length of 7 cm In Atuna, t eren keeled t unique feature in the family. olar stipules occur i s and some species ' Licania and Magnistipula. In r Magnistipula and in L. latisti ce, the stipules are lateral and foliaceous. In Magnistipula zenkeri P are imes up to 5 cm long and inflated. Although ms to be a n in the a abse present in this study due to the difficulty in in observing them in ium sss mens majority of species of Hunga possess stipules, the character is as t f e genus. According to de are present and caducous. The character has been scored as present for Chrysobalanus. 9. Bracts: bm E. Mii bracts and bracteoles cannot alwa; specimens. Therefore, ts and ‘racteles meh huie been scored as bracts. ee = 0; present = 1. 10. Bract size: Bracts and bracteoles are usually small, but in a few species they are relatively large and enclose small groups of Leur Ten This character was scored as small = 0 or large ik. Baya hus = 0; present = 1. Most taxa have eglandular bracts and bracteoles, wi in several species se the majority of speci Magnistipula, and Couepia lack alas the diis was scored as absent for these gene 12. Receptacle tube: Aer = = 0; present = 1. 13. Sepals: Acute = 0; obtuse = 1: round = 2 *14. Sepal shape: Equal rx smelt unequal = 2. 15. Petals: Absent = 0; pr 16. Petal length: Shorter i dad "e. calyx = 0; equaling the calyx = 1; longer than the calyx 17. Receptacle hairs: Absent = io prese 18. Receptacle hairs: Hairs on the inner ae of the e ee can be present at mouth = 0 or throughout the interi *19. e tube length: Shorter than calyx — equal to calyx = 1; longer than calyx = 2. The length of E ube was determined in vits to the calyx and, Couepi e shorter than ii most of the genera could be coded into discrete sta *20. Floral symmetry: aine = NA slightly zygomorphic = 1; strongly zygomorphic = 2. The floral try can be “wan ibed as eii (apart from the biis style) to strongly zygomorphi 21. Sexual habit: Unisexual — 0: | »22. ose hairs in throat: A distinct feature of the receptacle ei is the t of retrose hairs at the throat, which was TK. *23. men number: The number of stamens varies from l 5 Licania, which has only a very few species with nine to 12 or 10 to 11 stamens, this t was coded as 10 o ess. In Acioa, Atuna, and Dactyladenia, the few species with a stamen number between 10 and 20. 10 and 25, and 10 and 75 have been scored as more than 11. 24. Filaments: Absent — 0; present — *25. Fertile stamen placement: When a the stamens are fertile, they form a complete or an almost complete circle around the entrance to the flower. In the case with the presence of staminodes, the fertile stamens are et red as saca | complete circle = 0 or eii opposite Ma ca = E +26. Plenus ie Los The length of a filaments can dp from much shorter than the — = 0, as long as the e 1, or longer than the calyx = *27. Filament union: E a majority of ge the filaments are free or united at the base for less ion 1/3 of their length. In the case of the ree genera that have e ~ more -— 13 of their length, the union inal ligule. In the case of Punic. de sn hide is Te exserted and much longer Volume 97, Number 2 2010 than the combined length of the calyx and receptacle tube. In Acioa — Prance, a dubious species in the genus, the filaments free. However, because = majority is ligulately te this character has been scored at the ited more than 1/3 de length ~ a set. Filaments free = 1 united at base — 1; more than 1/3 its length — 28. Filament hairs: ¡renta = 0; present = 1. *29. Filaments in bud: In those genera with far-exserted stamens, the filaments are coiled in the bud. In a few — they are slightly undulate. This feature was scored as coiled — 0, u ndulate = 1, or coi 2 *30. es: Staminodes may be absent = 0 or = 1. Because the genus Acioa has rudimentary scored as base of i — 0, lateral — 1, or mouth of the receptacle t tube — 2. In most species of Hirtella, the ovary is inserted at a en of de — tube; therefore, it has been sco ptacle tube for the genus » = ete The “ovary. is unilocular, but in some This fea is scored as uni lecular = 0, Y toe = = ya true bilocular = trilocular = 33. Ovary Lex Pium = 34. Stigma: = stigma may de deni dba" Med = 0; presen 36. Gynobasic na : Absent — 0; p 37. Drupe: The fruit is a drupe, iN en can ke deis 0 or = | 38. Epicarp: Smooth = 0; rough = 39. Endocarp surface: ie > Tou = E 40. Endocarp interior: go — 0; hairy 41. Germination: Germination has been sedi :à in 12 genera (Prance, 1972, and lares therein) and provides useful taxonomic characters, especially for generic delimi- tation. The character was coded as lar = 0 or lar = 1 apt Duke (1965, Po scale leaves : beds can be absent — 0 or prese 43. First sek of cenis De Ben s. leaves with green, cpanded ista n =1. 44. Rays: Uniseriate = = 0; biseriate 45. Primary vein size: Primary x vein size was determined veut foliage width (vw) a wih) al ened os ve 100%. = 0;= s cas es cs ds dde secondary ve Angle 45° = 0; angle = 46° = 1. 47. Sec veins—variation in angle divergence: Variation in the angle of divergence can be uniform or nonuniform with upper more acute than lower or upper more than lower. This was scored as uniform = 0, nonuniform type E = 1, and nonuniform type 2 — 2. 48. course: The radiation pattern of he some sec „o paa such as the Neocarya type. For type 3, the ns turn up very close to the ca the division of de secondary veins that joi adjacent secondary veins is obscure. Type 1 "Q pp = 1; type 3 = 2. 49. Tertiary vein pattern: Parallel = 0; reticulate = 1. 50. Areoles: hen oe gia SUITO! by veins, which, taken t form conti field over most of the area of the leaf. ‘ieee = 0; well developed = 1. en RE EE ee A DN S. I Jue, thin A Volume 97, Number 2, pp. 141—282 of ANNALS oF THE Missouri BOTANICAL GARDEN was published on 9 July 2010. www.mbgpress. org CONTENTS A Revision of Deschampsia, Avenella, and Vahlodea (Poaceae, Poeae, Airinae) in South America Jorge Chiapella & Fernando O. Zuloaga A Taxonomic Revision of Rhododendron subg. Tsutsusi sect. Brachycalyx (Ericaceae) : a Jin Xiao-Feng, Ding Bing-Yang, Zhang Yue-Jiao & Hong De-Yuan Mulectiles Pi EL Character Evolution, and Suprageneric Classification of Lamioi- deae (Lamiaceae) Anne-Cathrine Scheen, Mika Bendiksby, Olof Ryding, re E ue Mur A. Albert & Charlotte Lindqvist Revision of the Asian Genus Koil P. C. van Welzen Origin, Diversification, and Cied of the Australasian Genus Dracophyllum (Richeeae, Ericaceae) Steven J. Wagstaff, Murray I. Dawson, Stephanus Venter, L Jéróme Munzinger, Darren M. Crayn, Dorothy A. Steane & Kristina L. Lemson Phyjopenetie Relationships of the Chrysobalanaceae Inferred from Chloroplast, Nuclear, and Morphological Data.. Deepthi Yakandawala, Cynthia M. Morton & Ghillean T. Prance pnl > A — 63 191 218 Cover illustration. Ginoria pulchra (Ekman & O. C. Schmidt) S. A. Graham, drawn by | Taciana Cavalcanti. Annals of the Missouri. Botanical Garden 20 MO * y Volume 97, Number 3 October 2010 Annals of the Missouri Botanical Garden | The Annals, published quarterly, contains e papers, primarily in systematic botany, tributed from the Missouri Botanical Garden, St. Louis Papers originating outside Í the Garden willalso be accepted. All ide are peer-reviewed by qualified, in- | px ee aie. Equina: to Authors are printed in the back of the last issue are also available online at www. mbgpress.org. | a Mieloris: € Hollovell Scientific Editor, : Missouri Botanical Garden | Beth Parada : Managing Editor, Missouri Botanical Allison M. Brock ' Associate Editor, Missouri Botanical Garden Tammy Charron Associate Editor, Missouri Botanical Garden Cirri Moran Press Coordinator, Missouri Botanical Garden x Charlotte Taylor E Roy! E. Gereau Misiles Botanical Garden Ihsan A. Al-Shehbaz Missouri Botanical Gert Davidse — . . Missouri Botanical Garden | Peter Goldblatt — | Missouri Botanical Garden Gordon McPherson : Missouri Botanical Garden Missouri Botanical pS Henk van der Werff - Missouri Botanical Garden For subscription information contact ANNALS oF THE Missouri BoranicaL GARDEN, % Allen Mar- keting € Management, P.O. Box 1897, Lawrence, KS 66044-8897. Subscription price for 2010 is $180 per volume U.S., $190 Canada & Mexico, $215 all other countries. Four issues per volume, The journal Novon is included in the subscription price of the Anna it 2 M (editorial queries) http://www.mbgpress.org Te J. L y 1/ he AGRICOLA (through 1 THE ANNALS OF THE Missouri BOTANICAL GARDEN (ISSN 0026-6493) is published quarterly by the Missouri Botanical Garden, 2345 Tower Grove Avenue, St. Louis, MO 63110. Periodicals post- age paid at St. Louis, MO and additional mail- ing offices. PoSTMASTER: Send address changes to ANNALS OF THE Missourt BOTANICAL GARDEN, % Allen Marketing & Management, P.O. Box 1897, Lawrence, KS 66044-8897. 994 . stract/Global Health en ingenta, ISIG databases, JST OR, Research Alert®, and e The full-text of ANNALS OF THE Missouri Botanica Garpen i is available online though BioOne™ (http:// | -© Missouri E ERE EE Rew Sib v " d eL Noui Bud Garden i is Lie iei sel share kom about plants and ` oA >. i their environment, in ), APT Online, BIOSIS®, CAB Ab- | Sci Search®. Volume 97 Annals Number 3 of the Y 2010 omnea Missouri \SSOUR! M ms Botanical GARDEN LIBRARY, Garden A FLORISTIC STUDY OF THE Paul V. A. Fine,?* Roosevelt García-Villacorta,** WHITE-SAND FORESTS OF PERU! Nigel C. A. Pitman,” Italo Mesones,° and Steven W. Kembel” - ABSTRACT Tropical forests occurring on white-sand soils have a inde structure and are famous = p p Yet, no — floristic study has ever been undertaken in white-sand “sas P in the western À e present the results of floristic inventories from 16 plots in ME sites bon the Feruvimn Amaron te ep. diversity, species composition, and endemism in dca pa ests fertile soils in the same region. We found that white-sand Soma pee have ete n" donee species cad (41.5 species per 0.1-ha plot) and that white-sand plots y s. We classify 114 A species: as endemic to to whit tes and, with another 21 sp ies that can b idered facultative sp ts or cr ypt ic en emics iai [4 na 02C;. fH ] 1 , Ë X c b text of the role of | heterogeneity Co amerad i in white-sand forest t plote. W patterns of species oe and the contain of Amazonian forests. Key words: Am bet ted caatinga, edaphic specialization, endemic species, habitat specialists, heath forests, tropical tree A denis vari ' This paper is dedicated to the ge of Alwyn H. Gentry, whose work inspired this study. We thank the Dirección General de Areas Naturales Protegidas y Fauna Silyestre INRENA, which provided necessary permits for study, collection, and exportation of specime ns; D. Del Castilla, E d E. Rengifo, and * Te Ho st me huerto bos jaypatigacionos. de la nía Peruan l (HA AP) fi £ GEI EE de Investigación Jenaro H sit ities of Tierra Blanca, Tamshiyacu, and Jeberos fo or permission to work near ar thcir villages; S. gue Don Monn > bao, and F. Yanik for field pecan’: | H. Mogollón, N. Deri la, » Rios LG M. Ahui uite. D. Cardenas, P. Núñez and E. Valderr: rrama for their extensive gI tsin the nén-whüe- sand plots d di in n ibus pe paper; C. Bode for help with the figures; and S. Brewer and C. V for n hi peris analyses. We thank P.D. Coley for iine during all stages of this "s A Álvarez Alonso bu continually red guidance and helped us to visit many of the field sites. This research was supported by grants DEB 02069196 (co- principal investigator P. D. Coley) and OISE | 0402061 t P. V.A.F. br the National Š Science ain. N. C. -A- P^ work was Biological Fraaie rogram, with support from T n and Betty Moore Foundatio nt of lisi Biology, — E California, Berkeley, California 94720, U.S.A - * Department of Ecology and Evoluti Biology, pee of Michigan, Ann Arbor, Michinan 48109, U.S.A. *Facultad de Ciencias Biológicas, Dasdi Naci: e la Amazonía Peruana, Iquitos, Peru. NE for Tropical Conservation, T cholas School of the Environment and Earth Sciences, Box 90381, Duke University, North Carolina 27708, U.S. * Facultad de Ciencias Faessen Taiversiad Nacional. de x MAMMA, Peruana, voe Peru. " Department of Integrative Biology, Uni U.S.A. Current address: aes for es & pet Biology "32s Pacific Hall, pe "a T reos, Eugene, Oregon 97403-5289, U for correspondence: paulfineGberkeley.ed Pre 10.3417/2008068 e Ann. Missouri Bor. Garp. 97: 283-305. PusuisHeD on 10 October 2010. Annals of the Missouri Botanical Garden The observation that white-sand soils in the Amazon basin support distinctive forest formations has long been noted (Spruce, 1908). White-sand forests have a shorter canopy, a brighter understory, and often a thicker layer of humus than the arch rainforest that is found on other terra firme soils (Anderson, 1981; Medina & Cuevas, 1989) In addition, white-sand forests are ted to harbor many edaphic endemic plants (Ducke & Black, 1953; Anderson, 1981; Gentry, 1986). White-sand soils cover approximately 3% of the Amazon Basin and are most common in the Rio Negro Basin of Venezuela and Brazil as well as in the Guianas (ter Steege et al., 2000). However, small patches of white sand occur as far west as the Andes in Peru, contributing to the mosaic of heterogenous habitats found in the western Amazon (Tuomisto et al., 1995; Fine et al., 2005). Gentry (1981, 1986 extraordinarily high diversity of the Amazon Basin, and as one example he cited the low overlap in species composition between white-sand and other terra firme forest types near Iquitos, Peru. Despite the attention white-sand forests hav. received in Peru as the cause célébre for specialization, very few floristic studies of white-sand forests in Peru have been published, and all have been near Iquitos. For example, Gentry (1986) published only the species richness numbers from a comparison of three 0.1-ha white-sand transects with transects from other soil types. Most other studies have generally focused on one plant clade (Melasto- mataceae or Burseraceae or Pteridophyta) in the region and whether their species composition patterns correlate with many different environmental variables (including but not limited to white sand) (Tuomisto et al., 1995, 2003; Ruokolainen et al., 1997; Ruokolai- nen & Tuomisto, 1998; Tuomisto & Poulsen, 2000; Fine et al., 2005). Ruokolainen and Tuomisto (1998) inventoried all trees in three white-sand plots (ca. 0.1 ha) and published the plot data as an appendix. The most detailed published survey of white-sand plants from Peru was published by García-Villacorta et al. (2003), in which they attempted to classify different types of white-sand forest using species composition, canopy height, and soil drainage in the Allpahuayo-Mishana National Reserve near Iquitos. Here, we present floristic data on seven geograph- ically separated white-sand forests in Peru in order to extend available information on its white-sand flora. The objectives of the present contribution are to provide preliminary answers to the following ques- tions: (1) How diverse are the white-sand forests of Peru? What are the most common species? Are Peruvian white-sand forests separated by hundreds of kilometers similar in composition to one another? (2) How much overlap in species composition is there between Peruvian white-sand an forest plots? How many white-sand species are endemic to white-sand forests? (3) How do Peruvian white-sand forests compare to other white-sand forests described from Colombia, Venezuela, Brazil, and the Guianas? METHODS WHITE-SAND FOREST INVENTORIES From 2001 to 2004, we conducted inventories of 16 white-sand (WS) forest plots in seven geographical locations in the state of Loreto, Peru (Table 1, Fig. 1). Because WS forests are structurally so much smaller than terra firme (TF) forests, it was necessary to modify standard sampling methods developed for TF forests to obtain representative samples of WS forests. Most inventories of TF rainforests in the past few decades have been conducted at the scale of 1 ha, with a minimum DBH cutoff of 10 cm. This protocol allows researchers to sample all of the reproductive trees of the midcanopy and canopy and most of the understory tree species. In WS forests, trees grow very slowly yet reach reproductive size with trunks smaller than 10 cm DBH (and in the extremely stunted forests, the great majority of individuals will never approach 10 cm DBH), thus a smaller cutoff is necessary to sample all reproductive adults. Another discrepancy is that some WS patches are smaller than 1 ha. To overcome these limitations, we sampled WS forests in two different ways, trying to sample comparable numbers of individuals as the TF plots. For varillales (García-Villacorta et al, 2003) (also known as caatinga forest [Anderson, 1981] or tall caatinga [Coomes € Grubb, 1996], which consisted of forests with canopies at approximately 10-20 m (N — 13), 0.1-ha plots were used with DBH cutoffs of 5 em to obtain a sample of approximately 300 individuals per plot. Three of the WS plots (WS 6, 10, and 15 in Fig. 1) were located in chamizal (or caatinga scrub [Anderson, 1981]) and consisted of stunted forest, with 99% of the trees less than 10 m tall and most around 5 m in height. To obtain a representative sample in these forests, we surveyed plots of 10 X 25 m (0.025 ha) and inventoried all stems larger than 2.5 cm DBH. Representatives of all species encountered were collected at each site, and voucher specimens are deposited in the Field Museum of Natural History Herbarium in Chicago, Illinois (F), and the Herbario Amazonense (AMAZ) at the Universidad Nacional de la Amazonía Peruana in Iquitos, Peru (see Appendix 1 TE V SSES FE ea tanien us PEN RN uod UR A Volume 97, Number 3 Fine e Study P: Vil dd Forests of Peru Table 1. The sites listed in Figure 1, with the plot codes for each site, the coordinates, habitat, and collectors. Site Plot code Lat DD Lon DD Collectors' Apayacu TF 1 —3.11667 "72.171250 N. Pitman, I. Mesones, M. Ríos Buenavista TF 2 —4.83444 — 72.39028 N. Pitman, R. García, H. Beltran, C. Vriesendorp Curacinha TF 3 —5.05139 - 72.12633 N. Pitman, R. García, H. Beltran, C. U Vriesendorp Curaray TF 4 —2.31869 —74.09147 N. Pitman, Ki García, H. Mogollón, P. Nuñez Ingano Llacta TF 5 —1.86953 —74.66778 N. Pitman, R. García, H. Mogollón, P. Nuñez Maronal TF 6 —2.96564 —12.12786 N. Pitman, I. Mesones, M. Ríos Nauta TE Z —4.44274 —73.61083 M. Abate, E. in TF 8 — 3.62464 —12.24260 M. Ríos, N. Dávil PV7.polvorin TF 9. j —15.21472 N. Pitman, R. (uen. H. Mogollón, P. Nuñez PV7.terrace TF 10 —0.87516 —75.20561 N. Pitman, R. García, H. Mogollón, P. Nuñez Quebrado Blanco 1 TF 11 —4.35911 —73.15894 M. Ríos, N. Dávila Quebrado Blanco 2 TF 12 —4.35928 —73.15728 M. Rios, N. Davila Sabalillo TF 13 — 3.333533 1231011 E. Valderrama, M. Ahuite San Jose TF 14 —2.51064 —73.66072 M. Ríos, N. Dávila Santa Maria TF 15 —1.41603 — 74.61650 N. Pi R. García, H. Mogollón, P. Nuñez a Te TF 16 —2.82572 B. M. Ríos, N. Dávila Vencedores TF 17 “1.138729 —75.01842 N. Pump, R. García, H. Mogollón, P. Nuñez Yaguas TF 18 = —71.41503 M. Ríos, N. Dávila . WS 1 —3.95611 —73.42861 I. Mesones (P. Fine, R. Garcia) Allpahuayo-Mishana WS 2 —3.95056 —73.40000 I. Mesones (P. Fine, R. García) Allpahuayo-Mishana WS 3 3.947 —73.41167 I. Mesones (P. Fine, R. Garcia) ih WS 4 —3.94167 —73.43889 I. Mesones (P. Fine, R. Garcia) Upper Nanay (chamizal) WS5 —3.74083 —14.12222 P. Fine, I. Mesones (R. García) Upper Nanay WS6 —3.74139 —74.13278 P. Fine, L Mesones (R. García) Jeberos WS7 -5 — 76.26667 P. Fine, I. Mesones (R. García) Jenaro Herrera WS8 —4.85000 —73.60000 P. Fine, I. Mesones, R. Garcia Jenaro Herrera WS 9 —4.85000 — 73.60000 P. Fine, I. Mesones, R. García Jenaro Herrera (chamizal) WS 10 4.85000 —73.60000 P. Fine, I. Mesones, R. García Moron: WS 11 —4.26667 —11.23333 P. Fine, I. Mesones (R. García) Morona WS 12 — 4.26667 — 1123333 P. Fine, I nes (R. García) Tamshiyacu WS 13 —3.98333 — 73.06667 P. Fine, I. Mesones (R. García) hiyacu WS 14 —3.98333 — 73.06667 P. Fine, I. Mesones (R. García) Tamshiyacu (chamizal) WS 15 —3.98333 — 73.06667 P. Fine, I. Mesones (R. García) Matsés WS 16 —5.85500 — 73.75400 P. Fine, N. Dávila, I. Mesones ! Persons in parentheses checked over a collected material, but were not present during field collection. All white-sand collections were ultimately ee by lata determined by N. P for collection numbers). Voucher specimens were identified by comparing them to specimens from the above two herbaria and the Missouri Botanical Garden (MO). A very few specimens were also identified at the New York Botanical Garden (NY). Specimens that were unable to be matched were left as pe- cies” and are presented with their genus name and morphospecies number (or if genus is unknown, the family and morphospecies number; see Appendix 1). COMPARING WS PLOTS TO OTHER TF PLOTS Pitman and colleagues provided data for 18 plots from Loreto, Peru (Fig. 1, Table 1; Pitman et al., 2008). These plots are 1-ha tree inventories (10 cm Fine, R. García, and I. Mesones, and all non-white-sand collections were DBH) of 18 TF sites, and none of them sample WS forests. Although still a work in progress, these plots allow for a reasonable comparison of species overlap between WS and other non-WS TF soil types. These TF plots contained 1750 species and morphospecies out of 10,867 individuals and averaged 251.7 species r plot. Two similarity matrices were constructed to compare the 34 plots. The first, B; — a'; / a'; * min(b';, c';, where a' is the number of species in common between two plots, b' is the species only in the neighboring plot, c' is the species only in the focal plot, and min means one chooses the smaller of the two numbers in parentheses (Lennon et al., 2001). This equation includes only the presence/absence Annals of the Missouri Botanical Garden Figure l. A map showing the locations of the white-sand (triangles, labeled TF 1 to 18) in northeastern Peru. Rivers A 2 d are dra with the exception of WS 1 to 4, which details data and is lifted S * t dos si saa account the differences in diversity between plots with the aim to decrease the influence that any local species richness has on dissimilarity. The second index that we used is the Steinhaus similariy" index. It is calculated as: between plots A and B — 2 X min ^. n" E (n^ + n") where one chooses the smaller number of overlapping individuals between plot A and B. doubles that number, and divides by the total number of individuals in the two plots (Potts et al.. 2002). Because WS plots are generally composed of a small number of fairly dominant species relative to TF plots, the Steinhaus index is likely to more accurately reflect similarity and differences between all of the plots, voy if the same species dominate different WS plots. To compare WS plots to each other and to the non- WS plots, we collated all plot lists into a single data file. Both the second and third authors have collected specimens in the field and identified specimens from both databases in the herbarium (see Table 1), and thus it is highly unlikely that more than a very few TF plots (gray shapes, labeled WS 1 to 16) and the terra firme plots are labeled in italics. Dashed line M the limit of the — sea level). White-sand areas € apad on this map ar o approximate their extent on the lan of those known in the scape (modified from Vriesendorp et al., 2006), the boundaries of the [e demi ci National Reserve of which approximately 25% of its area is covered by white-sand forests). See Table 1 1 for names and coordinates of all plots morphospecies are the same as “named” WS species or WS morphospecies To quantify the sid component of beta diversity, we tested whether sites that were closer together in pace were more similar in terms of their e composition using Mantel tests e 1967). W calculated the geographical distan tween all sites and tested whether the two measures of species compositional dissimilarity mentioned above were correlated with the spatial opin separating sites. The Mantel test compares the observed correlation between these measures of pros with a null model based on randomization of dissimilarities among sites. We used 999 randomizations for each test. A — M ipai that the two distance ted E y chance. Both a and the Steinhaus belie te were converted to their d form for these analyses (Legendre & Legendre, 1998). These analyses were repeated for all sites and Sous for WS and TF plots. Nonmetric multidimensional scaling (NMS) ordina- tions were used to visualize the overall similarity in D ro i einen api nta crees at e AS Td Volume 97, Number 3 2010 Fine et a Study of ues Forests of Peru NMDS2 0.2 NMDS1 b) NMDS Presence-Absence NMDS2 T T T T -03 -02 -01 00 0.1 02 03 NMDS1 ndi > Some touitidimensional scaling on ordinations for vai dissimilarity as as nue by the species as measu and TF is group into two distinct clusters. species composition among all sites. We performed NMS ordinations separately on each of the two intersite dissimilarity matrices (B,jm and the Steinhaus index) using the vegan package (Oksanen et al., 2007) in the R statistical ve language (R Develop- ment Core Team, 2008). Both ordinations converged on a stable two-dimensional solution within so conducted a multi-response re (MRPP) test to determine r naa types than expected by chance (Mielke & Berry, 2001). The MRPP test compares the ratio of within- and among-habitat similarity to the ratio expected under a null model of 999 randomizations of site assignments to habitats. ResuLrs DIVERSITY AND ABUNDANCE OF INDIVIDUALS IN WS FORESTS We encountered 3631 individual trees in the 16 WS plots and separated them into 221 species and morphospecies (Appendix 1). The 13 varillal plots contained an average of 222 individuals from 41.5 species (range, 26 to 71). The three chamizal plots contained an average of 248 individuals from 14.3 species (range, 9 to 22). Even though chamizal plots were structurally very different in appearance than varillal plots, with canopies less half the height of varillal plots, chamizal plots were not composition- ally distinct from varillal plots, and the chamizal plots ). In both panels, WS did not cluster together in either ordination (Fig. 2). One clear example of close similarity of a varillal and a chamizal plot was at the Upper Nanay site, where all but one of the 12 species encountered in the chamizal plot was also present in the nearby varillal plot. The most common species overall was Pachira brevipes (A. Robyns) W. S. Alverson (Malvaceae), accounting for 606 individuals, an incredible 17% of all stems —— The top 10 species in the WS plots were all ve: mmon, accounting for more than 49% of the total individuals. Clusiaceae was the most important family in the WS plots; 890 individuals (24.5% of total) from seven species were encounte (Table 2). When considering the top 10 most common species from each of the seven sites, 17 of these occur in more than one site, and eight of them occur three times on the top 10 lists in different WS sites (Table SIMILARITY COMPARISONS WITHIN AND AMONG WS AND TF PLOTS Measures of similarity between a given WS plot and dance statistics, very similar to the average similarity measures between a given TF plot and another TF plot (Table 4). Yet, similarity between sigas given WS and TF plot averaged at 9% with nce/absence and Jo with abundance data (Table 4). The NMS ordinations clearly separated WS and TF plots into two distinct groups in terms of their species bo Annals of the Missouri Botanical Garden Table 2. The top 12 families in importance in the 16 white-sand plots, the number of species in each family, the L £ L b 2 2:3 tal 4 f 4h total stems overall. No. of No. of J of total Family! species individuals individuals Clusiaceae (CVB) 7 890 24.5 Malvaceae (s.1.) CV 3 613 16.9 Fabaceae (CVB) 30 13.3 Arecaceae (CV) 7 175 4.8 Sapotaceae (CVB) 13 168 4.6 Rubiaceae (B) 162 4.4 5 139 3.8 Elaeocarpaceae (C) 4 135 37 nnonaceae 87 2.4 Myrtaceae (VB) u 82 2.3 Euphorbiaceae CVB) T 78 2l Lauraceae (CV) 18 66 1.8 All others (35) 88 571 15.7 ! C, V, and B in parentheses indicate whether the family was on a list of top 12 families in white-sand forest in Colombia e Venezuela (V), or the top six in Brazil (B) (Caquetá, Colombia, Duivenvoorden et al, 2001; La Esme M Y enezuela, Coomes & Grubb, 1996; Manaus, Brazil, Anderson, 1981). composition, regardless of the index used to measure similarity among sites (B,,, and Steinhaus index) Fig. 2), a result further supported by the highly significant differences in species composition among habitats detected by the MRPP tests (Bj: A = 0.06989, P < 0.0001; Steinhaus: A = 0.08853, P < 0.0001). PATTERNS OF ENDEMISM IN WS FORESTS Of the 221 species in the WS data set, 141 do not occur in the TF data set (64%) and 80 of them (36%) do. However, it would be premature to label all of the species that do not occur in the TF data set as WS endemics, since the 18 TF plots are likely such a poor sample of all of the non-WS habitats in the western Amazon. Therefore, we compared our WS list to the published Ecuadorian flora (Catalogue of the Vascular Plants of Ecuador, Jorgensen & Léon-Yanez, 1999). S forests had never been reported in Ecuador at the time of publication of this flora (a few WS areas in Ecuador have been found near the Peruvian border in the Cordillera del Condor in the past few years; D Neill, pers. comm.), thus if a species from our WS list appears in the Catalogue of Ecuador, it should not be considered a WS endemic. We found 81 of the 221 WS species also occurred in Ecuador (36%). Defined in this way, the number of WS endemics (species that do not occur in either the TF data set or the Catalogue of Ecuador) becomes 114 species (52% of the total). re are an additional 21 species that we propose should be classified as “facultative specialists” or “cryptic endemics.” Eleven of these 21 are species that also do not occur in the Catalogue of Ecuador and occur more commonly in WS than in TF plots and also are found in fewer than four total plots in TF. We speculate that this group of species has source populations in WS forests and sink populations in TF forests. The other 10 species occur in multiple WS plots, are represented by more than 10 individuals in the WS data set, are represented by one or zero individuals in the TF data set, and also occur in the Catalogue of Ecuador. We speculate that this group of pate may include cryptic species or are otherwise genetically distinct from populations that occur in Ecuador. Three of these species (discussed below) are listed in the Catalogue of Ecuador but according to its text do not occur in the Amazon Basin, and thus the taxa found in our WS data set are ee to be new Taken together, the WS endemics and “asalini specialists” account en 135 of ihe 221 species (61%) found in the WS plots, and 3110 individuals (83% of the total). Spatial distance was correlated with species compositional d with both the presence/ absence and abundance data when all plots were analyzed with Mantel tests (B.jm: 73.8% of variation in original data explained by NMDS, P < 0.001; Steinhaus: 71.4% of variation in original data explained by NMDS, P < 0.001). This is not surprising, given that in general, WS and TF plots were not evenly distributed throughout the region, and indeed many of the plots of the same soil type were located within a few hundred meters of one another (Fig. 1). When correlating just the TF plots with spatial distance, Mantel tests using both the presence/ absence and abundance data yielded significant correlations (P < 0.015 and 0.006, respectively). owever, Mantel tests of the WS plots with spatial distance were only significant when using the abundance data (P < 0.023). The Mantel test within WS plots using the presence/absence data was not significant, indicating no correlation between species composition similarity and spatial distance. DISCUSSION PATTERNS OF DIVERSITY IN WS FORESTS WS plots in Peru contain a low species diversity compared to other TF forest plots. We found only 221 species out of 3631 individuals occurring in the WS plots. Moreover, our average plot diversity was 36.4 iilo iie adn dcs iun gai Volume 97, Number 3 2010 Fine et a Study of _ Forests of Peru species per plot, an extremely low number for lowland Amazonia. For comparison, Gentry's plots from Loreto the same area as Fig. l) were also 0.1 ha (bu included all stems greater than 2.5 DBH as well as shrubs); these plots contained an average of 172.7 species (range, 114 to 210 species) (Gentry, 1988; Phillips & Miller, 2002). Low diversity for WS plots has been reported in eastern and central Amazonia, with P sasa (1981) estimating 25 species at 10 cm DBH per hectare near Manaus, Brazil. In Venezuela, a 0.1-ha transect of WS forest had 35 species of 5 cm DBH (same DBH cutoff and plot size as our study) (Coomes & Grubb, 1996). In Guyana, 62 species per hectare of 10 cm DBH trees has been reported (ter Steege et al., 2000). Previous reports from near Iquitos claimed plot-level diversity totals of more than 100 species for WS sasa plots (Gentry, 1986; Ruokolainen & Tuo 1998; Philips & Miller, 2002). bien pi this diserepancy results from their plots covering more than one type of soil, as Gentry (1986) used narrow m belt transects, and Ruokolainen and Tuomisto (1998) report percent sand in their soil analyses at only 80% from their “white-sand” plots near Iquitos, and their species list lacks many of the dominan species from our WS data set. Preliminary soil texture data from our WS plots indicate consistent values of > 95% sand (Fine, unpublished data). M e DOMINANCE PATTERNS IN PERUVIAN AMAZONIA WS plots in Peru often have substantial overlap in species composition (Table 3), and this pattern holds whether one compares adjacent plots in the same forest, or WS forests as far apart as Jeberos and Allpahuayo-Mishana (Figs. 1, 2). Mese. out of the 40 species that appear on the 10 most common species list for each of the seven sites, 17 of them occur more than once, and eight of them occur three times on the top 10 lists in different WS sites (Table 3). These 17 species dominate the WS forest plots, accounting for an 62.4% of all individuals (Table 3). WS plots are T dominated y a cadre of species, and this dominance is likely the main factor driving the pattern of low plot-level diversity. Pitman et al. (2001) found a remarkable similarity of species composition between Yasuní and Manu, 2000 km apart. There were 42 were common in both = (stem densities of over one individual per hectare). He extrapolated this pattern as evidence be forests found on fertile clay soils throughout the western Amazon e and dominated by an were predictabl oligarchy of relatively common species. Pitman et al. mo further predicted that the oligarchic taxa from rn Amazonian clay forests would not be common in Ta of other soil types (indeed, only two of the most common 42 species from Yasuní and Manu even occur in our WS data set), and they concluded that: “... the oligarchic taxa will v region, and in cases of environmental heterogeneity from patch to patch, but the patches themselves may be largely homogeneous in composition and struc- ture.” In many ways, the WS data match Pitman et al's expectation: WS forests have similar species composition across Peru, and each WS patch harbors low diversity forests dominated by a small number of species. Yet the WS oligarchy differs in one important respect from the patterns reported in western Amazonian clay forests (Pitman et al., 2001). Unlike clay forest plots, the common species in WS plots are not as predictable from site to site. For example, only one species, Pachira brevipes, was collected at all seven WS sites. In many of these sites, P. brevipes was the most common tree, or at least in the top 10 most common (Table 3), but in some sites, it was collected only a few times. Of the 17 species highlighted in Table 3, 13 occur in both the western and eastern WS sites (Fig. 1) and four occur only in eastern sites. The results of the Mantel tests indicate significant patterns of correlation between spatial distance and species abundance data, yet no significant pattern with spatial distance and baia similarity with the species presence/absence data. I 3 region to other words, ominant species in one plot were more likely to be dominant in nearby WS plots, while the overall species composition among all of the WS plots had no spatial correlation. This lack of spatial correlation is consistent with the idea that WS flora may be largely co of species that are wind or bird dispersed, i wide-ranging dispersal capabilities (Macedo & Prance, 1978, but see ter em et al, 2006). Moreover, that many of the common species do not occur in every WS site is likely due to the island-like nature of WS forests in Peru. In contrast to the clay soils that are found at Manu, Yasuní, and the intervening lowland forests near zi Andean foothills between these "e sites, dur are rare in the western d across the region in noncontiguous patches (Fig. g^ Even though many of the WS-dominant species are good d indeed 13/17 of them have arrived in and eastern WS patches), not all of them have had the good fortune to arrive at all sites. In addition, given that many of these habitat islands are small, those species that have arrived later may have a difficult time gaining a foothold. WS forests are different than TF forests in the fact that one often finds large patches composed of a single species (Fine, pers. A 290 Annals of the Missouri Botanical Garden Tabl The top 10 id Lora khi d forest ] i l in Figure 1. Species in boldface occur in the top 10 list for more than one site. Morona, WS 11 to 12 Arecaceae Euterpe catinga 41 ae Tachigali paniculata 35 ij eae S guianensis 28 Sapotaceae Chrysophyllum sanguinolentum subsp. sanguinolentum 17 Fabaceae microcalyx 17 Sapindae Matayba inele, 16 yristicaceae Virola calophylla 12 Humiriaceae Sacoglottis ceratocarpa 12 A eae Oxandra asbeckii 9 eae evea 9 Jeberos, WS 7 Fabaceae Parkia i, 31 Icacinaceae Emmotum floribundum 26 Sapotaceae Chrysophyllum sanguinolentum subsp. sanguinolentum 25 Apocynaceae Macoubea sprucei 16 Aquifoliaceae Ilex sp. indet., ef. nayana 14 uphorbiaceae evea guia. 14 Sapindaceae Matayba inelegans 14 iaceae Tovomita c 13 Sapotaceae Pouteria lucumifolia 11 Sapotaceae Pouteria cuspidata subsp. cuspidata 11 Jenaro Herrera, WS 8 to 10 Clusiaceae Caraipa tereticaulis 164 Clusiaceae H hra cordata TI Clusiaceae Calophyllum oe 70 Myrtaceae Marlierea ca 26 Rubiaceae Platycarpum orinocense 26 Burseraceae Protium subserratum 25 Annonaceae Bocageopsis canescens 25 Sapindaceae C ia di; 19 Siparunaceae Siparuna guianensis 19 Clusiaceae Tovomita calophyllophylla 17 Tamshiyacu, WS 13 to 15 usiaceae raipa utilis 209 Clusiaceae ae cordata 125 Malvaceae Pachira brevipes 92 Clusiaceae Caraipa tereticaulis 33 Sa ceae Matayba inelegans 21 Rubiaceae tycarpum orinocense 21 Fabaceae Tachigali paniculata 11 Clusiaceae ovomita calophyllophylla 11 Fabaceae Macrolobium sp. indet. B 11 Elaeocarpaceae Sloanea sp. indet., cf. robusta 11 Upper Nanay, WS 5 to 6 Malvaceae Pachira brevipes 96 Clusiaceae Carai i 73 Elaeocarpaceae Sloanea sp. indet., ef. robusta 68 Fabaceae Dic uaiparuensis 58 indaceae Cupania diphylla 37 Rubiaceae Ferdinandusa chlorantha 23 Arecaceae Mauritiella armata 17 Fabaceae Macrolobium mic i IU 13 Fabaceae Dimorphandra ni subsp. glabrifolia 12 Volume 97, Number 3 Fine et al. 291 Study of White-sand Forests of Peru Table 3. Continued. Allpahuayo-Mishana, WS 1 to 4 Malvaceae Pachira brevipes 271 Clusiaceae Caraipa utilis 53 Fabaceae Dicymbe uaiparue 48 Araliaceae Dendropanax umbellatus 30 Arecaceae Euterpe catinga 26 Fabaceae Tachigali ptychophysca 22 Sapotaceae Chrysophyllum sanguinolentum subsp. sanguinolentum 22 Fabaceae arkia igneiflora 21 Elaeocarpaceae Sloanea sp. indet., cf. robusta 20 Rubiaceae Pagamea guianensis 17 Matsés, WS 16 Malvaceae Pachira brevipes 131 Areca Euterpe catinga 50 Burseraceae Protium heptaphyllum subsp. ulei 18 Rubiaceae Platycarpum ori. 15 Malphigiaceae Byrsonima laevigata 14 Elaeocarpace Sloanea sp. indet., cf. robusta 13 Chrysobalanaceae Licania sp. indet. A 12 Aquifoliaceae Ilex sp. indet., cf. nayana 8 Three tied at 6 pattern at odds with the high-diversity TF forests that exhibit density-dependent spatial patterns (Wills et al., 2006). In TF forests, common species that occur at high densities are thought to suffer disproportionately high attacks from natural enemies, giving rare species an advantage. WS forests have lower rates of herbivory than TF forests near Iquitos (Fine et al., 2006). Thus, unlike TF forests, rare species (including recent arrivals) may not gain any such advantage in WS forests, and thus potential oligarchs may not be able to quickly increase their local abundance in new WS sites, even if they do happen to get dispersed there. OVERLAP IN SPECIES COMPOSITION BETWEEN WS AND NON-WS FOREST PLOTS WS and TF plots are distinctive from one another. This is reflected in the fact that there are local names for WS forests in every Amazonian country in which they are found (Anderson, 1981) But, how distinctive Table 4. Average similarity between plots of & a € soil type and pl of divergent soil types u oca (Bsim) and species abundance pres di statistics. Comparisons ^ Presence/Absence Species abundance WS-WS 0.23 0.16 TF-TF 0.20 0.19 WS-TF 0.09* 0.02* * Asterisks indicate ne differences with P < 0.0001 with mom pe tation procedure tests. are they? This question has no clear answer because, as far as we know, no one has formalized a standard ocabulary or statistical methods for rigorously defining similarity between communities of different species compositions (Koleff et al., 2003; Jost, 2007). The amount of similarity between the WS and TF plots that we report depends on which index we use to estimate it. Most WS-TF comparisons so far have used the Jaccard index and have reported similarities of 0.10 to 0.20 (Ruokolainen & Tuomisto, 1998; Duivenvoorden et B Tuomisto et al. (1995) suggest that the Peruvian Amazon omposed of more than 100 different duit" es harboring unique plant species compositions that closely track environmental vari- ables. If the biotope model properly depicts Amazo- nian forest diversity patterns, one would predict that each plot would have low overlap in species composition, and that different suites of species would dominate each plot. While we find that WS plots are indeed quite different from one another (Fig. 2), the ominant species at the seven sites were composed of a suite of 17 species that were found across many WS sites (Table 3). We should also emphasize that our plots were chosen to include all of the different kinds of WS forest, including both varillales and chamizales, well-drained and poorly drained areas, etc. (cf. García-Villacorta et al., 2003). Our results, together with the results of Pitman et al. (2001), thus paint a much broader picture of western Amazonian tree habitats. WS forest, heralded as the most distinctive TF forest type in the Amazon (Anderson, 1981; Annals of the Missouri Botanical Garden , 1986), still contains a substantial number of species that also occur in more fertile soils. Therefore, we conclude that although WS forests are certainly “distinctive” from forests on more fertile soils, they are distinctive because of their low diversity and the composition of their dominant species rather than just because of their overall species compositions. PATTERNS OF ENDEMISM IN WS FORESTS Our preliminary lusion is that a littl than half of the 221 species are WS endemics. These 114 species do not occur in the TF plots nor do they occur in the Catalogue of Ecuador. We believe that this is a fair estimate, although it does include 33 morphospe- cies that may or may not be new species (Appendix 1). Some of these morphospecies may be species for which we did not find a match in the herbarium but are distributed in lowland Amazonia in TF forests, but not where Pitman and colleagues set up plots (Fig. 1). Yet many of these 33 morphospecies are likely to be pecies. It is important to stress how few plant collections have been made in any WS forests in Peru, especially in WS forests distant from Iquitos. For example, three of the dominant Clusiaceae species in our WS plots were described only within the past two decades (Vasquez, 1991, 1993; García-Villacorta & Hammel, 2004). One of the collections from our inventories in Jeberos yielded a new genus for Peru (Hortia Vand., Rutaceae) (Brako & Zarucchi, 1993). In addition, there could be quite a few eryptic species that are hidden in the data set, artificially ular sequence divergence in the genus Inga Mill (2010) found sever. morphologically similar but molecularly divergent taxa that had previously been lumped together, after which further study yielded other morphological but previously overlooked characters, resulting in the discovery of new cryptic Inga species. Along these lines, there are three species on our list that we suggest should be investigated for cryptic diversity and whose clades should be subjected to a molecular — phylogenetic analysis: Ferdinandusa chlorantha (Wedd.) Standl. (Rubiaceae), Euterpe catinga Wallace (Arecaceae), and umbellatus (Ruiz & (two individuals). What is most intriguing about these three species is that the Catalogue of Ecuador reports them as being absent from Amazonian lowland forests. Ferdinandusa chlorantha and E. catinga are reported only from high elevations in the And (1000-1500 m), while D. umbellatus is reported to occur on the Pacific coast, on the other side of the Andes. COMPARING PERUVIAN WS FORESTS TO THOSE IN EASTERN AMAZONIA Ten out of the 12 most common families from Peruvian WS forests appear in lists of the most important families in WS forests farther east from published sources in Colombia, Brazil, and Venezuela (Table 2). One family in particular, the Clusiaceae, dominates WS forests throughout the Amazon. Unlike the Fabaceae, which dominates everywhere in Ama- zonia (Gentry, 1988), the Clusiaceae family does not appear in the top 12 families for Peruvian non-WS plots, suggesting that there is something about WS su te that encourages high populations of Clusia- ceae trees. To be able to examine the similarity of Peruvian WS plots to WS plots in eastern and central Amazonia and the Guianas, one needs to compare complete species lists, but as far as we know, there is not a single published account of any plot-level species list S forests in eastern Amazonia or th ulanas. There is a published checklist of the plants of the Guianas (including Guyana, Suriname, and French Guiana) (Boggan et al., 1997) as-well as a comparison of three florulas within Guyana with central French Guiana and the Reserva Ducke of Manaus, Brazil (Clarke et al., 2001). Although the checklist of Boggan et al. (1997) does not list edaphic associations of its ' Species, it is interesting to note that 78 (35%) of the species in our WS lists occur in this checklist, almost as many species that occur in the Catalogue of Ecuador (81 species, 36% of the total), even though the Guianas are more than 2000 km from Peru. Thirty- one of these 78 species are classified as WS endemics or facultative specialists here. One assumes that many of these species occur in sandy soil habitats in the Guianas, but this assumption will have to be tested with future inventory work. In addition, most of our herbarium comparisons were undertaken at F and MO, between Peruvian WS forests and WS forests farther east. Indeed, species from our WS list like Mauritia carana Wallace (Arecaceae) have been reported from WS forests in Colombia, Brazil, and Venezuela (Anderson, 1981; Coomes & Grubb, 1996; Duiven- voorden et al., 2001). On the other hand, even within the Rio Negro, WS forests have been reported to be compositionally extremely dissimilar (Anderson, Volume 97, Number 3 2010 Fine et al. Study of White-sand Forests of Peru 1981). Thus, the characterization of the South American WS flora remains an avenue of exciting future research. CONSERVATION OF AMAZONIAN FORESTS: THE FOCUS OF FUTURE BOTANICAL RESEARCH EFFORTS Articles reporting the results of current botanical resent i in ie Aan often suicide by recom- E £ + ADCI OL UCE ieee (ter SED et al., 2003). While accumu- lating more data on uncollected regions is certainly a laudable goal, more attention needs to be paid to understanding the diversity of tree plots that have already been inventoried. Too many of these trees languish as unidentified morphospecies, or just as tragic, dubiously named species from genera and families with no current taxonomic specialist (i.e., Nos land) How can we compare vast networks of plots across an entire continent when we have little idea of the identities of the tree species? Are similar-appearing species cryptic habitat Or are some morpho- logically distinct taxa exhibiting phenotypic plastic- ast questions can only be answered wi systematic monographs coupled with molecular phy- logenetic and population genetic studies, yet only a handful of tropical tree groups are currently the focus of any active research program in any laboratory. To solve this problem, we believe that research on the systematics and floristics of Amazonian plants ought to receive a very high priority for funding. specialists or local endemics? ity? These CONSERVATION IMPORTANCE OF WS FORESTS Despite being species-poor, we believe WS forests should be given high conservation priority. First, the species recordad in WS forests are often edaphic and geographic endemics, found nowhere else in: the world. In the past 20 years, biologists working in WS forests near Iquitos have discovered many animal and plant species new to science (Vásquez, 1991, 1993; Alvarez & Whitney, 2003; Garcia-Villacorta & Hammel, 2004). These species have not been registered outside of WS forests, and many are only found in Peru. S the current data set as a point of comparison, we compared our species list to a ublished cameras checklist of various os — ding three areas fi Guyana razil (the Ducke Reserve near Manaus), 7 “all m WS forest habitats (Clarke et al., 2001). Of the 135 species that we classified in this study as WS endemics, cryptic endemics, and facultative WS specialists, 41 do not occur in this checklist, and thus may be restricted to only western Amazonian WS areas, underscoring their rarity. Moreover, in Peru, WS habitats are even less common in the landscape than they are farther east in South America. Currently, there are only nine known patches of WS forest in the lowland Peruvian Amazon, representing less than 1% of lowland Peruvian rainforest (Fig. 1). These nine WS patches are isolated from one another and similar habitats in Colombia, Venezuela, and Brazil, and this —— sss. likely reinforces not only the nerability of Peru's WS flora and fauna. For ia fewer than 25 individuals are known of the newly described gnatcatcher Polioptila clementsi and all occur in two WS forest patches in and near the Reserva Nacional Allpahuayo-Mishana (Whitney & Alvarez, 2005). At present, only two areas in Peru that harbor WS forests enjoy any legal conservation status, the Reserva Nacional Allpa- huayo-Mishana (58,069 ha) and the Reserva Nacional Matsés (420,635 ha) (Vriensendorp et al., inally, TM arta are ane iple: These soils Moe lide nutrients reside within living organisms, and roots and fungi quickly capture any decomposing nutrients. If the trees are cleared in a WS us 5 1 1 pidly +L gh th nd the soil fertility quickly degrades. Using these forests for extractive or agicoltural activity is puc economicall y orest, clearing the forests than could ever be wnparapod from agricultural or logging enterprises CONCLUSIONS We now have a preliminary database with which we can describe the tree flora of the Peruvian WS forests. WS forests are different from other Amazonian forests on TF, mostly due to their very low plot-level diversity and dominance by a set of 17 species that account for a majority of all individuals. We expected the WS flora to be composed of mostly WS specialists because WS is so extremely nutrient poor relative to all other TF soils in the Amazon. On one hand, our prediction was m as most — Ss in WS pl to WS forests, or at least mek more common in WS plots than TF plots (“facultative WS specialists”). On the other hand, it was surprising that so many different species of trees common in other more fertile soil types were encountered in the WS plots. While their numbers could possibly be inflated due to cryptic diversity, it seems fair to estimate that almost half of the total number of species that we encountered in all WS plots were due to species more common on other soil types. We speculate that many species possess traits that allow for survival in WS soil, but very few species Annals of the Missouri Botanical Garden possess traits that allow them to become dominant, for example, traits that promote long-term growth or piece 3 in NR -> o leaf longevity, against iiaa enemies (Fine et sagen 2006), an for lineages like Dicymbe Spruce ex Benth. GAN among others, association with ectomycorrhyzae (Sing- er & Araujo, 1979; McGuire, 2007). 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Peter Linder,?* Marcelo Baeza,* Nigel P. Barker,? Chloé Galley,? THE DANTHONIOIDEAE Aelys M. Humphreys,? Kelvin M. Lloyd,’ (POACEAE) David A. Orlovich,’ Michael D. Pirie,?* Bryan K. Simon,” Neville Walsh, and G. Anthony Verboom'' ABSTRACT n on classification of the largely Southern Hemisphere grass subfamily Danthonioideae. This io is i honk a an almost completely — and well-resolved molecular phylogeny and on a complete morphological data set We "have en © delimit monophyletic genera (complicated by o presence of apparent e 17 genera, including five new gene ES N. P. Barker & H. P. Linder, Capeochloa H. P. Linder & N. P. Barker, Chimaerochloa H. P. Linder, Ie H. P. Linder & N. P. Barker, and Tenaxia N. P. Barker & H. P. Linder), and two sections newly designated for Pentameris P. Beauv. poon Dracomontanum H. P. Linder & Galley and section Pentaschistis (Nees) H. P. Linder & Cale Of the remaining 12 genera, the delimitations of seven are changed: Merxmuellera Conert 1s much — by the segregation of Geochloa, 2 and Tenaxia; Pentameris is expanded to islalode Prionanthium Desv. p p kabr ihi p Pilg. but reduced by the ana Si A 4 A š 1 z. Qe Ex š f Joycea HP Lider. A di seo ¡ d spes Linder. Nodal E. id Maadhya Merr.; and the species previously assigned to Karroochloa Conert & Y Tüne, $ Schismus P. Beauv., . Urochlaena Nees, and Tribolium Desv. have been reassi igned to only th two genera Finally, the Hi DC fi I llera. The 281 š species t that w we recognize in the subfamily are listed under their new genera, hich lin the phyl i Ew 100 necessary new combinations include: Merxmuellera andiflora (Hochst. ex A. Rich.) H. P. Linder, Geochloa decor am an P. Barker & H. P. Linder, Ç. —— € = appen . P. Linder, G. oe ) N. P. Barker & H. P. ie, Capeochloa arundinacea rgius) N. P. Barker Linder, C. cincta (Nees) N. P. Barker & H. P. Linder, C. cincta subsp. — ys p. Barker) N. P. Barker & H. P. T A setacea (N. P. Barker) N. P. Barker & H. P. Linder, Pentameris praecox (H. nder) Galley & H. P. Linder, P. — P) Galley & H. P. Linder, P. acinosa (Stapf) Galley & H. P. Linder, P. n Nees subsp. jugorum (Stapf) Galley P. Linder, P. $ n (H. P. Linder) Galley & H. P. Linder, P. ampla (Nees) Galley & H. P. Linder, Hs seii ane a amus) Galle ey & H. P. Linder, P. pe (Stapf) Galley & H. P. Linder, P. aristidoides (Thunb.) Galley & H. P. Linder, P. art Qam i) Galley & H. P. Linder, P. aspera (Thunb.) Galley & H. P. Linder, P. aurea (Steud ) Galley & H. P. Linder. rea subsp eo EN E & H. P. Linder, P. Mind (McClean) Galley & H. P. Linder, P leote d Steud. E is (H. P. Linder) Galley & H. P i H. Icicola var. hirsuta (H. P. Linder) ey & H. P. Linder, P. capensis (Nees) Galley & H. P. Linder, apillaris (Thunb) cae & H. P. Linder, P. caulescens (H. P. Linder) Galley & H. P. Linder, P. chippindalliae (H. P. esa Galley & H. P. emas P. chrysurus (K. Schum.) Galley & H. P. Linder, P. clavata i Galley & H. P. Linder, P. d args ) Galley & H. P. Linder, P. cista (L. f.) Galley & H. P. Linder, P. dolichochaeta (S. M. Phillips) Galley & H. ecklonii (Nees) Galley & H. P. Linder, P. exserta (H. P. Linder) Galley & H. P. T P. ane (Stapf) Calley n. E P. holciformis (Nees) Es & H. P. Linder, P. — (Galley) Galley & H. P. Li umbertii (A Camas) Galley & H. P. Linder, P. yq (Hemsl.) Galley € H. P. Linder, P. Ear (Stapf) Calley & H. P. Linder, P. pes (Stapf) Galley & H. P. Linder, P. malouinensis (Steud.) Calley & H. P. Linder, P. microphylla (Nees) Galley & H. r n P. minor (Ballard & C. E. Hubb) Galley & H. P. Linder, P. montana (H. P. Linder) Galley & H. P. Linder "This article is dedicated to Surrey ie (1946-2009) in honor of his lifelong work on and interest in the Aust grasses. This research was supported by the Swiss National Science Foundation (grant dr ut fieldwork was supported i in part by the Claraz x and in e by the Swiss Academy of Sciences. Collecting pe as gran by the nature conservation authorities in South Africa, Malawi, Australia, New Zealand, and Chile. The. ola were made by Jasmin Bauman * Institute of King Jic University of Zurich, Zollikerstrasse 107, CH-8008, Switzerland. * ¿Author for correspondence: peter.linder@systbot.u nto de Botanica, Universidad de oo Casilla 160-C, ee Chile. e of Botany, Rhodes University, ° La Research, Private Bag 1930, Dunedin 9054, New Zealand. — of Botany, University of Otago, P.O. Box 56, Dunedin 9054, New , Current address: Department of Biochemistry University of rer p E Bag XI, Matieland 7602, South Africa. and Herbarium, Toowong, Queens us “Royal Botanic Gardens Melbourne, Bi cae pS | South Y arra, Victoria a Australia. " Department of Botany, University of Cape Town, Bondelindh 7700, South Afric doi: 10.3417/2009006 ANN. Missourt Bor. Garp. 97: 306-364. PUBLISHED on 10 Ocronrn 2010. Sen ee dl c lal Volume 97, Number 3 Linder et al. 2010 - Classification of Danthonioideae natalensis (Stapf) Galley & H. P. Linder, P. oreodoxa (Schweick.) Galley & H. P. Linder, P. pallida (Thunb.) Galley & H. P. Linder, P. pholiuroides Pan) we & H. P. Linder, P. pictigluma (Steud. ) Galley & E P. Pepe P. ume var. gracilis (S. M. Phillips) pai & H Linder, P. pi € var. mannii (Sta Hubb.) Galley & H. P. Linder, P. pseudo, P. Linder 9 Gaus & H. P. Linder, P. pungens (H. P. «pera cale & H. E Lin der, P. € emm Galley & H. P. a. Pp pyrophil a (H. P. Linder) Galley ZHE H. P. Linder, P. H. P. Linder) Galley & H. . Linder, P. rosea sagi Linde ey & H. P. er, P. scandens (H. P. & H. P. i P. etha (Thunb.) . Linder, P. tomentella (Stapf) Galley & H. P. Linder, P. trifida (Galley) Calley & H. P. Linder, P. triseta (Thunb.) Calley & H. P. Linder, P. trisetoides t ex Steud.) Galley & H. P. Linder, P. velutina (H. P. Linder) Galley & H. E. Vases P. veneta (H. P. Dd e & na (Hitche.) N. P. Bar (Endl) N. P. Barker & H. P. “nage Linder, A. turbaria (Conno aureocephala (J. G. Anderson) N. P. cumminsii minsii (Hook. f.) N & H. P. Linder, T. iae (C nens P. Barker mp subulata (A. Rich.) N. P. Barker & H. P. Linder, Schism (Nees) Verboom & H. P. Linder. nder, Sch . T. pleuropogon Ve ion É H. P. Linder. an) N. P. Barker ge iue (Connor) N. P. Barker & H P Linder, A. toetoe (Zotov) N. P. Barker & H. P. r) N. P. Barker & = E. iE noe to archboldii (Hitchc.) Pirie € H. P. Linder, Tenaxia Barker P. Linder, T. cachemyriana (Jaub. & Spach) N. P. Barke F. Barker & H. P. pee E disticha (Nees) N. P. Barker & H. P. — T. dura (Stapf) N. P. Barker "s Men T. stricta Pean r & H. P. Linder, 7. er & H. P. Linder, T. ides (Stapf ex Conert) V H. P. Linder, Tribolium eU f.) Verboom & H. P. Linder, T. tenellum (Nees) AR & H. P. Linder, Rytidosperma bipartitum (Kunth) A. M. Humphreys & H. P. Linder, R. diemenicum (D. I. Morris) A. M. A. M. Humphreys & H. P e & H. P. Linder, R. fulvum (Vickery) A. M. Humphreys & H. P. Linder, R. . Linder, R. pallidum ; R. (R. Br.) A. M. Humphreys & H. P. Linder Typifications are designated for the following names: Achneria Munro ex Benth. & Hook. f., Avena aristidoides Thunb., A. s var , Geochloa lupulina, Pentameris trunculata Nees, aristido: idolis. . Danthonia sect. Himantochaete Nees, D. zeyheriana Steud. and o holciformis Key words: Danthorioidese, generic delimitation, Poaceae, taxonom The Danthonioideae constitutes a small, well- defined clade currently recognized to comprise 281 largely Southern Hemisphere grass san The genera that make up the clade were reco, as a coherent group only after 1957, with the ramen of the Arundinoideae (Tateoka, 1957). in which they were included. However, the present delimitation of the clade dates from the early e nul work of Barker et al. (1995). At the same tim Verboom et al. (1994) were able to aa that the aa could also be delimited by the possession of haustorial synergids. The subfamily was oo. erected by the Grass Phylogeny Working Group (200 Generic delimitations in the opted have been remarkably unstable (Reimer & Cota-Sanchez, 2007). De Candolle (1805) recognized Danthonia DC. in 1805 based on the American D. spicata (L.) P Beauv. ex Roem. & Schult. and characterized it by de bilobed, awned lemmas. Soon after that, Palisot de Beauvois (1812) desckibid Pentameris P. Beauv. (only two florets per spikelet, fruit an achene) and Schismus P. Beauv. (lemma unlobed, or with short lobes, and with a short, simple awn). During the 1830s, Tribolium Desv. (lemmas acute), Chaetobromus Nees € subtended by a tuft of hair), Prionanthi (annuals, glume keels with forked, mahincihular ms — and the section Pentaschistis Nees of nia (only two florets per spikelet, fruit a ae were added. Bentham and Hooker (1883) simplified matters again by including jue, Pentaschistis ) Spach, Chaetobromus, Plin- thanthesis Steud., as well as several genera now no longer retained in the Danthonioideae, in Danthonia. This left Prionanthium (as Pri Nees), Schis- mus, and Tribolium (as Lasiochloa Kunth) as separate genera. ral more genera were erected after the pub- lication of the Genera Plantarum. Cortaderia odioeci n 1897 by Stapf, who also erected Poagrostis Stapf, a — species of Pen- taschistis (Stapf, e last genera to be e F escri on new species, rather than diia of previously described genera, were Lamprothyrsus Pilg. (Pilger, 1906) from South Amer- ia. However, by 1900, both species currently recognized in the Danthonioideae were included in the large genus Danthonia, which included all species with bilo geniculate awns inserted between the lobes, and with more than two florets in the — Species that deviated from this (with only two florets in the spikelets, or without lemma lobes or lacking a geniculate awn) were placed in various small segregated genera. This concept prevailed for almost a century. It was evident that Danthonia was not natural, and the dismantling of this genus was pursued in parallel for the African and Australasian species. This process Annals of the Missouri Botanical Garden was started in New Zealand by Zotov (1963), who RM E a Sonn | And insightful peper » UE he his new genera Chienoechloa Zotov, Erythranthera Zotov, Pyrrhanthera Zotov, and Notodanthonia Zotov (= Rytidosperma Steud. [Nicora, 1973]. He also process was paralleled in Africa by Conert and his associates. M sub Sehassn mp e Danthonia Er Türpe "a & Lun 1969), Milos Cont (Conert, 1970), and meris Conert — 1971). In eic Blake (1972) separated ou Plinthanthesis Steud. (although the name dates back to Steudel [1853-1854], and Veldkamp (1980) transferred the Australian, Malesian, and many South American Danthonia species to Notodanthonia. How- ever, all Notodanthonia species had to be transferred to the older generic name, Rytidosperma (Connor & Edgar, 1979). This fragmentation resulted in an unsatisfactory delimitation of Rytidosperma. It seemed likely that the small genera Monostachya, Pyr- rhanthera, and Erythranthera might be embedded within Rytidosperma. Further, the relationship to the very similar South African species of Karroochloa and some species of Merxmuellera was not clear. Clayton and Renvoize (1986) followed a rather broad solution to these issues and included many of these segregates of Danthonia in a much expanded Rytidosperma Linder and Verboom (1996), by contrast, defined a narrower Rytidosperma and segregated out Austro- danthonia H. P. Linder, Joycea H. P. Linder, and nandia H. P. Linder (= Notodanthonia Zotov), but included Pyrrhanthera, Erythranthera, and Monosta- chya in Rytidosperma s. str. They indicated the close relationship between this clade and the African hloa, Schismus, Urochlaena Nees, and Tribo- lium. The first species-level molecular phylogenetic tage unveiled a host of further problems. Barker et al. (2003) demonstrated that Cortaderia was aa with the New Zealand and South American segregates not being sister clades. Further- more, they showed that the African Merxmuellera species belong to three distinct, unrelated clades and that M. papposa (Nees) Conert and M. rangei (Pilg.) Conert should be placed in a different subfamily, the ME (Barker et al., 2000, 2007). Verboom et al. (2006) showed that the generic limits between Schismus, Karroochloa, ribolium were mis- placed, ew that none of these three genera are monophyletic. A recent detailed molecular phylogenetic study by Pirie et al. (2008) provided a phylogenetic framework with which to address these problems in detail; it included 81% of all known species in the subfamily and most nodes were robustly resolved. It also nM the widespread occurrence of reticula- n. Here, we use this phylogenetic framework and de available morphological data to erect a ne generic classification for the subfamily. We decd and apply Z ~ for the main ranks (generic and infrageneri make all the new combinations er to apply the new generic classification at species level. MATERIALS AND METHODS TAXA, DATA, AND ANALYSIS Morphological descriptions were based on the study of herbarium collections in AD, B, BM, BOL, C, CANB, CHR, CONC, GRA, HO, K, L, MEL, NBG, NSW, NU, P, PRE, S, US, Z, and ZT over the past 15 years and were generated in the process of preparing revisions or flora accounts (Baeza, 1990, 1996a; Linder & Ellis, 1990a; Barker, 1993, 1995, 1999; Linder, 1997, 1999, 2005; — & Davidse, 1997; Verboom lost all species have been observed in the field, often at several locations, and over several years. Further descriptive obtained by preparing mounts of these organs in glycerine and stained with fuchsine. Caryopsis data for African taxa were taken from Barker (1986, 1994). Anciana sections were collected over many decades, by several laboratories, and using diverse methods. Leaf material was largely taken from the midportion of the blades, mostly from material fixed in the field in FAA, but also from herbarium material reconstituted in boiling soapy water. Sections were cut either free-hand or by sledge-microtome, or from mounted in xylene or Canada were prepared by softening leaves, then scraping off the mesophyll. Most slides are currently housed in the Institute of Systematic Botany of the University of Zurich or at the South African National Biodiversity Institute, Pretoria. The descriptive ter- minology follows Ellis (1976, 1979). e made no original cytological or embryological observations for this research but incorporated the published results. There have been many investiga- RR E LL ML DAI n e MSc RM iA Volume 97, Number 3 2010 Linder et al. Classification of Danthonioideae tions into the number of chromosomes in the subfamily (Calder, 1937; Stebbins & Love, 1941; Myers, 1947; de Wet, 1953, 1954; Gould, 1958; Abele, 1959; Bowden, 1960; Brock & Brown, 1961; Lóve & Lóve, 1961; Bowden & Senn, 1962; Borgmann, 1964; Packer, Lets Schwartz & rae 964; Mehra & Kalia, 1975; Moore et al., 1976; m 1977; Stl & Probatova, ds qi & Quraish, 1979; Beuzenberg & Hair, 1983; pee et al., pe du Plessis & Sho 1992; Spies et al., 1994; Visser & Spies, 1994b, c; Baeza, 1996b; Spies & Roodt, 2001; Hilu, 2004; Murray et al., 2005), but there are still some gaps in the i of genera for which no counts are available. The embryology has also received some attention, in particular the development of haustorial synergids (Philipson & Connor, 1984; Verboom et 1994). The reproductive system was investigated hy Connor (1967, 1970, 1979, 1981, 1991). The full descriptive information at species level was compiled in the software DELTA (Dallwitz, 1980; Dallwitz & Paine, 1986) and will be released as an INTKEY interactive key. This will also include the full nomenclatural inform including the synonymy. Phylogenetic results presented here are based on Pirie et al. (2008), which included 256 samples of 227 ingroup species (plus 14 subspecific taxa), represent- ing 81% of the danthonioid species recognized here. A matrix including multiple chloroplast and nuclear ribosomal DNA sequence markers (cpDNA and nrDNA) was constructed (available on TreeBase, accession number S10417), assembled from new sequences generated for that study together with sequences obtained from ius a (Barker et al., 1995, 2000, 2003, 200' 2006; Calley & Linder, 2007). ical PACCAD (Pani- coideae, Arundinoideae, Chloridoideae, Centothecoi- deae, Aristidoideae, and Danthonioideae) clade out- group sequences were obtained from GenBank. DNA extraction, polymerase chain reaction ne and sequencing protocols are described i e above studies and in Pirie et al. (2008). The fice markers were used: cpDNA from the trnL intron and trnL-F intergenic spacer, rpll6 spacer, atpB-rbcl. spacer, ndhF gene, matK gene (including flanking spacer regions), and L gene; and nrDNA sequences from the ITS Son and an 1100-bp-long fragment of the 26S gene. In total, more than 8200 bp of cpDNA and more than 1800 bp of nrDNA were sampled. Sequences were aligned manually and gaps were coded as separate presence/absence characters. A novel “taxon duplication” method was used to pene 2 e analys u o NA and nrDNA tic signals. This ation on each species, Kv ° approach is described in detail in Pirie et al. (2008, 2009), but is worth summarizing here in order to aid interpretation of the phylogenetic tree. Separate analyses were performed on each of the markers and the resulting topologies were Fp auqa q for conflicting "n supported by 70% or higher bootstrap support Where no such conflict was found, data ui. were combined. Where conflicting nodes were found, the corresponding inconsistently placed taxa were duplicated in the matrix, with one taxon as missing data, the other taxon copy by nrDNA only, with the cpDNA coded as missing. The partitions were then combined. The positions of the following taxa were subject to such conflict: a | clade including all witho ri ci archboldi (Hitche.) Connor & Edgar or C. pilosa (d'Urv. Hack ex Dusén (in total 11 species, representing the same conflict between the chloroplast and nuclear genomes); 10 species of Pentaschistis (each representing a separate incidence of conflict); Chionochloa australis (Buchanan) Zotov (one sample); Tribolium ciliare (Stapf) Renvoize (one sample); and T. pusillum (Nees) H. P. Linder & Davidse (one sample). These 30 samples, representing 27 species, were thus rejet iie in t me pu. PONE the number ft and nrDNA analyses up to 290. Parsimony analyses (heuristic search and boot- strapping) were performed using the software package PAUP* 4.0b10 (Swofford, 2002), and Bayesian in- ference was performed using MrBayes 3.12 (Ronquist & Huelsenbeck, 2003). For details, see Pirie et al. (2008) Generic delimitation criteria. We attempt to define the genera of the Danthonioideae according to explicit criteria. These criteria can into two categories: those that pertain to the delimitation of the clades (thus defining the content of the genera), and those that pertain to the ranking of the clades (thus which clades should be ranked as genera). We delimited the clades (monophyletic groups) primarily on the phylogeny e from DNA sequence data. This is based on assumption that the phylogeny provides the seas prediction for the characters of the groups. Morphological data were used in two situations. The first was to assign to the correct clades those species that were not included in the molecular phylogeny, either because we could not 310 Annals of the Missouri Botanical Garden obtain DNA suitable for sequencing, or because we had difficulty obtaining sequences. The morphological characteristics (diagnostic attributes) of the genera were derived from the species assigned in the molecular study to the genera. The second situation was where there was incongruence between the nuclear and plastid genomes. In this situation, the considered, in order to minimize the heterogeneity of the genera. Defining clades where one nucl partition is nonmonophyletic differs from the strategy proposed by Potter et al. (2007), in which only uncontradicted clades were recognized, and contra- dicted nodes result in new genera. Our strategy is less conservative. Here, two logical routes are possible. In the first (and presumably most widely used) approach we sought positive evidence that a species is a trap or posterior probability values. The second approach sought positive evidence that inclusion of a species in a clade renders that clade paraphyletic or polyphyletic. In most cases we used the second criterion. This implies that if a species was previously placed in a clade, or if morphological evidence indicates that it belongs in a particular clade, it was removed from that clade only if there was positive evidence from the molecular data that its inclusion would result in a paraphyletic or polyphy- letic group. We used several ranking criteria for the establish- ment of genera, listed here in no particular order. l. Genera should be delimited to minimize nomen- clatural changes. This means that we did not sink genera, or erect new genera, where the existin genera did not violate the monophyly requirement, as interpreted above (Funk, 1985). 2. Genera should be morphologically, ecologically, and geographically homogeneous. Ideally, the dis- parity within a genus should be minimized (e.g.. number of continents occupied, habitat range, morphological variance). However, in many cases this has been very difficult to achieve. w logically. Fortunately, the morphological and nomenclatural criteria generally coincide, as in the past genera were delimited on precisely these morphological criteria. Ideally, it possible to construct a simple key to the genera, based on characters that are readily observed on herbarium specimens. This, however, was almost impossible, due to the very extensive morpholog- ical convergence within the subfamily that is reflected by the frequency of reticulation evi- denced by the molecular phylogeny (Barker et al., 2000; Pirie et al., 2008). We largely accepted that it will not be possible to key out the genera (although regional floras may not encounter similar conflicts) and recommend that the users use a key to the species, rather than to the genera. 4. The number of monotypic genera should be minimized. Monotypic genera are generally estab- ished because they are morphologically aberrant in their “clade.” If this aberrance is due to a long evolutionary history, then they could be regarded as distinct, by definition monophyletic, lineages. Extreme cases of this argument are the genera Welwitschia Hook. f. and Ginkgo L. Monotypic genera could also be established to indicate phylogenetic uncertainty, either due to conflict between the genome partitions or due to lack of basal resolution, as was the case in the genus Caulipsolon Klak (Klak & Linder, 1998). The latter has the ad t ESA E a : approach that need more research. If these topologically uncertain speci placed in their most likely or demonstrated sister genera, there is a danger that they will be forgotten, and their attributes summed number of taxa erected, and so can be regarded as being nomenclaturally conservative. 5. Generic rank should take into account the age of the clades. Hennig (1966) suggested that ranks could be associated with the absolute age of the axa, and Goodman et al. (1998) proposed a classification of the primates in which the ranks of the clades are related to the crown ages. We explicitly did not delimit genera as the smallest lagnosable, monophyletic (e.g., polytypic) units. We rather sought larger, more inclusive units, akin to the generic concept that Bentham used in the Genera Plantarum (see Humphreys & Linder, 2009), that also meet the geographical, morphological, and ecological criteria listed above. The smallest diagnosable, polytyp- ic clades are recognized as sections. If another level of such units is available, we recognize them as subgenera. e. RESULTS AND DISCUSSION MOLECULAR PHYLOGENY FOR ALL SPECIES The topologies derived from the individual cpDNA markers were without significantly supported incon- gruence. The nuclear markers ITS and 26S also showed no significantly supported incongruence, but the numbers of informative characters, and thus dac albi i rad i patei Sr lise iste o NE A A a Volume 97, Number 3 2010 Linder et al. Classification of Danthonioideae 311 degree of amago were lower than those for the cpDNA analyses. The combination of all the e using died taxon duplication method to acco conflict between cpDNA and nrDNA, sailed. in strong support for the alternative positions of the conflicting taxa and greatly increased resolution and Tei pin = to the nrDNA tree (Fig. 1). Pars rt values for the tial sido deci in comparison to the values obtained from analysis of cpDNA only. However, Bayesian posterior probabilities for the same nodes remained high. This can, at least in part, be explained by the relative robustness of Bayesian inference to the large proportion of missing data representing the duplicated (conflicting) taxa (Pirie et al., 2008). GENERIC DELIMITATION A single mega-Danthonia. A simple solution would be to reconstruct the old genus Danthonia, as the sole genus in the subfamily, based on node A (Fig. 1A). The becom single-large-genus solution has recently me popular, with the reassembly of very large genera, such as Erica L. Olive, 1991), Disa P. J. Bergius (Bytebier et 7 2007), Eucalyptus L'Hér. (Brooker, 2000; Ladiges & Udovicic, 2000), Veronica L. (Garnock-Jones et anksia L. f. (Mast & Thiele, 2007). Morin Mill. (Golda et al., 2002), and Ornithogalum . (Manning et al., ), but equally th litti f large, old genera such as Acacia Mill. (Maslin et "i 2003) (viewed in Humphreys & is 2009). In the case of Danthonia, i y a medium-sized genus of some 281 However, there are several arguments against this solution. Some genera have been separated from Danthonia for more than a century (e.g., Pentaschistis, Schismus, and Pentameris), much of the breaking-up of Danthonia was completed more than 20 years ago, and the segregates have become well established and are widely used in diverse floras (e.g., Southern Africa [Gibbs Russell et al., 1990]; Australia [Mallett & Orchard, 2002]; New Zealand [Edgar & Connor, 2000]). Many of the segregate genera are morpholog- ically distinctive, and their species share a likeness. It L3. s Aa Rp aka xb odiis A of these patterns of similarity. Most of the segregate genera occupy a particular continent, thus o part of the range of the whole subfamily. These rg geographically and also ecologically definable. mega-Danthonia would include many species d have never been Danthonia and would therefore require 142 new combinations, which would be undesirable given that one of the criteria is to minimize nomenclatural changes. A monotypic sub- family carries very little information, as it duplicates all the information already contained in the pM The segregates would provide much more information, as each genus specifies a part of the variation hie the subfamily. On the basis of these arguments, we think that it would be better to retain the generic rank at the i Pata level, rather than have a single genus for the subfami Merxmuellera basal p Barker et al. (2000, 2007) showed that the genus Merxmuellera, as delimited by Conert (1970, 1971), is grossly re and this is confirmed by the results of Pirie et al. (2008). Two species (M. papposa and M. rangei) are in the subfamily u with the remainder in Danthonioideae. des (newly named here Geochloa, Capeoc. and Me eo form a basal grade ii to the rest of the nt A fourth clade (Tenaxia) is sister to the R ee uellera (Fig 1A, node B) is Net cabbie tie ie io is Afromontane, ranging the Drakensberg in southern Africa to the mountains of Madagascar and north to Ethiopia. The species of the genus can be recognized by the synapomorphy of the leaf blade disarticulating shortly above the ligule, thus leaving a distinctive stub, and by the more or less iagnostic indumentum pattern on the lemma back. 're are no obvious breaks in the variation in this clade; only one of the four species is morphologically rrant. The second basal segregate (Fig. 1A, node Cii) is almost impossible to define morphologically, but receives strong molecular support. It contains three very distinct elements, thus making it heterogeneous. The one ao, contains three villous geophytic asses (Merx ra rufa (Nees) Conert, M. decora (Nees) Conert, "M. pata iL. £) e the second, two large caespitose grasses (M. cincta (Nees) Conert); and the third, a very nik glabrous sedgelike geophytic grass (M. setacea N. P. Barker; Barker & Ellis, 1991). We are ambivalent about whether to recognize three, two, or one genera. It would be simple to group the three elements on the basis of their molecular support, and to recognize a highly heterogeneous genus. However, a closer inspec- tion of the cladograms and chronograms (unp: ublished data) shows that the three geophytic grasses diverge very early from the remaining three species, and this supports te Pup for ha eee them at generic level, — ages. The jocugaition of a separate genus for the geophytic Cape grasses leaves us with a difficult problem with the remaining three species, but it is a ld have more or less 312 Annals of the Missouri Botanical Garden Centropodia glauca Centropodia mossamedensis D Merxmuellera papposa 1.00 r Merxmuellera davyi 3 Merxmuellera macowanii 3 palencia Merxmuellera drakensbergensis Ë Merxmuellera stereophylla š g aid Merxmuellera arundinacea NPB1017 cpDNA ) $ 71 = ne ane š Š o z E o o 4.00 š 100 / 94 / 100 $5 Ng v x T olen mn E o 1.00 See Fig. 1b 99 / 99 / 100 Fig 1.00 D 961-*198 1.00 70 / <50 / 58 š S 1.00 8 100 steps 90/<50/81 1.00 E 91/<50/ A c 93 / <50 / 86 Figure l. A-D. PEUT with specime named acc to th Where more than on specimen per species was sampled, these are rdi erned with voucher E (ses Pirie et al., 2008). bons for which de nuclear. and | plastid partitions are significantly incongruent are indicated in bold y "nrDNA" and the plastid by “ 2 bs d referred to in the text is indicated ie three values for bootstrap support (cpDNA/nrDNA/combined) and a single value for Bayesian posterior Dro (combined). Where the clades are not identical in the two partitions, the relevant support value is marked by erisk. The new genera are indicated to the right of the cladogram. A AS Volume 97, Number 3 Linder et al. 313 2010 Classification of Danthonioideae 0.97 98 / <50 / 56 B Penteschistis pictigluma v var. mannii nrDNA Figure 1. Continued. 314 Annals of the i Missouri Botanical Garden Chaetobromus involucratus ssp. involucratus ) a involucratus ssp. dregeanus — Chaetobromus Hl y Vil B I hi i Austroderia a 1.00 Cortaderia — 2 Cortaderia tu 84*/ 81 / B: 2 Notochloe os nrDNA Notoch MDP326 nrDNA , 11:00! Notochloe microdon AMH66 nrDNA 182 1 68 Plinthanthesis urvillei 1.00 76/65*|«50|r— Plinthanthesis paradoxa 85 / «50 /l K Plinthanthesis rodwayi «0.50 Cortaderia bifida nrDNA «50 1-* | «50 W Cortaderia columbiana nrDNA end. Notochloe Plinthanthesis š š Hal z Cortaderia L 4.00 Cortaderia ju 98 / 98 / 99 initia scule nrDNA Cortaderia pilosa MDP345 Cortaderia pilosa 3 4a Notochloe microdon Watson sn cpDNA ) m Notochloe | Jii Danthonia inn, 0.99 M - 152/70 1.00 D. 79/ <50/59 59 | Danthonia compressa N 95*/«50/91 1.00 Danthonia ae Danthonia a MDP480 cpDNA Danthonia prea MDP481 ina H Š 5 Danthonia re) Danthonia secundiflora Ü Danthonia filifolia — SeeFig. 1d M malacantha 99/61/100 Danthonia chilensis var. chilensis n — var. Dant raucana 100 steps man cue var. aureofulva Figure 1. Continued. Volume 97, Number 3 Linder et al. Classification of Danthonioideae 1.00 100 / <50 / 100 1.00 84/68/90 1.00 95/<50/77 V 100 steps D Figure 1. Continued. Schismus Tenaxia Tribolium Rytidosperma 316 Annals of the Missouri Botanical Garden problem that is not solved through lumping them with the geophytic species in this clade. The clade of geophytic grasses is easy to diagnose by the swollen rhizomes clothed in furry sheaths and Mom Recon this clade a the generic | y to refer to thi habit. Furthermore, it draws attention to their (for grasses) unusual fire biology, flowering in the year after fire and then persisting vegetatively during the interfire periods (Linder & Ellis, 1990b). This biology is well known from Iridaceae, Orchidaceae, and Asparagaceae s.l. in fynbos (le Maitre & Midgley, 1992). Consequently, we erect the genus Geochloa to commodate these species. ac The remaining three species (Merxmuellera arun- dinacea, M. cincta, and M. setacea) do not form a morphologically sensible group. Merxmuellera arun- dinacea and M. cincta are tall, caespitose grasses that share some similarities in the spikelet construction, but these features are not remarkable and could well be plesiomorphic. It would satisfy most generic criteria if we grouped these two together, sd the genus would be difficult to diagnose. Merxmuellera setacea is much more x ekle. h has few characters in common wi are —— The plastid DNA places M. arundi- ated position near the base of the dun (Fig. 1A, node Ci) whereas the nuclear DNA groups it next to the morphologically similar cincta (Fig. 1A, node Cii). While it is clear where the nuclear affinities lie, the d affinities are unclear and could be used to or a segregate gen Indeed, if we only had e Seid DNA. this t have been recognized as a segregate genus. Ecolog- ically, M. arundinacea differs somewhat from the rest of the clade, in that it occupies drier habitats and is mostly found on shale, although it has also been recorded from sandstone-derived soils. The other species are more restricted to sandstone- derived soils. However, this ecological range is not unusual in the Cape flora. Consequently, we choose to group the three age into a new genus, Capeochloa H. P. Linder Barker. This is based on the strong ans similarity be- tween M. arundinacea and M. cincta, thus between two of the three included taxa. It also minimizes the number of monotypic genera and is consistent with the nuclear Eve The implication is that we assume that M. arundinacea is of hybrid origin, with the plastid genome derived from a now extinct lineage that was sister to the rest of the Danthonioi- deae, while the nuclear genome derives from a lineage related to M. cincta. Pentameris clade. Cu rrently, this readily diagnosed clade (Fig. 1B, ncludes three genera Lin Pseudopentameris obusjolia (Hochst.) N. P. Barker (Pirie et al., 2008). nanthium is morphologically unique, with forked multicellular glands and an acute lemma (Davidse, 1988). Although this small genus of three rare, annual species is clearly monophyletic, it is deeply embedded within Pentaschistis and can only be retained at the cost of fragmenting Pentaschistis into many genera. Furthermore, Prionanthium is readily interpreted as a specialized annual Pen- taschistis. We propose to include Prionanthium in Pentaschistis. ' Pentaschistis and Pentameris have been separated since 1830; only Steudel in his Nomenclator Botanicus (1841) placed all known Pentaschistis species under Pentameris. While Pentameris was always recognized as a separate genus, Pentaschistis was, until 1899, a section of the large genus Danthonia. Pentaschistis and Pentameris share several inobobpial charac- ters, such as 2-flowered spikelets, lemma setae borne from the sinus between the lemma lobes and the central awn, and acute paleae with poorly developed keels that do not reach the apex of the palea. They have been separated in the past century by the presence of a villous indumentum on the ovaries and the free, brittle pericarp of the fruits of Pentameris (Barker, 1986). This character combination breaks wn in Pentameris obtusifolia (Hochst.) Schweick., which has a villous ovary and a pericarp that is fused to the seed. There is no morphological evidence for the monophyly of Pentaschistis relative to Pentameris. It is therefore not surprising that molecular data group two Pentaschistis species (P. tysonii Stapf and P. praecox H. P. Linder, Fig. 1B, node Dii) with Pentameris (Fig. 1B, node Diii) rather than Pen- taschistis. This makes it impossible to diagnose the two genera and leads to the suggestion that they should be combined. An alternative solution, which is more conservative nomenclaturally while still retain- ing monophyly, is to transfer P. tysonii and P. praecox to Pentameris. However, we then have two genera (Pentaschistis and Pentameris) that we cannot diag- nose morphologically and that largely overlap ecolog- ically and morphologically. The argument for combining the two genera is that the new, expanded genus would be easy to diagnose, while the various ential segregates are not. Ecologically, they are din: as both occur in the mountains of southern Africa, on oligotrophic soils, in oc heathland or grassland. The habitat of ntameris is a subset of the habitat range of Potosi. The morphological range of Pentameris Volume 97, Number 3 2010 Linder et al. 317 Classification of Danthonioideae is also part of the morphological range of Pentaschis- tis: the only unique Pentameris features are the brittle caryopses with a hairy cap. The strongest counterar- gument to a single large Pentameris is that Pentameris and Pentaschistis have been known as separate entities for almost two centuries, thus largely a historical argument. Indeed, it is not clear why the species of Pentaschistis were grouped as a section of Danthonia, rather than as part of Pentameris. If it had not been for this, there would not have been a problem with combining the two genera. The combined new genus is relatively big (including almost 100 species). oldest name is Pentameris, this also results in many new combinations for the much larger genus Pentaschistis. It is tempting to conserve Pentaschistis over Pentameris ra are not well known and not economically important, the arguments for overriding the priority rule are not convincing. We will retain the distinction, though, by recog- nizing three sections. Chionochloa clade. Zotov (1963) separated Chiono- chloa from Danthonia, based on the deeply grooved leaves with the microhairs along the bases of the grooves, the round silica cells, and the coarse tussocks. The genus is indeed very distinct morpho- logically and also has s lecular support (Fig. 1A, node E). Furthermore, it forms a coherent ecogeographical entity, largely restricted to the more hilly and mountainous parts of New Zealand, with one species on Mt. Kosciuszko in Australia and another on Lord Howe Island in the Tasman Sea. At least the Australian species appears to be derived from New Zealand ancestors (Pirie et al., 2010). Chaetobromus—Pseudopentameris clade. The Cha- etobromus—Pseudopentameris clade (Fig. 1C, node F + G) was recognized in the very first molecular analyses (Barker et al., 1995) and is strongly supported in the analysis of Pirie et al. (2008). Morphologically, the clade can be SUSE W the ey long, ines e pungent calli, th do not mech the tip, and the pales-backs thai are inrolled. so that the keels almost touch each other. habitats and coastal sands (Verboom & Linder, 1998). Pseudopentameris is found along the much melee aonik cont of of southern Africa, where it is found in — bhi on soils. : Danthonia clade. The evidence for the monophyly of the Danthonia clade is ambiguous (Fig. 1C, node W), and neither the nuclear nor the plastid phylogeny explicitly supports the clade. However, combining the two phylogenies suggests that the simplest solution is a Danthonia clade, which includes the genera Dein Plinthanthesis, , , and C. archboldii. This implies a single origin for the very unusual gynodioecious breeding system (Connor, 1979, 1981) in the Danthonioideae, with secondary losses i n Danthonia in Notochloe/ . The iiem i incongruence between the phylogenies based on the nuclear and the plastid genomes is discussed in detail in a separate paper (Pirie et al., 2009). The yly of Danthonia s. str. is not challenged (Fig. 1C, node N). Within the genus there are two different lemma types: in the first the indumentum is restricted to the lemma margins, in the second it is evenly scattered on the lemma back. This could be used as a key for separating Danthonia into two genera, but since the genus is not otherwise heterogeneous (indeed less so than most other danthonioid genera of the same number of species) and occupies a coherent geographical area, we do not support this split. However, the African (D. subulata A. Rich., D. grandiflora Hochst. ex A. Rich.) and Himalayan (D. cumminsii Hook. f., D. cachemyriana Jaub. & Spach) species do not belong in Danthonia, but in the largely African segregates of Merxmuellera included in either Chionochloa (Conert, 1975a) or Cortaderia (Connor & Edgar, 1974) and is morpho- logically intermediate between these two genera (Clayton & Renvoize, 1986). The molecular data set supports the groupi C. archboldii with Danthonia, and more broadly the monophyly of C. archboldii, Cortaderia, and Danthonia (Fig. 1C, node Hii). Thus, are several reasons for not including the species in Danthonia. Danthonia is restricted to America and , and €. archboldii is found on the island of Mer Cua It makes sense to attempt to define genera that are y and that do not show such massive disjunctions. However, in itself from the sheaths and are tough and sclerophyllous. Such tough, fibrous leaves do not otherwise occur in Danthonia. Also, the lemma structure is very ss eee io asia see sender, Annals of the Missouri Botanical Garden with three (or rarely five) veins, and with the lemma lobes absent or very poorly developed. Such lemmas are typical of Cortaderia. In Danthonia the lemmas ap eed and "e. TAE seven ° nine wan and ] The inflorescente | in C. arshhoidi PE 50 to 150 spikelets, and altho it is not plumose, it is certainly widely open and paniculate. In Danthonia in general, the inflorescences have fewer than 50 spikelets and tend to be linear or lanceolate and somewhat more compact. Cortaderia archboldii a ious breeding system (Connor, 1970), as is Pee found in Cortaderia, but not in Danthonia The morphological and anatomical cde is clearly against pasas archboldii being included in Danthonia ting rather a grouping with Cortaderia. malate ij molecular evidence conclu- sively rejects the monophyly of Cortaderia pace C. archboldii. Consequently, we recognize a genus, Chimaerochloa H. P. Linder, for C. RA The small eastern Australian genera Plinthanthesis and Notochloe are retrieved as clades in both genomic partitions. In agreement with the leaf anatomical data, the nuclear genome places the two genera as sisters E 1C, node Ji). However, the plastid data group with Cortaderia pilosa (Fig. 1C, node Jii + L) xat Plinthanthesis with the New Zealand species of Cortaderia. We follow the anatomical (unpublished data) and nuclear data and propose a sister-taxon relationship between Plinthanthesis and Notochloe. This is also corroborated by ecogeographical data: both taxa are found in pyrophytic heathy vegetation on oligotrophic soils, typical of the Sydney sandstones in Australia. Although Notochloe is monotypic, we retain the two genera because the three species of Plinthanthesis form a clade and the two genera are readily diagnosed by the spikelet structure, so there is no good reason for upsetting an established taxonomy Cortaderia presents a number of problems. The disintegration of Cortaderia into a South America clade (Cortaderia s. str., Fig. 1C, nodes Hi and Hii) and a New Zealand clade (Austroderia, Fig. 1C, node I) as first reported by Barker et al. (2003), and extended here, is surprising. These large grasses are very similar in their general appearance as well as in their detailed spikelet structure, with single-veined glumes, pilose lemmas, reduced lemma venation, and absent or poorly developed lemma lobes anatomical differences provide morphological support for the segregation between these two genera (the New Zealand segregate has multiple-veined leaves, while the South American segregate has leaves with a single im and e by Histo would os have been wever, cese i is molecular Mam for inks a division, albeit in some ways ambiguous, from both the plastid and the nuclear partitions. Consequently, on the basis of recognizing monophyletic genera, we have chosen to retain Cortaderia for the South American species and to erect a new genus, Austroderia N. P. Barker & H. p. Linder, to accommodate the New Zealand species. Lamprothyrsus is deeply embedded within the South A Y : Za oa Es AN LT th e O J : Li 1 1 1 1 aci „itis is immediately Furthermore, —— Ar — force a radical fragmentation of Cortaderia. Lamprothyrsus shares many vegetative and spikelet characters with , thus we include both in the same genus. More difficult to resolve is the position of the southern South America Cortaderia pilosa. The nuclear partition is uninformative: the species is placed in ina "n with the bulk of the species of g. 1C). The plastid partition (Fig. 1C) Notochloe, in the surprising (Plinthanthesis—Austroderia). It is evident that the nuclear genome does not d the monophyly of Cortaderia including C. pilosa, i rejects the TODE of Cortaderia including C. pilosa. Consequently, the inclusion of C. pilosa in Cortaderia implies that the plastid genome is misleading. This is possibly the result of hybridiza- tion, a scenario put forward to explain the situation in Notochloe and Merxmuellera arundinacea. We can test this by searching for more nuclear sequence data, which can either support or contradict a potential nuclear relationship of C. pilosa-Cortaderia. This is currently only a Poeni E since the nuclear data set neither ecologically so similar that if they were reciprocally monophyletic sister-taxa, it would be difficult to justify recognition of two separate genera. Consequently, the phylogenetically conservative approach would be to place C. pilosa in a separate g, ince th iprocal monophyly of C. pilosa and Cortaderia is not contradicted by either data set. By placing it in its own genus, the monophyly requirement is met in both A partitions. However, this is a very reductionist position: by placing each species in its own genus, monophyly will never be violated. Hence, we argue that the morphologically and nomenclaturally conservative option is to include C. pilosa in Cortaderia. This is also consistent with the treatment of M. arundinacea. Consequently, we follow that option here. Rytidosperma clade. The monophyly of the Rytidos- perma clade (Fig. 1D, node 0), comprising all species of Austrodanthonia H. P. Linder, Joycea, Karroochloa, Linder et al. 319 Classification of Danthonioideae id nuin h ically diverse (e species with and without awns, annuals and . diverse lemma morphologies, etc). A single genus thus defined would lack homogeneity and would also be cytologically very heterogeneous. The morphological characters, which may be used to define the clade, have very numerous exceptions, and the genus would be very difficult to di In order to minimize taxonomic change, and in favor of morphological homogeneity, we have therefore opted to retain the existing African segregate genera (transferring taxa where necessary to ensure generic monophyly). Under this option at least three African genera need to be : Tenaxia, Schismus. and Tribolium. Necessary changes include (1) the transfer of Karroochloa schismoides (Stapf ex Conert) Conert & Tiirpe to Schismus, (2) th binati í Ki hi wish Tribolium, and (3) the establishment of a new genus, Tenaxia, to accommodate Danthonia myriana, D. cumminsii, D. subulata, Schismus is based entirely on the molecular phylog- p t from both DNA partitions (nodes P and Q. respectively, in Fig. 1D). However, the situation is less clear in the case of Tribolium. The variation in this genus would also be consistent with the oaii d ie m (Nees) Renvoize and T. © very distinctive growth form. Thibsliam (Pig. 1D, but all species in Tribolium s. str. have hispid glumes, often Clearly, the three do. Tribolium s... (Fig. 1D, node) would be more AU S but it would still be morphologically and ecogeogra- phically homogeneous. This solution also has the define a larger genus, Tribolium s.l., and recognize the three segregates at sectional rank. There have been numerous and different delimita- tions of Rytidosperma. The Australasian species included here in the genus were separated into Austrodanthonia, Rytidosperma, Notodanthonia, and je by pede Verboom (1996). This was based attributes. the segregates were based largely on the pattems of and the relative sizes of the callus (Fig. 1D, nodo V), roaring to an extrsúed val 1* 7107 southem entity distinguished from its norihem coun- ¿Ti L -ag ak lI Ë " è T ee tn We mapped the most over a simplified Taxonomic TREATMENT a. (Appendix 2). The relevent new NN es pintas aos ame band. Pel D ate E be mede availeble in H synonymy leading to Ps ad Annals of the 320 ent Botanical Garden 5 G -— Merxmuellera 24 b Capeochloa w Lon Geochloa ' Pentameris 1 0 1 4— C hionochloa 31171 z J&5— Chaetobromus Pseudopentameris 0 1 Tenaxia 13 20 : Yd v S chis mus 2 R ytidos perma [:] Š ° Tribolium 0 a Aus troderia : iv Notochloe HAL 15 18 3 " 1 12 15 011 Oa Plinthanthes is 10 1 2 Cortaderia t5 12 ° s D2000— Danthonia T 001 9 Chimaerochloa Figure 2. Simplified ~~ hie genera as s terminals indicated above the squares, the state below The key to the genera presented below should not be treated as a strict, analytical key that will assign all species to their correct genera. Instead, we aim to indicate the concept of the genera. It is important to use all characters in the couplets. These might be contra- dictory for some species and we recommend that you follow the majority case (e.g., the lead that has the most attributes that fit). The reason for this is that in many of the genera unique attributes are lost in several species, and a key that attempts to take these individually into account would soon be a key to the species the squares. are 6 changes; e homoplasious. The character ndi and their states are listed in Table l a Appen and vae E mapped. The character numbers ar Filled-in es mpty squares are dix KEY TO THE GENERA OF THE DANTHONIOIDEAE la. — with 2(1) florets with a minute a n; palea keels parallel; setae inserted i uses en lemma lobes and awns ........ 2 lb. Spikelets generally with more than 2 florets, if only h a well-developed rachilla extension; ea keels sinuose; setae when present at apic of lemma lobes VI. Ps Pseudopentameris 2b. Glumes — less than 25 mm E plants I with multicellular glands IV. Pentameris s dc cu il TAN RR N iae 5 ido iaa PAN Ea ere eee PES A Ey EME Senay eee Eke DE N NA E A eC TE E ld Volume 97, Number 3 Linder et al. 321 2010 Classification of Danthonioideae Table 1. Morphol ogical ch t d th o” tree (Fig. 2). States between parentheses polymorphic and le the states cri for that samin Debes indicate missing data or inapplicable states. Morphological characters and character states are described in Appendix 1 Ca, 010100(01)0021100(01) 10(01) 100 Chaetobromus 010100100111000011101 Chionochloa 11011010121100010(01) «ou Austroderia 110102110210001(01)01(01)0 Cortaderia 110111100210001(01)0(01) (01) 00 Danthonia 0(01)010010021100000(01)-01 Geoci 011100100211000101100 Chimaerochloa 110110100210000001000 Merxmuellera 01012000021120(01)00(01)100 Notochloe 010100110211301001101 Pe 010(01)0010020101000(01) (01)0(01) Plinthanthesis 010100110211000000101 Pseudopentameris 01010010020101001(01 Rytidosperma See En e Schismus 010100100(12)11200(01)0(01)0 Tenaxia 010100(01)002112000010(01)0 Tribolium 010100100(02)1100(01)(01)0(01)(01)11 3a. Lemmas with lto 3(to pen veins; lemma apex ret or 9b. Spikelets never e tuft of hair at a disarticu- lation point pedicel; basal florets same as setae usually p t but small; g tly with upper Res. ees ave ee be we 10 one i" sp us ordioecious ...... 4 10a. Callus shorter than rachilla; joint to “sama 3b. 5 to 9(to d ecd lemma apex horizontal; caryopsis turbinate; native to e lobed, eat generally e] EB sc seu. o dicic ciae 11 lobes; glumes — vith more gea one vein; 10b. r than rachilla; joint oblique; cary- ue generally hisewal e ee a 6 opeis lorate-cylindrical o 12 4a. awn prie into column and limb; lla. Spikelets with 2 to ] dorsally w lemma lateral lobes well developed; plants up to a shoni, desee indumentum . .... X. Plinthanthesis 4 m tall; from New Guinea ... XII. Chimaerochloa — |]h, Spikelets with 7 to 9 florets; lemmas dorsally 4b. Lawana i wn not n into col Mie o. s eese veniri XE Notochlae limb; lomma lateral lobes not distinct; plants 12a. ea ate embryo mark less than 2/5 of ore than m tall; from New: Zenda or Sou th porno... 99 «Wa »bere9t$9vveoese94.998894*9* o Rb ee be be a re eS ee > st rd» e rs 5 12b. LT ii k 1 h oj. f 5a. with several wide, strongly sclerified caryo ix o ee o Te 14 veins € midrib) surrounding fine, indis- 13a Planta with cleistorenes: leaves ortho- tinctly sclerified veins; from New Zealand phyllous, ant onna n ng shore the e gules a eee ee ce IX. Austroderia i Nee . Vii hn 5b. Leaves with only the midrib prominent and 13b. Plants without concen leaves M strongly sclerified; from South DUM Boos lous, generally disarticulating above the ligules; Gd n EE per ees : UT remaining leaf bases often split into 2 recurving 6a. Palea flaps often with long hair; n with abus: dich Ju Mire “rela scattered indumentum... ej ES inda E 14a. ei wate to the Pacific ma m pm or €— flaps usually glabrous; n wena higher; lemma in ir ndumentum often in 2 rows ° tuits (with g ) te Generar nm RE SR cmap ee ` RVI. Ber 7b. Tall a plants, or if geophytes, then leaf 14b. — at T. = id uS Uu I Epi i ees Eod oos e. Leaf blades often disuicuating pas pa 15a. Glumes with tubercle-besed hairs or plants Pise cid "e densa keel: in pent on stoloniferous or inflorescence spicate; lemmas Too aT a Chionochloa a d LM E. ue E umes lacking t e- ç on- sp: und Á ici am a iferous, and if the inflorescence is spicate then or evenly sca ttered on the lemma back, or the lemmas have well-developed awns ....... 16 largely as rows; native to Africa 16a. r awn usually ie he 5 III. Capeochloa shorter than the lobes; plants less than 0.35 m 9a. Spikelets with tuft of hair from a ation € o A n., XV. Schismus point along l; basal florets different from 16b. Lemmas lobed; plants 0.12-0.9 m tall; me upper floreta .............. VH. Choetobrome — poema ........................ XIV. Tenaxia Annals of the Missouri Botanical Garden Figure - Me anii. —A. Spikelet. —B. Lemma. Palea. Drawn by Jasmin fein from Schuette in iM 30869. I. Merxmuellera Conert, Senckenberg. Biol. 51: 129. 1970. TYPE: Merxmuellera davyi (C. E. Hubb.) Conert (= Danthonia davyi C. E. Hubb.). Figure 3. Caespitose, perennial grasses without stolons, culms 0.3-1.5 m tall. Sheaths + persistent, not variously lacerated or fragmenting; ligule ciliate; leaf blades setaceous or expanded, sclerophyllous, tough, glabrous, occasionally with a weftlike indumentum on the upper surface directly above the ligule; mostly disarticulating 10-20 mm above the ligule leaving a short stub that is either entire or split, straight or more usually recurved. Inflorescences + paniculate, mostly open or more rarely contracted or linear. Spikelets usually with more than 2 florets, all similar and bisexual; glumes shorter to longer than the florets, with 1 to 3 nerves, glabrous or micro-scaberulose, 7— 35 mm; callus rounded or truncate, villous, shorter or longer than the rachilla internode; lemmas with 7 or 9 veins; lemma dorsal indumentum as 3 hair tufts arranged in a diagonal stripe from the midrib to the rarely fused to the central awn; central awn always present and exceeding the lemma lobes, sometimes differentiated into a flat, corkscrewed base and a straight, hairlike apical part; palea linear, without tufts of hair on the palea flaps; lodicules rhomboid, lodicule upper margin fringed with numerous bristle hairs shorter than the body of the lodicule, microhairs apparently absent; ovary glabrous. Caryopsis + elliptical, embryo and linear hilum ca. 1/2 the caryopsis length. Cytology. Unknown. Anatomy. The leaves are sclerophyllous; adaxial ribs variously developed; adaxial sclerenchyma as massive T-shaped or inversely anchor-shaped girders associated with both 1- and 3-order vascular bundles; leaves asymmetrical with one side with more vascular bundles than the other; clear cells in the chlorenchy- ma absent; adaxial bulliform cells present in the grooves. Distribution and habitat. These are Afromontane tussock grasses. They are most common in montane grassland in Africa and Madagascar, usually in areas with a higher rainfall. Generally, they seem to be absent from bogs or waterlogged soils, but also avoid asonally dry, freely draining habitats. These drier hoftes are typically occupied by species of Tenaxia. These grasslands are subjected to regular fire (two- to four-year cycles) and often to frost in winter. Discussion. This genus is relatively clearly delim- ited, but no characters apply to all species. In all species except Merxmuellera stereophylla (J. G. Anderson) Conert, the leaf blade breaks off above the ligule and the remaining stub sometimes splits, metimes often curls or spirals. This attribute is unique to this genus in the Danthonioi- most species the awn lacks a clear separation into id and limb. Although the lower portion of the awn.can corkscrew, it is not clearly differentiated from the upper portion of the awn. However, the egree of development of the column is a matter of interpretation. All species except M. stereophylla have a lemma indumentum organized into a diagonal stripe with ca. three tufts flanking the midvein of the lemmas. In M. stereophylla this pattern is somewhat simplified and can be interpreted as derived from the diagonal stripe of three tufts. The leaf blades are most often folded (thus setaceous) and are always sclerophyllous. Merxmuellera grandiflora may be an exception, as it has not yet been investigated anatomically. The lodicules are rhomboid (triangu- lar), quite hairy in the upper half. Similar lodicules are also found in various other genera, often not in all species, but are smaller than those of C not, an = Volume 97, Number 3 2010 Linder et al i 323 Classification of Danthonioideae chloa, where they are developed to quite massive ructures. ncluded species. We include seven species in Mona which is part e species originally assigned to the genus br Conert (1970, 1975b, 1987) and as treated by Barker (Gibbs Russell et al., 1990). 1. Merxmue ambalav. (A. Camus) Conert, OA. Biol. Sl: 12 132. 1970. 2. Merxmuellera davyi (C. E. Hubb.) Conert, Senckenberg. "Biol. "St: 132. 1970. 3. Merxmuellera drakensberge ‘oe Conert, Senckenberg. Biol. 51: 132.1 1970. 4. Merxmuellera grandiflora (Hochst. ex A. Rich.) H. P. Linder, comb. nov. Basionym: Danthonia grandiflora Hochst. ex A. Rich., acbr., Rytidosperma in (Hochst. ex A. Rich.) S. M. Phillips, Fl. Ethiopia & Eritrea 7: 74. 1995. TYPE: Ethiopia. “in monte Silke ad rupes,” 16 Feb. 1840, W. G. Schimper 690 (holotype, P not seen; isotypes, BM!, GOET!, K!, S!, TCD!, Z!). 5. Merxm owanii (Stapf) Conert, Ll "Biol. si: 132. 1970. 6. Merxmuellera stereophylla (J. G. Anderson) Conert, Senckenberg. Biol. 51: 133. 1970. 7. Merxmuellera tsaratananensis (A. Camus) Conert, Sen henley Biol. 51: 133. 1970. Il. Geochloa H. P. Linder & N. P. Barker, gen. nov. TYPE: Geochloa lupulina (L. f.) H. P. Linder & N. P. Barker (= Avena lupulina L. f.). Danthonia DC. sect. Himantochaete Nees, Fl. Afr. A Ill. 323. 1841. TYPE: Danthonia rufa (= Geochloa rufa (Nees) N. P. Barker & H. P. ire (lectotype, designated here). novum Genus Merxmuellerae affine qua rhizomatibus tumidis, vaginis foliaribus afa ia lantis et ne ve plerumque compactis differt Plants perennial, tufted geophytes without stolons; rhizomes short, — with swollen nodes forming perennating organs, encased in persistent, an sheaths; culms 0350. 75 m tall. Ligule with 1 or several rows of cilia; leaf blades expanded or o tough. Inflorescence mostly compact, contracted, ovate, more rarely open; inflorescence branches mostly shorter than the spikelets; indumentum glabrous or puberulent. Spikelets with 2 to 7 florets, all similar and bisexual; glumes similar, at least as long as the florets, with 1 to 5 veins, 7-55 mm; callus blunt, villous, about as long as the rachilla internode; lemmas with 9 veins, with a scattered dorsal indumentum that may be longer below the sinus and me shorter toward the base of the lemma; lemma lobes sometimes extended into up to 2-mm setae plus lobes 4.5-9 mm; central awn 4—20 mm, longer than the setae, the basal half forming a distinct column, straight or corkscrewed many times; paleae shorter than or overtopping the lemma sinus, glabrous to villous between the keels; palea keel flaps infolded with tufts of hair; lodicules rhomboid, with 3 veins, bristles shorter than the lodicules; microhairs absent. aryopses obovate, shiny; hilum linear, less than 1/4 of caryopsis length. Nomenclatural note. Nees included in section Himanutochaete all African Danthonia species, except Pentaschistis. ue concept of the section was panded in Bentham and Hooker (1883) t "e genus. E ME any of the ds African species included by Nees could be used as type. We selected D. rufa, as almost all species in the genus Geochloa are listed by Nees under section Himantochloa. Nees did not explicitly assign a rank to his infrageneric groups (Pentaschistis, Himanto- chaete); we interpret them here at sectional rank, rather than as subgenera Cytology. 2n = 48. This has been counted only for Geochloa decora (Nees) N. P. Barker & H. P. Linder (Du Pressis, pers. comm.). Anatomy. The leaves are sclerophyllous; adaxial ribs variously developed, often massive, separated by narrow clefts; adaxial sclerenchyma as T-shaped or a anchor-s ers associated with both 1- -order vascular bundles; leaves symmetrical; adaxial bulliform cells present. — - habitat. All three Geochloa are cted to the Cape Floristic Region Cola. 1978. panis et al., 2006), where they are idespread in the lowlands and mountains. d occur on both sandstone- and shale- derived substrates, and consequently in both fynbos and renosterveld vegetation, in well-drained habitats, or lowland areas with some impeded drainage. The piniis typically over i in w first m she: fire, and y egetatior 1. aioa the leaves are visible. The fire cycle in this vegetation is between six and 50 years, which results in relatively rare flowering events for some populations. 324 Annals of the Missouri Botanical Garden Discussion. The small genus Geochloa shares with Capeochloa cited: chu rhomboid- bristled lodicules, and paleae with pilose margins. However, it can be diagnosed by several attributes. The plants are geophytes, with swollen rhizomes storing starch, and encased in woolly leaf sheaths. Geophytes are occasional in the grass flora of the Cape (Linder & Ellis, 1990b), but Geochloa can be separated from the geophytic Pentameris aristi- doides (Thunb.) Galley & H. P. Linder by the 2- flowered spikelets of the latter, and from the more closely related geophytic C. setacea (N. P. Barker) N. P. Barker & H. P. Linder by the shiny glabrous basal sheaths. In two of the three species, the inflorescence is contracted into a compact ovate structure; only in G. decora does it spread more “ase during anthesis. ymolo, e name refers to the geophytic ids of the plants in this genus. This habit is unusual in the grasses and seems particularly characteristic of the three species in Geochloa. Included species. The three species included in this genus were originally classified in Danthonia (Stapf, 1899; Chippendall, 1955). They were then transferred to Merxmuellera by Conert (1971), a treatment also followed in southern Africa (Gibbs Russell et al., 1990). 1. Geochloa decora (Nees) N. P. Barker & H. P. Linder, comb. nov. Basionym: Danthonia decora Nees, Fl. Afr. Austral. Ill. 332. 1841. Merxmuel- lera decora (Nees) Conert, Mitt. Bot. Staats- samml. München 10: 306. 1971. TYPE: South Africa. s. loc., s.d., J. F. Drège 5651 (holotype, B not seen; isotype, B fragm. at FR!). Danthonia zeyheriana Steud., Syn. Pl. Glumac. 1: 244. 1854. TYPE: South Africa. Cape Province: Swellendam Division, Puspas Valley, s.d., C. L. P. Zeyher 4555 or 4556 (types, HBG!, K!, MO not seen, PRE!). Danthonia pac Steud. var. trichostachya Stapf, Fl. Cap. (Harvey) 7: 522. 1899. TYPE: South Africa. Cape Province: Cape Division, betw. Slang Kop & Red Hill H. Wolley-Dod 3 s.d., A. 3002 (lectotype, designated here, K!). ears listed two collections as syntypes: Wolley-Dod Wolley-Dod 3002; the latter is selected as eae because it is a more complete specimen. 2. Geochloa lupulina (L. f.) N. P. Barker & H. P. Linder, comb. nov. Basionym: Avena lupulina L. f., Suppl. Pl.: 113. 1781. Danthonia lupulina (L. f.) P. Beauv. ex Roem. & Schult., Syst. Veg. ed. 16 (Sprengel) 2: 690. 1817. Merxmuellera lupulina (L. f) Conert, Mitt. Bot. Staatssamml. München 10: 306. 1971. Danthonia coronata Trin., Mém. Acad. Imp. Sci. St.-Pétersbourg, Sér. 6, Sci. Math. 1: 70. 1831. TYPE: [South Africa.] Cape of Good Hope, s.d., C. P. Thunberg s.n. (lectotype, designated here, UPS 2604!; isotype, S! Based on the assumption that the top set of Thunberg's collections are indeed in his herbarium, and that he, rather than Linnaeus filius, wrote the descriptions of the Cape plants described in the Supplementum Plantarum, we designate the UPS collection as lectotype. 3. Geochloa rufa (Nees) N. P. Barker & H. P. Linder, comb. nov. Basionym: Danthonia rufa Nees, Fl. Afr. Austral. Ill. 330. 1841. Merxmuel- lera rufa (Nees) on Mitt. Bot. Staatssamml. Miinchen 10: 306. 1971. TYPE: [South Africa.] "In iugi bad hes monte Blaauwberg locis saxosis alt. 4000'," s.d., J. F. Drège 2559 (type, PRE!). Avena lanata Schrad., Gött. Gel. Anz. 3: 2075. 1821, nom. hrad. jtd Man. (Schultes) 2: 386. 1824. TYPE: South pe Province: Cape Town, s.d., Hesse s.n. M COET 23223). Danthonia macrocephala Stapf, Fl. Cap. (Harvey) 7: 522. 1899. TYPE: [South Africa.] s. loc. [probably from Caledon, Tulbagh, or Clanwilliam Division], s.d., Thom s.n. (holotype, K!). IIl. Capeochloa H. P. Linder & N. P. Barker, gen. nov. TYPE: Capeochloa cincta (Nees) N. P. r & H. P. Linder (= Danthonia cincta Nees). Figur m quod a Merxmuellera Conert indumento matis non caespitoso et phloemate cellulis scleroticis destituto, a Geochloa H. P. Linder & N arker vaginis foliaribus basalibus glabratis recedit. Plants perennial, tufted, without stolons; culms 0.5-2.5 m tall; basal sheath either of leaf remnants, or of white shiny persistent leaf bases. Ligule either a simple or multiple row of cilia; leaf blades tough, expanded or inrolled, sometimes adaxially with a web of interlocking hairs above the ligule, some- times pungent. Inflorescence open to plumose, with up to 200 spikelets, ovate or elliptical; inflorescence branches glabrous, seaberulose or villous. Spikelets with 2 to 4 fertile and bisexual florets; glumes at least as long as the florets, 8-23 mm upper and lower glumes similar, with 1 vein; ade blunt, villous, as long as the rachilla internode; lemma 2.5-5 mm, bilobed, villous with the hairs either Volume 97, Number 3 Linder et al. 325 2010 Classification of Danthonioideae | | 1mm z Z Z Z ` à x Figure 4. . —A. Spikelet. —B. Lemma back. —C. Palea. —D. Gynoecium. —E. Anthers. —F. Ç Lodicules. Drawn € sia Gd Ecklon & Zeyher 4548. — Annals of the Missouri Botanical Garden scattered over the backs, or longer along the lemma margin, or in a row across the lemma backs; lemma lobes acute to acuminate, sometimes with setae to 5 mm; lemma awn 5.5-17 mm, geniculate, with a 3— 4.5 mm, + twisted column base; palea truncate to bilobed, longer than the lemma sinus, with sinuose never with microhairs, obtriangular or rhomboid, with 3 to 4 veins; anthers 2-3.2 mm. Caryopsis not known. Cytology. 2n = 12, 36 (de Wet, 1954). y. The leaves are sclerophyllous; adaxial ribs variously developed; adaxial sclerenchyma as massive T-shaped or inversely anchor-shaped girders associated with both 1- and 3-order vascular bundles; clear cells in the chlorenchyma are absent, and the grooves contain bulliform cells. Distribution and habitat. The genus is restricted to the Cape Floristic Region, where the species are found both in the lowlands and mountains. Most populations are on sandstone, but Capeochloa arundinacea (P. J. Bergius) N. P. Barker & H. P. Linder is also found on shales and can locally be a typical element in renosterveld vegetation. The geophytic species seems to flower only after fire, while the two large tussocks usually flower every year (except for some western populations of C. cincta). All species are restricted to shrubland or heathland and are absent from grassland. Discussion. This genus lacks unique morphologi- cal markers but has a number of unusual attributes. One of the three species is a geophyte, and the remaining two are robust tufted perennials. The genus can be separated from Geochloa by the glabrous plant bases and by the inflorescences, which are always open panicles. Both Capeochloa and Geochloa can be separated from Merxmuellera s. str. by the lemma indumentum never being tufted, by the usually wider leaves (more than 3 mm wide), by the absence of sclerosed cells in the phloem, and by the regular presence of tertiary vascular bundles between all primary vascular bundles. They all seem to have diamond-shaped lodicules, where the bristles are shorter than the lodicule, and the whole structure is antial, about as big as the ovary. This could be unique but is difficult to clearly delimit from other, similar, structures in other genera. Furthermore, we have little data on variation within the species. The lodicules are larger than those in Merxmuellera. The arundinacea it is more or less evenly scattered over the back of the lemma; C. cincta has a line of long hairs below the lemma sinus and with no hair toward the lemma base; and C. setacea has only marginal tufts, while the rest of the lemma is glabrous. All species (except C. cincta subsp. cincta) have tufts of hair on the palea margins; these usually developed as a line of hairs. This feature is widespread in the subfamily, especially in Rytidosperma and its allies. Capeochloa, Geochloa, and Chionochloa seem to be the only genera in which this feature is found in almost all species. Etymology. The name refers to the geographical center for the genus, as characteristic of the Cape flora. Included species. The four taxa, including three species, were initially classified in Danthonia (Stapf, 1899; Chippendall, 1955) before being transferred to Merxmuellera (Conert, 1970). Their inclusion in Merxmuellera has been generally accepted (Gibbs Russell et al., 1990). 1. Capeochloa arundinacea (P. J. Bergius) N. P. Barker € H. P. Linder, comb. nov. Basionym: | Andropogon arundinaceus P. J. Bergius, Descr. PI. Cap. 356. 1767, non Andropogon arundina- ceus Scop., Fl. Carniol., ed. 2, 2: 274. 1772, nom. illeg. Andropogon bergii Roem. & Schultes, Syst. Veg. ed. 15 bis (Roemer & Schultes) 2: 813. 1817, nom superfl. Danthonia arundinacea (P. J. Bergius) Schweick., Notizbl. Bot. Gart. Berlin- Dahlem 14 , non Danthonia arundinacea Steud., Nomencl. Bot., ed. 2, 1: 482. 1840. Merxmuellera arundinacea (P. J. Bergius) Conert, Senckenberg. Biol. 51: 132. 1970. TYPE: [South Africa.] s. loc., s.d., s. coll. (holotype, SBT!). Avena elephantina Thunb., Prodr. Pl. Cap. 23 Ill. 334. 1841. TYPE: South Altea, Swartland, s.d., Thunberg (lectotype, designated here, UPS 2593!). There are two specimens in the Thunberg herbar- ium: UPS 2593 and UPS 2594. These might be isotypes or they could be syntypes. Of these two collections, the former is selected as lectotype, as it is a better specimen. 2. Capeochloa cincta (Nees) N. P. Barker & H. P. Linder, comb. nov. Basionym: Danthonia cincta Nees, Fl. Afr. Austral. Ill. 332. 1841. Merxmuel- lera cincta (Nees) Conert, Senckenberg. Biol. 51: 132. 1970. TYPE: [South Africa.] *In Promotorio bonae spei, Reeves in Herb. Lindley," s.d ., Reeves s.n. (lectotype, designated by Conert [1970: 132], K not seen). 2a. Capeochloa cincta (Nees) N. P. Barker & H. P. Linder subsp. eineta. RA A u Se, i cU. a M cs Cras | kai a eh Lcd a E eia Volume 97, Number 3 2010 Linder et al. 327 Classification of Danthonioideae Figure 5. Pentameris curvifolia. —A. Spikelet. —B. Lemma back, —C. Palea. Drawn by Jasmin Baumann from MacOwan 1695. 2b. Capeochloa cincta (Nees) N. P. Barker & H. P. Linder subsp. sericea (N. P. Barker) N. P. Barker & H. P. Linder, comb. nov. Basionym: Merxmuellera cincta (Nees) Conert subsp. sericea N. P. Barker, S. African J. Bot. 65: 105. 1999. TYPE: South Africa. Eastern Cape: Rufanes river mouth, 9 Nov. 1997, N. P. Barker 1545 (holotype, GRA!; isotypes, BOL!, K!, MO!, NBG!, PRE!). 3. Capeochloa setacea (N. P. ae NP Barker & H. P. Linder, comb. nov. : Merx N. P. Barker, E 21: 27. Winterhoek Wilderness Area, s.d., R. P. Ellis 5500 (holotype, PRE!) IV. Pentameris P. Beauv., Ess. Agrostogr. 92, tab. 18, fig. viii. 1812. Danthonia DC. sect. Penta- meris (P. Beauv.) Steud., Syn. Pl. Glumac. 1: 238. 1855. TYPE: Pentameris thuarii P. Beauv. Figure 5. Prionanthium Desv., MS Sci. Phys. Nat. 64. 1831. TYPE: Prionanthium Desv. (= Pentameris dentata (L. f.) Galley & H. P. Linder). hne Nees, Intr. Nat. Syst. Bot., ed. 2 1836. Nees, Fl. Afr. Austral. nm. di 1841, nom. superfl. TYPE: ecklonii Nees (= sae ecklonii (Nees) Galley & H. P. Linder). Danthonia sect. Pentaschistis Nees, Index Seminum (Vra- Afr. A na aristidoides Thunb., is aristi- e (Thunb) Galley & H. P. aa (lectotype, designated jd Phillips [1951: 121]). Poagrostis Stapf, Fl. Cap. (Harvey) 7: 760. 1900. TYPE: pe pusilla (Nees) Stapf (= l. emo don] Mans ex Benth. & Hook... f Cox PL 3.1158. £ & Hook. f., 1883. TYPE: Achneria microphylla (Nees) T. Durand s poe vu Eriachne microphylla Nees, hylla (Nees) Galley & H. P. Linder) tala pie here). ants annual, biennial, or perennial, caespitose, mat-forming, geophytic, or suffrutescent, sometimes with rhizomes or nece culms up to uw m o Plants often with llul on the leaves, inflorescences, or imt Sheath + persistent, not variously lacerated o ligule a simple line of cilia; leaf blades iilis or sclerophyllous, expanded or setaceo occasionally with a weftlike indumentum on ie eae surface directly above the ligule. orescences paniculate and open, contracted, or linear. Spikelets with 2 or rarely 1 floret(s), all similar and bisexual; glumes longer than the florets, 2-25 mm, with 1 to 7 nerves, glabrou micro-scaberulose, rarely with tufts of long has: URS rounded or truncate, villous, short; lemmas with 3 to 9 indistinct veins, dorsally pilose; lemma lobes weakly developed, acute, trun- cate, or lacerate; setae originating between the lobes and the central awn, often very long and exserted from the glumes; central awn absent or more usually present and exceeding the lemma lobes, generally Jifeventisied into a flat, corkscrewed base and a ight, hairlike apical part; paleae linear, without tufts of hair on the palea margins, these not infolded, the 2 keels poorly developed, straight, and sometimes not e palea apex; lodicules cuneate, ah without microhairs or bristles; ovary gla- brous or with a hairy cap. Seed a caryopsis or achene (thus with free pericarp), + elliptical; embryo about 1/2 the length of the caryopsis; hilum usually linear to rarely punctate, up to 6/10 of the caryopsis length. + linear UL Nomenclatural note on Pentaschistis. | Pentaschistis was first mentioned as an unranked division of the genus Danthonia by Nees (1835) in a seed list, which was probably published at the end of 1835 or the beginning of 1836. He also listed the name in the second edition of Lindleys A Natural System of Annals of the Missouri Botanical Garden Botany (Lindley, 1836), which was published in July 1836. The name was validated, but again without explicit rank, on p. 280 in the Florae Africae Australioris, Illustrationis monographicae, I. Grami- neae (Nees, 1841). The combination at generic rank was then made by Spach in 1846. The rank of Nees’s name is unclear, but is between species and genus. Because subgenera were rarely used in the 19th century and sections were commonly used, we interpret the name at sectional rank. The typification is difficult. Nees, in the seed list, included only D. glandulosa Schrad. in section Pentaschistis. However, typification is also followed by the Index Nominum Genericorum. Although this species was included under Danthonia sect. Pentaschistis by Nees in 1841, he gave it the illegitimate name of D. trichotoma Nees, including Avena aristidoides Thunb. in synonymy. As such, the lectotypification is valid and should be followed, even if P. glandulosa would have been a more satisfactory type, as it was included at the first mention of the new taxon by Nees. Nomenclatural note on Achneria. Munro in Har- vey (1968) transferred the African species that Nees (1841) had grouped under Eriachne R. Br. into Achneria P. Beauv. This was based on an incorrect ransferred to Achneria constituted a new genus, so they changed the concept of Achneria by reducing Achneria P. Beauv. into Eriachne and keeping the African Species under Achneria sensu Munro. Bentham therefore recognized à new genus and gave it an invalid, homonymic name. Sprague (1922) correctly interpreted the situation and proposed the new name Afrachneria for Achneria Munro ex Benth. & Hook. f. Munro recognized seven species in Eriachne but did not list them. Here we select a typical species, which would have been known to Munro, as lectotype. Cytology. 2n = 14, 24, 26, 28, 40, 42, 52, 56, 91 (Hedberg, 1957; de Wet, 1960; Tateoka, 1965; Davidse et al., 1986; Davidse, 1988; Spies & du Plessis, 1988; Spies et al., 1990; du Plessis & Spies, 1992). Anatomy. The leaves are orthophyllous or scler- 1- and 3-order vascular bundles; clear cells in the chlorenchyma absent; bulliform cells present in the ial grooves. Distribution and habitat. This is a typical element of the Afrotemperate flora (Linder, 1990; Galley et al., ith a concentration of species in the Cape , Floristic Region, but it is also common in the w Ethiopian uplands in the northeast, and Amsterdam Island in the Indian Ocean. Several species have been introduced into Australia, where they have become weedy (Linder, 2005). This is a distribution pattern that is common for several Cape floral elements, such as the orchid genus Disa and several genera of the Iridaceae, such as Moraea and Gladiolus L. Most species of Pentameris are found in the Cape Floristic Region, where they form an important floristic compo- nent, often dominant in the first years after fire (Taylor, 1978). In the more arid Namaqualand, several annual species are found. In tropical Africa, the genus contributes substantially to the Afroalpine grassland (Hedberg, 1964; Lind & Morrison, 1974), and in the subalpine and montane zone from the Drakensberg (Mucina et al., 2006) to Mt. Cameroon, where P. pictigluma (Steud.) Galley & H. P. Linder dominates the grassland on th tai it (Maitland, 1932). Discussion. This large clade of 83 species is very distinctive by its 2-flowered spikelets, the lemma setae inserted in the sinus between the lobes and awn, and the paleae with short, weakly developed, parallel keels. Nonetheless, as is evident from the description, ere is extensive variation within the genus. This includes single-flowered spikelets (but no cases of species with more than two florets per spikelet); complex multicellular glands (Linder et al l inder, 2007); an immense variation in growth form, including geophytes, stoloniferous spe- cies, and suffrutescent species (Linder & Ellis, 1990b); annual, biennial, and perennial species; hairy ovary apices (characteristic of section Pentameris); sclero- phyllous or mesophyllous leaves (Ellis & Linder, 1992; Galley & Linder, 2007); and cytological variation, including the unusual base number of x — 7 The genus has been studied from various aspects recently, including the morphology of the glands (Linder I995 aka pca L; exit Fas. (M , et (Galley & Linder, 2007), and the variation in the leaf anatomy (Ellis & Linder, 1992). In addition, the taxonomy all three previous genera (Davidse, 1988; Linder & Ellis, 1990a; Barker, 1993) has recently been revised. One of the more remarkable reclassifications made here is the placement of Pseudopentameris obtusifolia into Pentameris. This species has the large glumes of Pseudopentameris (albeit somewhat smaller than typical of the genus), but it also has the villous ovary characteristic of Pentameris s. str. M4 we E E EUM hi I hapa ars CS Qu DE QA mO SAPA E ufus ias: Volume 97, Number 3 2010 Linder et al. 329 Classification of Danthonioideae IVa. Pentameris P. Beauv. sect. Pentameris. This section is readily distinguished from the other two sections by fruit with a brittle pericarp crowned with a tuft of white hairs. Included species. The 10 species included have historically been placed in this genus. 1. Pentameris oT (Lehm.) Nees, Lin- 14. 183. naea 7: 314. 2. Pentameris glacialis N. P. Barker, Bothalia 23: 44. 1993. 3. Pentameris hirtiglumis N. P. Barker, Bothalia 23: 39. 1993. 4. Pentam longiglumis (Nees) E No- mencl. d Y E ed. 2, 2: 299. 1 4a. Pentameris longiglumis (Nees) Steud. subsp. longiglumis. 4b. Pentameris longiglumis (Nees) Steud. subsp. gymnocolea N. P. Barker, Bothalia 23: 39. 1993. 5. Pentameris macrocalycina (Steud.) - Repert. Spec. Nov. Regni Veg. 43: 91. 1 6. Pentameris obtusifolia (Hochst.) diva Repert. Spec. Nov. Regni Veg. 43: 1938. 7. Pentameris oreophila N. P. Barker, Bothalia 23: 41. 1993. 8. Pentameris swartbergensis N. P. Barker, Botha- lia 23: 43. 1993. 9. Pentameris thuarii P. Beauv, Ess. Agrostogr. 92, t. 18, fig. 8. 1812. 10. Pentameris uniflora N. P. Barker, Bothalia 23: 35. 1993. IVb. Pentame H. P. Linder & Galley, sect. nov. TYPE: Pentameris tysonii (Stapf) Galley & H. P. Linder (= Pentaschistis tysonii Stapf). Haec sectio a Pentameride P. Beauv. sect. Pentameride caryopsidibus glabratis differt. ameris P. Beauv. sect. Dracomontanum Included species. Only two species are included i . These were previously included in Pentaschistis (Gibbs Russell et al., 1990; Linder & Ellis, 1990a). 1. Pentameris praecox (H. P. Linder) Galley & H. P. Linder, comb. nov. Basionym: Pen- taschistis praecox H. P. Linder, Contr. Bolus Herb. 12: 95. 1990. TYPE: South Africa. Natal, Natl. Park area, Inner Tower Ravine, 17 July 1963, E. E. Esterhuysen 30242 (holotype, BOL. 2. Pentameris tysonii (Stapf) Galley & H. P. Linder, comb. nov. Basionym: pero tysonii ’ Stapf, FL bs. wegen A 493. wenn South Africa. Natal, Mt. Currie, L de 883, W. Tyson 1312 (holotype, K!; isotypes, NOL SAM)). IVe. Pentameris P. Beauv. sect. Pentaschistis (Nees) H. P. Linder & Galley, comb. nov. Basionym: Danthonia sect. Pentaschistis Nees, Fl. Afr. Austr. Ill. 280. 1841. The typification and rank of this section are discussed above under the generic synonymy. In section Pentaschistis, the fruit is a glabrous caryopsis and the plants often have multicellular glands Included species. This section includes 72 species, previously included in the genera Pentaschistis (Linder & Ellis, 1990a) and Prionanthium (Davidse, 1988). The wey follows Linder and Ellis (1990a) and Davidse (1988), where the synonyms and their typification are also i a All new synonyms are listed here. l. Pentameris acinosa d Galley & H. P. Linder, comb. nov. Basionym: Pentaschistis acinosa Stapf, Fl. Cap. (Harvey) T: 495. 1899. TYPE: South Africa. Cape Province: Appelskraal (am Ufer des Rivierzondereinde), s.d., K. L. P. Zeyher 4539 (lectotype, designated by Linder & Ellis [1990a: 99], K!; isotypes, B!, H!, P!, S!, SAM!). — (Nees) — 5 D (Harvey) 7: 496. TYPE: South Af 4, E Drëge ee 4 ostotypa, nd e BI; isotypes, K!, P!). B specimen was annotated by Nees and is The therefore selected as lectotype. 2. Pentameris airoides Nees, Sem. Hort. Bot. Vratisl. 1834. 2a. Pentameris airoides Nees subsp. airoides. 2b. Pentameris airoides Nees subsp. jugorum (Stapf) Galley & H. P. Linder, comb. nov. Basionym: Pentaschistis jugorum Stapf, Fl. Cap. (Harvey) 7: 504. 1899. Pentaschistis airoides (Nees) Stapf subsp. jugorum (Stapf) H. P. Linder, Contr. Bolus Herb. 12: 48. 1990. TYPE: South Annals of the Missouri Botanical Garden Africa. Cape Province: Witteberge near Aliwal North, s.d., J. F. Drège s.n. (holotype, K!). 3. Pentameris alticola (H. P. Linder) Galley & H. P. Linder, comb. nov. Basionym: Pentaschistis alticola H. P. Linder, Contr. Bolus Herb. 12: 79. 1990. TYPE: South Africa. Cape Province: Ceres, Milner Vlakte in Hex River Mtns., 20 Nov. 1987, H. P. Linder 4486 (holotype, BOL!; isotype, S!). 4. Pentameris ampla (Nees) Galley & H. P. Linder, comb. nov. Basionym: Eriachne ampla Nees, Fl. Afr. Austral. Ill. 277. 1841. Achneria ampla ampla (Nees) McClean, S. African J. Sci. 23: 282. 1926. Afrachneria ampla (Nees) Adamson, J. S. African Bot. 5: 53. 1939. TYPE: South Africa. Cape Province: betw. Paarlberg & Du Toits Kloof, s.d., J. F. Drége 1674 (lectotype, designated by Linder & Ellis [1990a: 59], B!). Eriachne pallida Nees, Fl. Afr. Austral. Ill. 275. 1841. Achneria pallida (Nees) T. Durand & Schinz, Consp. Fl. Afr. (T. A. Durand & H. Schinz) 5: 836. 1894. TYPE: South Africa. Cape Province: Zwartkopsriver, s.d., C. F. Ecklon s.n. D. otype, Eriachne aurea (Steud.) Nees var. virens Nees Afr. Austral. Ill. 276. 1841. Achneria aurea Dat E and & Schinz var. virens (Nees) Stapf, Fl. Cap. pet di T 1899. TYPE: South Africa. Cape Du Toits Kloof, s.d., J. F. Drège s.n. MN. B!; isotype, K!). 5. Pentameris andringitrensis (A. Camus) Galley & H. P. Linder, comb. nov. Basionym: Pen- taschistis andringitrensis A. Camus, Bull. Soc. Bot. France 74: 689. 1927. TYPE: Madagascar. Massif d'Andringitra, s.d., J. M. H. A. Perrier de la Bathie 10832 (lectotype, designated by Linder & Ellis [1990a: 104], P!). 6. Pentameris argentea (Stapf) Galley & H. P. Linder, comb. nov. Basionym: Pentaschistis argentea. Stapf, Fl. Cap. (Harvey) 7: 487. 1899. TYPE: South Africa. Cape Province: Cape Peninsula, Orange Kloof, s.d., A Wolley-Dod 3342 (lectotype, desicion b; Linder & Ellis [1990a: 68], K!; isotype, K fragm. at PRE!). 7. Pentameris aristidoides (Thunb.) Galley & H. P. Linder, comb. nov. Basionym: Avena aristidoides Thunb. Prodr. Pl. Cap. 22. 1794. Danthonia trichotoma Nees, Fl. Afr. Austral. Ill. 318. 1841, nom. superfl. P. histis aristidoides (Thunb.) Stapf, Fl. Cap. (Harvey) 7: 485. 1899. TYPE: South Africa. Cape Province: s.d., . Thun- berg s.n. (lectotype, designated here, UPS 25771). There are two collections in the Thunberg Herbar- ium in UPS (UPS 2577 and UPS 2578). It is not clear m . (isotypes). UPS 2577 is the more complete specimen, and so is selected as lectotype. 8. Pentameris aristifolia (Schweick.) Galley & H. P. Linder, comb. nov. Basionym: Pentaschistis aristifolia Schweick., ren Spec. Nov. Regni 1 E: South Africa. Cape — Veg. 43: 89. 1938. TYP Provin 40 mi. SE of Williston, s.d., Tahsan 981 (holotype, K 9. Pentameris aspera (Thunb.) Galley & H. P. Linder, comb. nov. Basionym: Holcus asper Thunb., Prodr. Pl. Cap. 20. 1794. Sorghum asperum (Thunb.) Roem. & Schult., Syst. Veg. ed. 15 (bis) (Roemer & Schultes) 2: 839. 1817. Pentaschistis aspera (Thunb.) Stapf, Fl. Cap. (Harvey) 7: 500. 1899. TYPE: [South Africa. Cape Province:] “crescit in summis ee montium urbis,” | Thunb. 23841 «oe: UPS! i: PAN BOL!)). 10. Pentameris aurea (Steud.) Galley & H. P. Linder, comb. nov. Basionym: Aira aurea Steud., ora 12: 470. 1829. Airopsis aurea (Steud.) ees, Linnaea 7: 317. 1832. Eriachne aurea (Steud.) Nees, Fl. Afr. Austral. Ill. 276. 1841. Achneria aurea (Steud.) T. Durand & Schinz, Consp. Fl. Afr. (T. A. Durand & H. Schinz) 5: 94. Afrachneria aurea (Steud.) Adamson, J. S. African Bot. 5: 53. 1939. Pentaschistis aurea (Steud.) McClean, S. African J. Sci. 23: 282. 1926. TYPE: South Africa. Cape Province: Table Mtn., s.d., C. F. Ecklon 915 (holotype, P not seen; isotypes, BM!, K!). 10a. Pentameris aurea (Steud.) Galley & H. P. Linder subsp. aurea. 10b. Pentameris aurea (Steud.) Galley & H. P. Linder subsp. pilosoghuma (McClean) Galley & H. P. Linder, comb. nov. Basionym: Pentaschistis puilosogluma McClean, S. African J. Sci. 23: 282. 1926. Pentaschistis aurea (Steud.) McClean subsp. pilosogluma veg Clean) H. P. Linder, Contr. Bolus Herb. 12: 76. 1990, replacement snm hirsuta Nees, Fl. Afr. din "n. 282. 1841. Achneria hirsuta (Nees) ie Fl. Cap. (Harvey) 7: 462. 1899. TYPE: HEC Ed Tila a iia TA To e CR DRA eros A Lo Veo Ede REEL CIE P Ra phim ote TG a Na teh nti E Se eae Re le Regn SRE RE ane AC Ur pM id d e equ re re mtr a os eae Volume 97, Number 3 2010 Linder et al. 331 Classification of Danthonioideae South Africa. Cape Province: Witteberge, s.d., J. F. Drége 8116 (holotype, B!; isotype, K!). 11. Pentameris bachmannii (McClean) Galley & H. P. Linder, comb. nov. Basionym: Pentaschistis bachmannii McClean, S. African J. Sci. 23: 282. 1926, replacement name, pro Agrostis curvifolia H rb. ee 3: 384. 1895. ia (Hack) Stapf, Fl. Cap. (Harvey) 7: 458. "qoo. TYPE: South Africa. Cape Province: near Hopefield, s.d., F. E. Bachmann 1017 (holotype, B!; isotype, K!). Eriachne ecklonii Nees, Fl. Afr. Austral. Ill., 273. 1841. 836. 1894. Achneria FEE (Steud.) T dns m Fl. Afr. Durand & & H. Schinz) 5: 836. 1894, nom. illeg. a ecklonii (Nees) Adamson, J. S. African Bot. 5: 53. 1939. Pentaschistis — (Nees) McClean, S. African J. Sci. 23: 282. . TYPE: South beia Cape Province: Klein kia at the Bergri s.d., J. F. Drège 1660 a designated by i. & Ellis [1990a: 52], sotypes, BM!, E!, K!). TI il E. MAE. z the result of the lectotypification of E. ecklonii by Linder and Ellis (1990a); otherwise, this would be the oldest name available for this species. 12. Pentameris barbata (Nees) Steud., Nomencl. Bot. (Steudel), ed. 2, 2: 298. 1841. 12a. Pentameris barbata (Nees) Steud. subsp. barbata. 12b. Pentameris barbata orientalis (H. P. Linder) Galley & H. (Nees) Steud. subsp. P. Linder, Linder, Contr. Bolus Herb. 12: 31. 1990. TYPE: South a. Cape Province: Goukamma Nature Reserve, 2 Jan. 1970, P. van der Merwe 1765 (holotype, STE!). 13. Pentameris basutorum (Stapf) Galley & H. P. Linder, comb. nov. Basionym: Pentaschistis basu- torum Stapf, Bull. Misc. Inform. Kew 1914: 20. 1914. TYPE: Lesotho. Leribe, s.d., A. Dieterlen 222 (holotype, K!; isotypes, BM!, P!, ur STE). 14. Pentameris borussica (K. Schum .) Galley & H. P Li i ym: borussica K. Schum., Pflanzenw. Ost-Afrikas C: 109. 1895. Pentaschistis borussica (K. Schum.) Pilg., Notizbl. Bot. Gart. Berlin-Dahlem 9: 517. 1926. TYPE: Tanzania. Mt. Kilimanjaro, 11 Jan. 1893, G. Volkens 1368 (holotype, B!; isotypes, BM!, E!, HBG!, K!). P. ES s : a E x p Star ie ) Pilo Pilg., Notzibl. Bot. Gart. Berdin Deblent > 516. 19 1926. entaschistis expansa (Pilg.) C. E. Hubb., Fl. Trop. Afr. 10: 130. 1937. TYPE: Kenya. Mt. Kenya, 1921, T. C. x Fries & R. E. Fries 1200b (holotype, B not seen; K!). Ponsho Pans Peter, Repert. Spec. Nov. Regni Veg. ~~ Anhang): 97 t. 56/1. 1930. t. Kilimanjaro, A. Peter 46685 (holotype, B not cs Pentaschistis so M. E Hubb., a Bull. 1936: 501. 1936. TYPE: a. Arusha Distr., Mt. Meru, s.d., B. D. Burtt 2062 2 (oloiype, K. Pentaschistis ruwenzoriensis C. E. Hubb., Kew Bull. 1936: 500. 1936. TYPE: det Toro Distr., Mt. Ruwenzori, s.d., G. Taylor 2903 (holotype, K!; isotype, BM!). 15. Pentameris calcicola (H. P. Linder) Galley & H. P. Linder, comb. nov. Basionym: Pentaschistis calcicola H. P. Linder, Contr. Bolus Herb. 12: 81. 1990. TYPE: South Africa. Cape Province: Bredasdorp, farm Wydgelee, 20 Oct. 1987, H. P. Linder 4365 (holotype, BOL!; isotypes, K!, PRE!) 15a. Pentameris calcicola (H. P. Linder) Galley & H. P. Linder var. ealeicola. 15b. Pentameris calcicola (H. P. Linder) Galley & H. P. Linder var. hirsuta (H. P. Linder) Galley & H. P. Linder, comb. nov. Basionym: Pentaschistis calcicola H. P. Linder var. hirsuta H. P. Linder, Contr. Bolus Herb. 12: 83. 1990. TYPE: South Africa. Cape Province: Bredasdorp, farm Wyd- gelee, 20 Oct. 1987, H. P. Linder 4366 (holotype, BOLI; isotype, K!). 16. Pentameris capensis (Nees) Galley & H. P. radicans Steud., Syn. Pl. Glumac. 1: 243. 1854, nom. superfl. Pentaschistis capensis (Nees) Stapf, Fl. Cap. (Harvey) 7: 494. 1899. TYPE: h Africa. Cape Province: Du Toits Kloof, s.d., J. F. Drége s.n. (holotype, B!; isotypes, BM!, H!, K!, Pt, S!, SAMI). 17. Pentameris capillaris (Thunb.) Galley & H. P. Achneria capillaris (Thunb.) Stapf, Hooker’s Icon. 27, t. 2604. 1899, non Achneria capillaris (R. Br.) P. Beauv., Ess. Agrostogr. 73. 1812. Pen- taschistis capillaris (Thunb.) McClean, S. African Annals of the Missouri Botanical Garden J. Sci. 23: 281. 1926. TYPE: [South Africa.] s. loc., s.d., C. P. Thunberg (holotype, UPS 23845!). 18. Pentameris caulescens (H. P. Linder) Galley & H. P. Linder, comb. nov. Basionym: Pen- tis caulescens H. P. Linder, Contr. Bolus Herb. 12: 99. 1990. TYPE: South Africa. Cape Province: Ceres, Buffelshoek Peak in the Hex- river Mtns., 8 Oct. 1956, E. E. Esterhuysen 26349 (holotype, BOL!). 19. Pentameris chi (H. hippindalliae Galley & H. P. Linder, comb. nov. Basi Pentaschistis chippindalliae H. P. Linder, Contr. Bolus Herb. 12: 92. 1990. TYPE: South Africa. Transvaal, Dullstroom, 10 Feb. 1988, H. P. Linder 4711 (holotype, BOL!; isotypes, K!, M!, MO!, NBG!, PRE!, S!). P. Linder) asionym: 20. Pentameris chrysurus (K. Schum.) Galley & H. P. Linder, comb. nov. Basionym: Danthonia chrysurus K. Schum., Pflanzenw. Ost-Afrikas C: 110. 1895. Pestaschisti chrysurus (K. Schum.) am Repert. jaro, 14 Feb. 1894, G. Volkens 1826a holis. B!). 21. Pentameris cirrhulosa (Nees) T No- mencl. Bot. (Steudel), ed. 2, 2: 298. 1 22. Pentameris clavata (Galley) Galley € H. P. Linder, comb. nov. asionym: Pentaschistis clavata Galley, Bothalia 36: 159. 2006. TYPE: South Africa. Western Cape Province: Koue Bokkeveld S of Hex Berg, 7 Nov. 2004, C. A. Galley 567 (holotype, Z!; isotypes, BOL!, E!, G!, K!, MO!, NBG!, NSW!, NY!, PRE!, S!, UPS!, W?) 23. Pentameris colorata (Steud.) Galley & H. P. Linder, comb. nov. Basi lonym: Avena colorata Steud., Flora 12: 481. 1829. Pentaschistis color- 24. Pentameris curvifolia (Schrad.) Nees, Linnaea 7: 313. 1832. 25. Pentameris densifolia oe m ; Nomencl. Bot. (Steudel), ed. 2, 2: 298. | 26. Pentameris dentata (L. £) Galley & H. P. Linder, comb. nov. Bas asionym: Phalaris dentata dentata A f) Trin, Sp Gram. (Trinius) 168. 1824. Prionanthium rigidum Desv., Opusc. Sci. Phys. Nat. 65. 1831. Lasio- chloa pectinata Trin. ex Pritz, Sp. Gram. E corrigenda et emendanda, 1(7), tab. Henrard, Blumea 4 . TYPE: [South Africa.] Cape, Bockland; 1723, C. P. Thunberg s.n. (holotype, UPS 1773". i 27. Pentameris dolichochaeta (S. M. Phillips) | Bull. 50: 615. 1995. TYPE: Ethiopia. Showa, cobere m, sd. G. Selassie 887 (uabaype, ETH!, ETH photo at K!). 28. Pentameris ecklonii (Nees) Galley & H. P. Linder, comb. nov. Basionym: Prionachne ecklo- nii Nees, Nat. Syst. Bot. 448. 1836. Chondro- laena phalaroides Nees, Fl. Afr. Austral. Ill. 134. 1841, nom. illeg. Prionanthium ni dne Stapf, Fl. Cap. (Harvey) 7: 456. 1899. TYPE South Africa. *ad Olifantsrivier faa alt. L Clanwilliam,” s.d., C. F. Ecklon s.n. (lectotype, ` designated by Davidse [1988: 151|, MO not seen; 1 isotypes, BM, BM fragm. at PRE!, US not seen, | Z!). ; 29. Pentameris elegans (Nees) B" Nomencl . Bot. (Steudel), ed. 2, 2: 298. 1 30. Pentameris ellisii H. P. Linder, Bothalia 40: 191. 2010. 31. Pentameris eriostoma (Nees) Steud., No- mencl. Bot. (Steudel), ed. 2, 2: 298. 1841. 32. Pentameris exserta (H. P. Linder) Galley & - H. P. Linder, comb. nov. taschistis exserta H. P. ym: Pen- (holotype, BOL)). 33. Pentameris galpinii (Stapf) Galley & H. P. Linder, comb. nov. Pentaschistis galpinii (Stapf) McClean, S. African J. Sci. 23: 282. 1926. TYPE: South Africa. Cape Province: Barkly East, Ben Macdhui, 11 Mar. 1904, E. E. Galpin 6915 (holotype, K!; isotypes, B!, BOL!, GRA!, SAM)). Basionym: Achneria galpinii 4 x Stapf, Bull. Misc. Inform. Kew 1910: 59. 1910. — E A EM. Lr EB A E a a E A A E A e O, fee I Volume 97, Number 3 2010 Linder et al. 333 Classification of Danthonioideae 34. Pentameris glandulosa (Schrad.) Steud., No- mencl. Bot. (Steudel), ed. 2, 2: 298. 1841 35. Pentameris heptameris (Nees) HN No- mencl. Bot. gj Hane ed. 2, 2: 298. 1 36. Pentameris holciformis (Nees) Galley & H. P. is Contr. Bolus Herb. 12: 91. 1990. TYPE: South Africa. Cape Province: Palmietriver at Grietjies- gat, s.d., C. F. Ecklon s.n. (lectotype, designated here, B!; isotype, S!). The B specimen was annotated by Nees and is selected here as lectotype. M. Pentameris horrida (Galley) Galley & H. P. . Basionym: Pentaschistis y, Bothalia 36: 160. 2006. TYPE: South hea Western Cape: Ceres, Baviaans- ma 26 Oct. 1997, H. P. Linder 6799 (holotype, Z!; isotypes, BOL!, E!, G!, K!, MO!, NBG!, NSW!, PRE! j) 38. Pentameris humbertii (A. Camus) Galley & H. 90. 1928. TYPE: Madagascar. Pic d'lvohibe (Bara), 5 Nov. 1924, J.-H. mbert 3310 (holotype, P!; isotypes, B!, K!). 39. Pentameris insularis (Hemsl.) Galley & H. P. Linder, comb. nov. Basionym: Trisetum insulare Hemsl., Rep. Voy. Challenger, Bot. 1(2): 267, t. 52. 1884. Pentaschistis insularis (Hemsl.) H. P. Linder, Contr. Bolus Herb. 12: 103. 1990. TYPE: Territory of the French Southern and Antarctic Lands. St. Paul Island, Indian Ocean, s.d., J. MacGillivray & W. G. Milne (lectotype, desig- nated by Linder € Ellis [1990a: 104], K'), Figure 6. 40. Pentameris juncifolia (Stapf) Galley € H. P. Linder, comb. nov. Basionym: Pentaschistis juncifolia Stapf, Fl. Cap. (Harvey) 7: 490. 1 TYPE: South Africa. Riversdale dn. hills near Zoetemelksrivier, s.d., W. J. Burchell 6750 (lectotype, designated id Linder & Ellis [1990a: 107], K!). 41. Pentameris lima (Nees) Steud., Nomencl. Bot. (Steudel), ed. 2, 2: 299. 1841 42. Pentameris longipes (Stapf) Galley & H. P. Linder, comb. nov. — Pentaschistis < NY SN Ww j EN MUN 74 EN RN NN VW AN iy A SSS WP Ñ ° S ER < Ni NY V) ; “wv. = Z 3 ^w >> Figure 6. Pentameris insularis. Drawn by Jasmin Bau- ann. 43. P longipes Stapf, Fl. Cap. (Harvey) 7: 509. 1899. TYPE: South Africa. Cape Province: Albany, s.d., J. Bowie s.n. (holotype, K!). entameris malouinensis (Steud.) Galley € H. P. Linder, comb. nov. Basionym: Eriac malouinensis Steud., Syn. Pl. Glumac. 1: 2 1854. Pentaschistis malouinensis (Steud.) Clay- ton, Kew Bull. 23: 294. 1969. TYPE: Falkland Islands, s.d., D. d'Urville s.n. 1 CN not seen; isotype, CN photo at Annals of the Missouri Botanical Garden The Falkland Islands as type locality is almost certainly an error: the species is endemic to southern ica. 44. D rR - . ph yll (N Linder, comb. nov. Basionym: Eriaci phylla Nees, Fl. Afr. Austral. Ill. 277. 1841. Achneria microphylla (Nees) T. Durand & Schinz, Consp. Fl. Afr. (T. A. Durand & H. Schinz) 5: 836. 1894. Pentaschistis microphylla (Nees) McClean, S. African 1. 23: 1926. bri in anthesi,” s.d., J. F. Drége 3891 (holotype, BI; isotypes, BM!, K!, SAM)). 45. Pentameris minor (Ballard & C. E. Hubb.) Galley & H. P. Linder, comb. nov. Basionym: Pentaschistis borussica (K. Schum.) Pilg. var. minor Ballard & C. E. Hubb., Bull. Misc. Inform. Kew 1930: 121. 1930. Pentaschistis minor (Ballard & C. E. Hubb.) Ballard & C. E. Hubb., Fl. Trop. Afr. (Oliver et al) 10: 132. 1937. tu Taxonomique de la Flore d'Afrique Tropical] Zomba Malawi 371. 1994. TYPE: Tanzania. Mt. Kilimanjaro, near Peters Hut, s.d., A. D. Cotton & A. S. Hitchcock 64 (holotype, K!). 46. Pentameris montana (H. P. Linder) Galley & . P. Linder, comb. nov. Basionym: Pentaschistis berg, 7 Nov. 1987, H. P. Linder 4413 (holotype, BOL!). 47. Pentameris natalensis (Stapf) Galley & H. P. Linder, comb. nov. Basionym: Pentaschistis nata- lensis Stapf, FL. Cap. (Harvey) 7: 493. 1899. TYPE: South Africa. Natal, Riet Vlei, s.d., J. Buchanan 283 (holotype, K!; isotypes, B!, BOL)). 48. Pentameris oreodoxa (Schweick.) Galley & H. P. Linder, comb. nov. Basionym: Pentaschistis oreodoxa Schweick., Repert. Spec. Nov. Regni Veg. 43: 90. 1938. TYPE: South Africa. Natal, Bergville, Mont aux Sources, near summit of min., s.d., A. J. W. Bayer & A. P. D. McClean 273 (holotype, K!). 49. Pentameris pallescens (Schrad.) Nees, Lin- naea 7: 312. 1832. 50. Pentameris pallida (Thunb.) Galley & H. P. Linder, comb. now. Basionym: Avena pallida Thunb., Prod. Pl. Cap. 22. 1794. Danthonia pallida (Thunb.) Roem. & Schult., Syst. Veg. 2: - 657. 1817, nom. illeg., non Danthonia pallida R. Br., Prodr. Fl. Nov. Hollan 177. 1810. Pentaschistis pallida (Thunb.) P. Linder, Contr. Bolus Herb. 12: 36. 1990. TYPE: So Africa. Cape Province: Verkeerde Vlei, s.d., C. x P. Thunberg (lectotype, designated by Linder & Ellis [1990a: 36], UPS 2610!). Danthonia angustifolia Nees, Fl. Afr. Austral. Ill. 302. 1841. gustifolia (Nees) Stapf, Fl. Cap. (Harvey) 7: 502. 1899. ica. Cape Province: on fields at Zwartkopsvlei and at Adow, s.d., C. F. Ecklon 839 ` (lectotype, designated by Linder & Ellis [1990a: 37], B)). Pentaschistis thunbergii Stapf, Fl. Cap. (Harvey) 7: 507. 1899, non Pentaschistis thunbergii Kunth. Stapf (1899) misapplied Pentaschistis thunbergii, and its incorrect use was widespread in the literature until corrected by Linder and Ellis (1990a). 51 a (Nees) Steud., Nomencl. a 1841 a . Pentameris patul Bot. (Steudel), ed. 2, 2: 299. ; à 52. Pentameris pholiuroides (Stapf) Galley & H. P. Linder, comb. nov. Basionym: Prionanthium pholiuroides Stapf, Fl. Cap. (Harvey) 7: 456. 1899. Prionachne pholiuroides (Stapf) E. Phil- lips, Intr. S. African Grass. 6, t. 63. 1931. TYPE: A South Africa. Fish Hoek valley, damp hollow, Nov. 1897, A. H. Wolley-Dod 3394 (holotype, K not seen; isotypes, BM not seen, BOL', MO not. — seen, PRE!). 53. Pentameris pictigluma (Steud.) Galley & H. P. Linder, comb. nov. Basionym: Aira pictigluma Steud., Syn. PI. Glumac. 1: 221. 1854. Dantho- nia anthoxanthiformis Hochst., Flora 38: 276. 1855, nom. illeg. superfl. Pentaschistis gluma (Steud.) Pilg., Notizbl. Bot. Gart. Dahlem 9: 517. 1926. TYPE: Ethiopia. s.d., W. G. Schimper (holotype, P not seen). U The species delimitation in Pentameris pictigluma Is still most unsatisfactory, and a critical evaluation of the populations on the different mountains, and in | different altitude zones, is needed. Until such time, 1 the potential taxa are here recognized as varieties (thus following the treatment of Phillips [1995], except that P. minor is maintained at species level). 53a. Pentameris pictigluma (Steud.) Galley & H. i P. Linder var. pietigluma. Volume 97, Number 3 2010 Linder et al. Classification of Danthonioideae 53b. Pentameris pictigluma (Steud.) Galley & H. P. Linder var. gracilis (S. M. Phillips) Galley & H. P. Linder, comb. nov. Basionym: Pentaschistis gracilis S. M. Phillips, Kew Bull. 41: 1028. 1986. ie prs ay pictigluma (Steud.) Pilg. var. grac- is (S. M. Philli a S. M. Phillips, Proc. XIII "d Vu AETF Taxonomique de Flore d'Afrique Tropical] Zomba Malawi 372. 1994. TYPE: Ethiopia. Shoa Province, Entoto Hill, along a small stream, s.d., I. Friis, M. Gilbert, F. Rasmussen & K. Vollesen 1303 (holotype, K!). T [Association pour l'Étude 53c. Pentameris picti a (Steud.) Galley & H. . Linder var. mannii (Stapf ex C. E. Hubb.) Galley & H. P. Linder, comb. nov. Basionym: Pentaschistis mannii Stapf ex C. E. Hubb., Bull. Misc. Inform. Kew 1936: 501. 1936. TYPE: Cameroun. Mt. Cameroun, s.d., G. Mann 1351 olotype, K!). 54. Pentameris pseudopallescens (H. P. Linder) Province: Ceres, Milner Vlakte, Hex Giver Mtns., 20 Nov. 1987, H. P. r 4483 (holotype, BOL!). 55. Pentameris pungens (H. P. Linder) Galley & H. P. Linder, comb. nov. Basionym: Pentaschistis pungens H. P. Linder, Contr. Bolus Herb. 12: 97. 1990. TYPE: South Oct. 1975, E. E. Esterhuysen 34010 (holotype, BOLI; isotypes, K!, P 56. Pentameris pusilla (Nees) Galley & H. P. Linder, comb. nov. Basionym: Colpodium pusil- lum Nees, Fl. Afr. Austral. Ill. 149. 1841. Poagrostis pusilla (Nees) Stapf, Fl. Cap. (Harvey) 7: 760. 1900. Agrostis umbellata Trin., Graminea Agrostidea. II. Callus rotundus (Agrostea), 370. 1841, nom. illeg., non Agrostis umbellata Colla, Herb. Pedem. 6: 18. 1836. Pentaschistis o (Nees) H. P. me Contr. Bolus Herb. 12: 1990. TYPE: South Africa. Cape Province: i Mtin., s.d., J. F. Drège s.n. (holotype, B not seen; isotype, K!). 57. Pentameris pyrophila (H. P. Linder) Galley & H. P. Linder, comb. nov. Basionym: Pentaschistis pyrophila H. P. Linder, Contr. Bolus Herb. 12: 81. 1990. TYPE: South Africa. Cape Province: Ceres, Milner Peak, Hex River Mtns., 20 Nov. 1987, H. P. Linder 4477 (holotype, BOL!). 58. Pentameris reflexa (H. P. Linder) Galley & H. P. Linder, comb. nov. Basionym: Pentaschistis reflexa H. P. Linder, Contr. Bolus Herb. 12: 53. 1990. TYPE: South Africa. Cape Province: Cedarberg, slopes below Middelberg at Algeria, 6 Dec. 1987, H. P. Linder 4531 (holotype, BOL!; isotypes, K!, MO!, PRE!, STE!). 59. Pentameris a (Pilg. ex H. P. Linder) Galley & H. P. Linder, comb. nov. Basionym: Pentaschistis rigidissima Pilg. ex H. P. Linder, Contr. Bolus Herb. 12: 85. 1990. TYPE: South a. Cape Province: Worcester, Milner Peak, Hex Be Mtns., 18 Dec. 1948, E. E. Esterhuy- sen 14903 (holotype, BOL!; isotypes, NBG!, PRE!, SAM!). 60. Pentameris rosea (H. P. Linder) Galley & H. P. Linder, comb. nov. Basionym: Pentaschistis rosea H. P. Linder, Contr. Bolus Herb. 12: 70. 1990. TYPE: South Africa. Cape Province: ee Mtns., Groot Winterhoek Forest Reserve, Suu lekte. 14 Oct. 1988, H. P. Linder 4777 tore BOL. 60a. Pentameris rosea (H. P. Linder) Galley & H. P. Linder subsp. rosea. 60b. Pentameris rosea (H. P. Linder) Galley & H. P. Linder subsp. purpuraseens (H. P. Linder) Galley & H. P. Linder, comb. nov. Pentaschistis rosea H. P. Linder subsp. purpur- ascens H. P. Linder, Contr. Bolus Herb. 12: 72. TYPE: South Africa. Cape Province: Ceres Distr., Milner Vlakte, Hexriver Mtns., 24 Oct. 1987, P. Linder 4403 (holotype, BOL!) Basionym: 61. Pentameris rupestris (Nees) Steud., Nomencl. Bot. (Steudel), ed. 2, 2: 299. 1841. 62. P. seabra (Nees) = Nomencl. E. T An ed. 2, 2: 299. 184 Avena papillosa Steud., Flora 12: 484. 1829, non Schrad., Cape Province: Cape Town, mmitate montis tabularis, Fl. Novbr. ie t F. 936 (types, E!, K!). oy subulifolia Stapf, Fl. Cap. (Harvey) 7: 499. 899. TYPE: South Africa. Cape e Table Mtn., vag tsar 1698 (lectotype, design: by Linder & vide [1990a: 37], K!; isotypes, BM!, S AND Ec iini Annals of the Missouri Botanical Garden 63. Pentameris scandens (H. P. Linder) Galley & H. P. Linder, comb. nov. Basionym: Pentaschistis scandens H. P. Linder, Contr. Bolus Herb. 12: 101. 1990. TYPE: South Africa. Cape Province: Bredasdorp, Bontebok Park, 25 Aug. 1962, J. P. H. Acocks 22619 (holotype, PRE!). 64. Pentameris setifolia (Thunb.) Galley & H. P. Linder, comb. nov. Basionym: Holcus setifolius Thunb., Fl. Cap. (Thunberg, ed. 2), 1: 413. 1813. Achneria setifolia (Thunb. Stapf, FI. Cap. (Harvey) 7: 462. 1899. Pentaschistis Ln (Thunb.) McClean, S$. African J. Sci. 23: 1926. TYPE: [South Africa] s. loc., Wu Thunberg s.n. in herb. C. P. Thunb. 23857 (holotype, UPS!). — mutica Nees, Fl. Afr. Austral. Ill. 281. 1841. is mutica (Nees) Steu Bot. ape Province Windvogelberg & Swartkei River, d FD (lectoype, — by Li & Ellis [1995: 58], B!; isotype ,B fragm. l, K). Cape Drè e 3893 kde. B t seen; pues BM!, K!, OXF!, PRC!, B fragm. at PRE! T rovince: ee s.d., J. F. va Ve UNE Np B!; isotypes, B Kt). at PRE!, 65. Pentameris tomentella (Stapf) Galley & H. P. Linder, comb. nov. Basionym: Pentaschistis tomentella Stapf, Fl. Cap. (Harvey) 7: 502. 1899. TYPE: South Africa. Cape Province: Namaqualand. Modderfonteinsberg, s EU Drége s.n. (holotype, K!; isotype, S!). — d. DM Fl. Cap. (Harvey) 7: 507. E: Sout a. Cape Province e: Namaqua- “ee. betw. Pedros Kloo & Lilyfontein s.d., J. F. Drége 2580 (holotype, K!; isotypes, B!, BM!). or Pentaschistis tomentella, note that the types are to “Pentaschistis papillosa Schrad.” 66. Pentameris tortuosa (Trin.) Nees, Linnaea 7: 310, 311. 1832. 67. Pentameris trifida (Galley) Galley & H. P. Linder, comb. nov. Basion onym: Pentaschistis trifida Calley, Bothalia 36: 157. 2006. TYPE: South - isotypes, BOL!, K!, NBGI, PRE)). . Pentameris triseta (Thunb.) Galley € H. P. — Linder, comb. nov. Basionym: Avena triseta Thunb., Prodr. Pl. Cap. 22. 1794. Trisetum ` villosum Pers., Syn. Pl. (Persoon) 1: 97. 1805, nom. superfl. Pentameris villosa (Pers.) Nees, Linnaea 7: 310. 1832, nom. illeg. Danthonia villosa (Pers.) Trin., Mém. Acad. Imp. Sci. St.- Pétersbourg, Sci. Math, Seconde Pt. 33. 1836, nom. illeg. Avena capensis Spreng., Syst. Veg. 1: - 333. 1825, nom. superfl. Danthonia thunbergii Kunth, Révis. Gramin. 1: 107. 1829, nom. illeg. Pentaschistis eti (Kunth) Stapf, Fl. Cap. - (Harvey) 7: , nom. illeg. Danthonia collinita Ka A Afr. Austral. Ill. 315. 1841, x nom. superfl. Pentaschistis triseta (Thunb.) Stapf, H. bus (Harvey) 7: 495. 1899. TYPE: [South ca.] s. loc, sd, Thunberg s.n. (holotype, UPS 2632!). These names all cite Avena triseta, and so include : x its type. Hence they are all homotypic. However, the - situation is quite complex: it seems that initially ` risetum villosum Pers. was misapplied, leading toa series of misunderstandings. 69. Pentameris trisetoides (Hochst. ex Steud.) - Galley & H. P. Linder, comb. nov. Basionym: Danthonia trisetoides Hochst. ex Steud., Syn. PI. Glumac. 1: 244. 1854. Pentaschistis trisetoides (Hochst. ex Steud.) Pilg., Notizbl. Bot. Gart. * Berlin-Dahlem 9: 516. 1926. TYPE: Ethiopia. ` Near Debra Eski, s.d., W. G. Schimper 109 a (holotype, P!; isotype, kK)” i Pentameris velutina (H. P. Linder) Galley & ` H. P. Linder, comb. nov. Basionym: Pentaschistis velutina H. P. Linder, Contr. Bolus Herb. 12: 66. — 990. TYPE: South Africa. Western Cape Prov., 70. . Mtns., on ridge on Berghof farm, 14 _ - 1988, H. Ms. E). P. Linder 4791 (holotype, BOL!; Pentameris veneta (H. P. Linder) Lana i H. P. Linder, comb. nov. Basionym: Pen A veneta H. P. Linder, Contr. Bolus y 12: 29. GN 1990. TYPE: South Africa. C Jape Province: Cedarberg, Blaauwberg, s.d., J. F. Drége 1682b (holotype, K!). 72. tie viseidula (Nees) Steud., Nomencl Bot. (Steudel), ed. 2, 2: 299. 1841. x Volume 97, Number 3 Linder et al. 337 Classification of Danthonioideae Figure 7. rt rigida subsp. rigida. —A. me let. —B. Lemma Palea. Drawn by Jas Hannes fix Qs in CHR 217596. V. Chionochloa Zotov, New Zealand J. Bot. 1: 87. 1963. TYPE: Chionochloa rigida (Raoul) Zotov (5 Danthonia rigida Raoul). Figure 7. Danthonia DC. sect. a Pilg., Willdenowia = 474. 1969. rs Danthonia cunninghamii Hook. f. (= Chionoc conspicua G. Forst.) Zotov subsp. cunninghamii Vei f.) TD eer Plants forming ae perennial tussocks or mats; culms 0.8-3 m tall. Sheaths often fragmenting horizontally; a ciliate; leaf blades sclerophyl- lous, tough, occasionally with a weftlike indumentum on the upper surface directly above the ligule, often disarticulating from the sheaths at the ligules or falling with part of the sheath, but in many cases persistent. Inflorescences + paniculate, open to plumose. Spikelets with more than 2 florets, all similar; glumes shorter to longer than the florets, 4- 16 mm, with 1 to 13 nerves, glabrous or micro- scaberulose, rarely with tufts of long hairs; callus rounded or truncate, villous, ape to longer than the rachilla internode; lemmas with 3 to 9 indistinct the hairs , usually shorter than the lemma body, setae well developed; lemma central awn usually present and exceeding the lemma lobes, sometimes differ- entiated into a flat, corkscrewed base and a straight, hairlike apical part; paleae lorate to linear, with long tufts of hair on the palea-flaps; lodicules rhomboid to rarely cuneate, generally with microhairs and bristles; ovary glabrous. Caryopsis lorate to obovate; embryo and linear hilum about 1/2 of the caryopsis length. Cytology. 2n = 42 (Abele, 1959; Brock & Brown, 1961; Beuzenberg & Hair, 1983; Dawson, 1989; Connor & Lloyd, 2004; Murray et al., 2005). Anatomy. The leaves are sclerophyllous, expand- ed; adaxial ribs variously developed, usually with deep cleftlike furrows with overlapping microhairs at the base, often with dense and large tubercles on the ribs and in the grooves; adaxial sclerenchyma as massive T-shaped or inversely anchor-shaped girders associated with both 1- and 3-order vascular bundles; the abaxial epidermis often with a continuous subepidermal layer; clear cells in the chlorenchyma and bulliform cells absent. Distribution and habitat. Twenty-two of the 24 endemic to the Mt. Kosciuszko area. Several species are found on the various off-shore islands around New Zealand. This genus often dominates the grasslands the mountains of South Island (Wardle, 1991). Several species are cliff specialists, and a few occur on coastal rocks. The ecology of the species has received much attention due to their T to Lt and grazing and their importance und cover, cially in the mountains of E South Island. of New Zealand (Connor, 1967). Discussion. Chionochloa is very distinctive, but it remains difficult to precisely define its attributes, as re are numerous exceptions. The most reliable attribute is the plant habit with tall, tough tussocks by which Chionochloa can be readily distinguished from the other genera of danthonioid grasses in New Zealand and Australia, all of which, with the exception of Austroderia, are fine-leaved and weakly to moderately caespitose, but never massive, grasses. Austroderia, while forming substantial tussocks, has inflorescences that are considerably larger and more 338 Annals of the Missouri Botanical Garden plumose than those in species of Chionochloa. The 8e. Chionochloa crassiuscula (Kirk) Zotov subsp. x lemmas are also distinctive, with the indumentum in inal and midrib-flanking stripes, and the central awn without a clearly developed column. The paleae always have hair-tufts along the margins. While this occurs in many other genera, it is usually uncommon. Most cuti iue. is e leaf ener with the dee at the bu: ques with the pieri estranoes often partially occluded by the dense tubercles. The limits between the species in Chionochloa are very difficult, possibly due to hybridization (Connor, 1991). In the most recent revision, Connor (1991) ized numerous subspecies and varieties; these may include intermediate forms, but many are geographically separated and distinct taxa. Included species. This genus of 25 species was revised taxonomicaly by Connor (1991), whose taxonomy and nomenclature we follow here. l. Chionochloa acicularis Zotov, New Zealand J. Bot. 1: 101. 1963. 2. Chionochloa xem — f.) Zotov, New Zealand J. Bot. 1: 99 3. Chionochloa australis ee Zotov, New Zealand J. Bot. 1: 103. 1 4. Chionochloa beddiei Zotov, New Zealand J. Bot. 1: 90. 1963. 5. Chionochloa bromoides . f.) Zotov, New Zealand J. Bot. 1: 90. 1 6. Chionochloa cheesemanii (Hack. ex Cheese- man) Zotov, New Zealand J. Bot. 1: 95. 1963. 7. Chionochloa eonspieua "s cren Zotov, New Zealand J. Bot. 1: 92. 1 Ta. Chionochloa conspicua (G. Forst) Zotoy subsp. conspicua. Tb. ME conspicua (G. Forst) Zotov subsp. porns f) Zoto Zelma L ku. L 94 ) v, New 8. Chionochloa c crassiuseula "n Jos N Zealand J. Bot. 1: 103. 1963 oe 8a. Chionochloa crassiuscula (Kirk) Zotoy subsp. crassiuseula. 8b. Chionochloa erassiuscula (Kirk) Zotoy subsp. directa Connor, New Bot. 29: 236 1991. Ñ torta Connor, New Zealand J. Bot. 29: 237. 1991 a 9. Chionochloa defracta Connor, New Zealand J. Bot. 25: 164. 1987. 10. Chionochloa flavescens Zotov, New Zealand J. Bot. 1: 97. 1963 10a. Chionochloa flavescens Zotov subsp. flaves- ` cens. 10b. Chionochloa flavescens Zotov subsp. brevis Connor, New Zealand J. Bot. 29: 240. 1991. 10c. Chionochloa flavescens Zotov subsp. hirta Connor, New Zealand J. Bot. 29: 241. 1991. 10d. Chionochloa flavescens Zotov subsp. bu- — peola Connor, New Zealand J. Bot. 29: 242. 1991 11. Chionochloa flavicans Zotov, New Zealand J. Bot. 1: 91. 1963. 12. Chionochloa frigida d Conert, Senck- ` enberg. Biol. 56: 154. 1975. 13. Chionochloa howensis S. W. L. Jacobs, Telopea 3: 281. 1988. 14. Chionochloa juncea Zotov, New Zealand J. Bot. 1: 101. 1963. 15. Chionochloa lanea Connor, New Zealand J. Bot. 25: 165. 1987 16. Chionochloa maera Zotov, New Zealand J. Bot. 8: 91. 1970. 17. Chionochloa nivifera Connor & K. M. Lloyd, | New Zealand J. Bot. 42: 531. 2004 18. Chionochloa rd E Zotov, New Y Zealand J. Bot. 1: 104. 1 19. Chionochloa Ta. (Buchanan) Zotov, New | Zealand J. Bot. 1: 1963. 20. Chionochloa P ac Zotov, New Zealand J. Bot. 1: 99, ] 20a. Chionochloa pallens Zotov subsp. pallens. 20b. Chionochloa pallens Zotov subsp. €a- dens Connor, New Zealand J. Bot. 29: 251. 199], 20e. Chionochloa pallens Zotov subsp. pilosa Connor, New Zealand J. Bot. 29: 252. 1991. Volume 97, Number 3 2010 Linder et al. Classification of Danthonioideae 21. Chionochloa rigida (Raoul) Zotov, New Zea- land J. Bot. 1: 96. 1963. 2 2). øT NT. L 2la. mah: Li 21b. Chionochloa rigida T is subsp. amara Connor, New Zealand J. Bot. 29: 254. 1991. 22. Chionochloa rubra Zotov, New Zealand J. Bot. 1: 96. 1963. 22a. Chionochloa rubra Zotov subsp. rubra. 22a(i). Chionochloa rubra Zotov var. rubra. 22a(ii). Chionochloa rubra Zotov var. iner- mis Connor, New Zealand J. Bot. 29: 255. 1991. 22b. Chionochloa rubra Zotov subsp. cuprea Connor, New Zealand J. Bot. 29: 256. 1991. 22e. Chionochloa rubra Zotov subsp. occulta Connor, New Zealand J. Bot. 29: 257. 1991. 23. Chionochloa spiralis Zotov, New Zealand J. Bot. 1: 100. 1963. . Chionochloa teretifolia (Petrie) Zotov, New Zealand J. Bot. 1: 100. 1963. 295. hloa vireta Connor, New Zealand J. Chionoc Bot. 29: 261. 1991. VI. Pseudopentameris Conert, Mitt. Bot. Staats- samml. München 10: 303. 1971. TYPE: Pseudo- pentameris macrantha (Schrad. ex Schult.) Con- ert (= Danthonia macrantha Schrad. ex Schult.). Figure 8. Plants forming perennial tussocks, suffrutescences, or with single erect shoots from large unde rhizomes, culms to 0.8 m tall. "-— ciliate; leaf blades sclerophyllous, tough, glabrous. Inflorescences + paniculate, open. Spikelets with 2 similar florets; glumes longer than the florets, large, 25-35 mm, with 1 to 5 nerves; callus rounded or truncate, villous, about twice as long as the rachilla internode; lemmas with 9 veins, dorsally pilose; lemma lobes acute, usually shorter than the lemma body, setae variously developed, usually seated on the inner margin of the lemma lobes; lemma central awn usually present and exceeding the lemma lobes, differentiated in a corkscrewed basal column and a straight, hairlike apical part; paleae lorate to linear, glabrous except for the scabrid keel margins; lodicules rhomboid to cuneate, sometimes with bristles; ovary glabrous. Caryopsis reticulately sculptured, embryo 1/5 and Pseudopentameris macrantha. —A. Spikelet. —B. Lemma back. —C. Palea. Drawn by Jasmin Baumann from Ecklon & Zeyher 1825. Figure 8. Cytology. Unknown. Anatomy. The leaves are mostly d expanded; adaxial ribs variously developed; adaxial sleis as caps, massive T-shaped girders or inversely anchor-shaped girders associated with both - and 3-order vascular bundles; bulliform cells present in the adaxial furrows. Distribution and habitat. Pseudopentameris is restricted to the Cape region of southern Africa. All three species grow on sandstone or granite substrates, where they are found in heathy fynbos vegetation, which they can dominate in the first years after fire. Pseudopentameris macrantha can form very large tussocks with aerial rhizomes that grow up with the fynbos after fire (Verboom & Linder, 1998). Discussion. Although this genus groups with romus on molecular evidence, it is morpho- logically very different. Pseudopentameris shares with Pentameris 2-flowered spikelets, but differs by the large spikelets (glumes 25-35 mm long vs. 2-25 mm in Pentameris). Included species. When Conert (1971) segregated this genus from Danthonia, he placed only two species in Annals of the Missouri Botanical Garden Figure 9. Chaetobromus invol —A. Spikel Tenis Rina, 8 from Linder s. ucratus subsp. sericeus. et. —B. Lemma s —C. Palea. Drawn by it. Since then, a third new species has been recognized, and we follow the tax and nomenclature proposed by Barker (1995) in his revision of the genus. 1. Pseudopentameris brachyphylla (Stapf) Con- Staatssamml. ert, Mitt. Bot. München 10: 304. 1971 2. Pse ntameris caespitosa N. P. Barker, Bothalia 25: 147. 1995. 3. Pseudopentameris macrantha (Schrad.) Con- pri Mitt. Bot. Staatssamml. Miinchen 10: 304. Vil. Nees in J. Lindley, Nat. Syst. Bot., ed. 2, 449. 1836. Danthonia DC. sect. Chaeto. . TYPE: Chaetobromus involucratus (Schrad.) Nees (= Avena involucrata Schrad.). Figure 9. Plants forming perennial weich ulms 0.3-0.8 m tall, sometir n rhizomes. Ligule ciliate; leaf blades usually “aba. emmas with 7 to 9 indistinct veins, dorsally pilose; lemma lobes acute, usually shorter than the lemma body, setae variously ` developed from the apex of the lobes; lemma central | awn exceeding the lemma lobes, differentiated intoa flat, corkscrewed base and a straight, hairlike apical | part; paleae lorate to linear, flat; lodicules cuneate, — with bristles but without microhairs; ovary us. Caryopsis lorate; hilum linear. : Cytology. 2n = 12, 18, 36, 48, 52, 72 (Spies et al., 1990; Verboom & Linder, 1998). Anatomy. The leaves are orthophyllous, expand- : ed; adaxial ribs poorly developed; sclerenchyma as | small girders mostly over the l-order adaxial | vascular bundles; phloem with a thickened sheath; | bulliform cells restricted to the grooves flanking the ` midrib. Distribution and habitat. The genus includes a single species on the west coast of southern Africa. This species can be separated into three subspecies that show ploidy differences and occupy somewhat ` different habitats. Chaetobromus involucratus subsp. ` sericeus occurs on Quaternary coastal sands in the arid northwest, subspecies involucratus occurs on similar substrates in the more mesic southwest, and subspe- cies dregeanus occurs on shale- and granite-derived soils in the interior. Discussion. Although molecular data indicate that this genus is sister to Pseudopentameris, it shares only — attributes of the palea and the callus with this | otherwise very different genus. Chaetobromus is A readily diagnosed by the tuft of hair at the base of the spikelets (hence the generic name), at a joint —— where the spikelets disarticulate below the glumes. 4 Furthermore, the basal floret differs from the upper florets by its smaller size, shorter setae and awn, and only seven instead of nine veins. These attributes are both unique within the Danthonioideae. x Included species. Various classifications have recognized between three (Chippendall, 1955) and one (Verboom & Linder, 1998) species in this genus. - We follow the latter approach, of one species, but with a three subspecies. The nomenclature follows Verboom — - and Linder (1998) 1. Chaetobromus involucratus (Schrad.) Nees, Fl | Afr. Austral. Ill. 344. 1841. la. Chaetobromus imvolueratus (Schrad. Nees | subsp. involucratus lb. Chaetobromus involucratus (Schrad.) Nees — | subsp. dregeanus (Nees) Verboom, Nein 1 Bot. 18: 74. 1998. Volume 97, Number 3 2010 Linder et al. Classification of Danthonioideae C Figure 10. Cortaderia bifida. —A. Spikelet. —B. Lem- ma back. —C. Palea. Drawn by Jasmin Baumann from Ramsaus and Arrow-Smith 592. c. Chaetobromus involucratus (Schrad.) Nees subsp. sericeus (Nees) Verboom, Nordic J. Bot. 18: 72. 1998. VIII. Casi Cal U. ser. 3, 22: 378. nom. cons. : Cortaderia selloana C. & Schult. f.) Asch. & Graebn. (= Arundo selloana Schult. & Schult. f.). Figure 10. Moorea Lem., Ill. Ws 2 (Misc.): 15. ay nom rejic., non Moorea Rolf 7. 1890. Gard. Chron., ser. 3 Moorea cca asin rau oe Chest wigan Nees). om H9 — Syst. 37, | 85: 58. 1906, s syn hieronymi (Kuntze) Pilg, (= E hieronymi pot Plants gynodioecious, or female only, or female and apomictic; forming tough, perennial tussocks; culms to 4.5 m tall. Sheaths persistent, leaving a burnt sheath after fire, shiny and white, or variously fragmenting horizontally, or becoming lacerated and curly; ligule ciliate, often with several rows of cilia; leaf blades sclerophyllous, tough, occasionally with a weftlike indumentum on the upper surface directly above the ligule, with a well-developed midrib, often resupinate shortly above the sheath, the ins and often the entire terminal half of the leaves viciously scabrid. Inflorescences paniculate, plumose. Spike- lets generally with more than 2 florets, male spikelets much less hairy than female spikelets; glumes shorter to longer than the florets, 4-22 mm, with up to 5 nerves, glabrous or finely scaberulose; callus rounded or truncate, villous, shorter to longer than the rachilla internode; lemmas with 3 to 7 indistinct veins, dorsally pilose; lemma lobes usually absent, when present small and acute; setae absent to well developed, sometimes appearing as indistinct narrow lobes or teeth on the attenuated part of the central lobe; lemma central awn not differentiated into twisting column and straight apical part, occasionally with the lemma blade extending. to the bristles; ovary glabrous. Caryopsis lorate, elliptical, turbinate, or obovate; embryo 1/4 to 3/5 of the caryopsis length, linear hilum 1/3 to 7/10 of the caryopsis len Cytology. 2n = 36, 72, 108, 136 (Tsvelev, 1984; Connor & Dawson, 1993). Anatomy. The leaves are —. expand- ed; adaxial ribs variously developed; adaxial scleren- chyma in strands, massive T-shaped at or as inversely anchor-shaped girders associated with both 1- and 3-order vascular bundles; the abaxial epider- mis often with a continuous subepidermal layer; clear cells in the chlorenchyma usually present between the vascular bundles directly below the abaxial epider- mis; adaxial bulliform cells usually absent. Distribution and habitat. Cortaderia. in its current delimitation, is restricted to South America, ranging from Tierra del Fuego to Colombia. The southernmost species is found in marshes and wetlands; the Patagonian species mostly along streams on the plains. Around the Amazon Basin the genus is found on mountains, reaching up to 4500 m. In these habitats it Annals of the Missouri Botanical Garden is found in marshes or well-drained grasslands. often dominating the surrounding vegetation. Discussion. Cortaderia is related to Austroderia and Chimaerochloa by the gynodioecious reproduc- tive system, as well as the 3- or 5-veined, narrow le and long lemma hairs. In addition, the glumes have only a single vein. The lemma lateral lobes and their associated setae are poorly devel- oped and in many species scarcely visible, except in the two species previously included in Lamprothyr- sus, where they are conspicuous and almost as long as the awns. As a result, Lamprothyrsus species can be readily distinguished from Cortaderia species, and it is quite possible that the genus is monophy- letie, even though this is not corroborated by the molecular phylogeny. However, Cortaderia is para- phyletic relative to Lamprothyrsus for both the plastid and nuclear genomes, indicating that Lam- ha nas is best regarded as a specialized form of Cortaderia. Consequently, it is impossible to main- tain the formal recognition of the two genera as detailed under those genera. We recognize two sections in Cortaderia. Villa. Cortaderia Stapf sect. Cortaderia. Cortaderia Stapf sect. Mutica Conert, Syst. Anat. Arundineae 114, 1961. TYPE: Cortaderia modes ene Hack. ex Doll . Arundineae Cortaderia aristata Pilg. (= Corta- deria bifida Pilg). er pee Included | species. Although several species of Cortaderia are invasive weeds, there is no recent species-level revision available for the genus. More- over, the delimitations of some species may be questioned. Here, we follow the currently most widely used classification (Connor & Edgar, 1974; Connor, 1983), recognizing 19 species, while fully aware that this could be changed by a critical revision. 1. Cortaderia ugue Stapf, Gard. Chron., ser. 3, 22: 396. 189 2. Cortaderia amensis (Phil. ) Pi Bot. Syst. 37: ares 1906. T He 3. oo bifida Pilg., Bot. Jahrb. Syst. 37: 374. 4. Cortaderia boliviensis Lyle, Novon 6: 72. 1996. 5. Cortaderia e AM Bot. Syst. 37, Beibl. 85: 65. ] . 6. Cortaderia hapalotricha E Conert, Syst. 1 Anat. Arundineae 102. 196 Z. Cortaderia hieronymi (Kuntze) N. P. Barker & € H. P. Linder, comb. nov. Basionym: Triraphis 3. 1898. hieronymi Kuntze, Revis. Gen. Pl. 3: 37. ; Danthonia hieronymi (Kuntze) Hack. ex Stuck- ert, Anal. Mus. Buenos Aires, Ser. III: 4: 484. 1 1906. d hieronymi eese Pig, € Bot. Jahrb. Syst. 37, Beibl. 85: 58. 1906. TYPE: PORTEN “Cordoba, pr. urbem,” 6 Nov. 1881, Hieronymus s.n. (holotype, B!; isotype, K!). 8. Cortaderia jubata (Lemoine) Stapf, Bot. Mag. t. 7607. 1898. 9. Cortaderia modesta (Dóll) Hack. ex Dusén, Ark. Bot. 9(5): 4. 1909. 10. Cortaderia nitida (Kunth) Pilg., Bot. Jahrb. Syst. 37: 374. 1906. 11. Cortaderia peruviana (Hitchc.) N. P. Barker & H. P. Linder, comb. nov. Basionym: Lamprothyr- sus peruvianus Hitchc., Proc. Biol. Soc. Wash. 36: 195. 1923, TYPE: Peru. Yanahuanca, 16-22 E June 1922, J. F. Macbride & W. Featherstone 1205 (type, K not seen). 12. Cortaderia planifolia Swallen, Contr. Natl. Herb. 29: 253. 1949. US 13. Cortaderia pungens Swallen, Contr. U.S. Natl. Herb. 29: 251. 1949, 14. Cortaderia roraimensis (N. E. Br.) Pilg, Notizbl. Königl. Bot. Gart. Berlin 6: 112. 1914. 15. Cortaderia rudiuscula Stapf, Gard. Chron, ser. 3, 22: 396. 1897. 16. Cortaderia selloana (Schult. & Schult. f.) Asch. & Graebn. E Mitteleur. Fl. (Ascherson & Graebner) 2: 325. 1900. 17. Cortaderia sericantha (Steud.) Hitche., Contr. U.S. Natl. Herb. 24: 348. 1927 18. Cortaderia speciosa m Stapf, Gard. Chron., ser. 3, 22: 396. 1 19. Cortaderia vaginata Swallen, Sellowia 7: 9. | 1956. VIIb. Cortaderia Stapf sect. Monoaristata Conert, Syst. Anat. Arundineae 117. 1961. TYPE: Cortaderia pilosa (d'Urv.) Hack. ex Dusén (= Arundo pilosa d'Urv.). Figure 11. The single species in section Monoaristata is * morphologically difficult to distinguish from those m Volume 97, Number 3 Linder et ee of Danthonioideae Figure 11. -Sp Lodicules. Drawn by Jasmin Meus fon Moore Cortaderia pilosa section Cortaderia, but in general the old leaf sheaths remain intact, while in section Cortaderia they usually fragment or become eren There are some leaf anatomical differenc in particular the presence of bulliform ela in the more distal adaxial grooves may be absent from ortaderi l. Cortaderia pilosa (d'Urv. Hack. ex Dusén, Svenska Exped. Magellanslinderna (1895- 1897) 3, pt. 5: 222. 1900. la. Cortaderia pilosa (d’Urv.) Hack. var. pilosa. lb. Cortaderia pilosa (d'Urv.) Hack. var. minima (Conert) Nicora, Darwiniana 18: 80. 1973. IX. Austroderia N. P. Barker & H. P. Linder, gen. noy. TYPE: Austroderia richardii (Endl) N. P. Barker & H. P. Linder is Endl.). EY V ikelet. —B. Lemma back. —C. Palea. —D. Gynoecium with filaments. —E. 1697. Hoc genus apparatu reproductivo a glumis- 1- nerviis et lobis lemmatum pou n Stapf primo aspectu maxi e, sed ab ea costis aliquot per folium differt. Plants gynodioecious, forming tough, perennial tussocks, in one species ipta culms 0.5-6 m tall. Sheaths a shiny and white; ligule ciliate, often with sev rows of cilia; leaf blades scler- ophyllous, debi usually with a weftlike indumentum on the upper surface directly above the ligule, with several prominent, midriblike veins, the margins often the entire terminal half . Inflorescences paniculate, plumose. Spikelets generally with more than 2 florets, male spikelets much less hairy than female spikelets; glumes at least as long as the florets, 11.5-40 mm, with 1 nerve, glabrous or finely scaberulose; callus rounded or truncate, villous, shorter to longer than the rachilla internode; lemmas 3-veined, dorsally pilose; lemma lobes usually absent, when present small and acute, of the leaves viciously Annals of the Missouri Botanical Garden setae absent to well developed; lemma central awn not differentiated into twisting column and straight apical part; paleae lorate to linear, occasionally with tufts of long hair on the palea margins; lodicules rhomboid to cuneate, generally with microhairs and bristles; ovary glabrous. Caryopsis lorate, elliptical, turbinate, or obovate; embryo and linear hilum ca. 1/2 as long as the caryopsis. Cytology. 2n = 90 (Hair & Beuzenberg, 1966; Murray et al., 2005). Anatomy. The leaves are sclerophyllous, expanded: adaxial ribs variously developed; with 1-, 2-, and 3-order vascular bundles; adaxial sclerenchyma as strands, massive T-shaped girders, or inversely anchor-shaped girders associated with all vascular bundles; the abaxial epidermis often with a continuous subepidermal layer; adaxial bulliform cells usually absent. Distribution and habitat. Austroderia is restricted to New Zealand, where it occupies diverse habitats: along streams, on beaches, and on coastal cliffs. Most of these habitats seem to be exposed to regular, and possibly quite massive, disturbance. Discussion. The genus Austroderia is related to Cortaderia and Chimaerochloa by the gynodioecious reproductive system, as well as the 3-veined narrow lemmas and long lemma hairs, and awns without twisted columns. In addition, the glumes have only a single vein. The plants are massive, and the i ces are huge and plumose. In particular, it is difficult to differentiate Austroderia from Cortaderia, and there seem to be no clear morpho- logical differences in the spikelets. Geographically, Cortaderia is found in South America and Austroderia in New Zealand. However, the Most striking differ- ences are in the leaf anatomy. The leaf blades of Austroderia have several prominently sclerified veins in addition to the midrib, com where only the midrib is sheaths of Austroderia mesophyll while in Cortaderia there are usually zones of clear cells directly below the abaxial epidermis, often between the veins or ribs, Ety * The name Austroderia js derived from the Latin "australis," meaning “southern,” and from the genus name Cortaderia. Included Species. This small Eenus includes only five species, revised in the Flora of New Zealand under the generic name Cortaderia (Edgar & Connor, 2000). 1. Austroderia fulvida (Buchanan) N. P. Barker € H. 84. 1963. TYPE: New Zealand. Wellington, s.d., ; J. Buchanan s.n. (holotype, WELT not seen). | 2. Austroderia richardii (Endl.) N. P. Barker & H. P. Linder, comb. nov. Basionym: Arundo richar- dii Endl., Ann. Wiener Mus. Naturgesch. 1: 158. 1836. Replaced s Arundo australis A. Zelande, s.d., Herb. Rich. no. 29 (holotype, P not seen; isotype, CHR 236584 not seen). 1971. TYPE: New Zealand. Ruapuke Beach, 20 : Dec. 1967, Bell s.n. (holotype, CHR 184354 not seen). a 4. Austroderia toetoe (Zotov) N. P. Barker & H. P. — Linder, comb. nov. Basionym: Cortaderia toetoe Zotov, New Zealand J. Bot. 1: 85. 1963. TYPE: New Zealand. Wainui-o-mata Valley, s.d., V. D. Zotov s.n. (holotype, CHR 95457 not seen). 5. Austroderia turbaria (Connor) N. P. Barker & H. P. Linder, comb. nov. Basionym: Cortaderia a turbaria Connor, New Zealand J. Bot. 25: 167. f 1987. TYPE: New Zealand. Chatham Island, T Rakeinui, sd, D. R. Given 13899 (holotype, CHR 417471 not seen). Plinthanthesis Steud., Syn. Pl. Glumac. 1: 14. 1853. TYPE: Plinthanthesis urvillei Steud. (lecto- type, designated by Blake [1972: 3]). Figure 12. Danthonia sect. Micrathera Benth., Fl. Austral. 7: 590. 1878. Blakeochloa Veldkamp, Taxon 30: 478. 1981. TYPE: — — Danthonia paradoxa R. Br. Plants forming perennial tussocks; culms 0.2-lm tall. Sheaths persistent, shiny and white; ligule ciliate; leaf blades orthophyllous, persistent on the sheaths. nees paniculate, open. Spikelets generally Volume 97, Number 3 2010 Linder et al. 345 Classification of Danthonioideae Figure 12. Plinthanthesis paradoxa. —A. Spikelet. —B. Lemma back. —C. Palea. Drawn by Jasmin Baumann from Pirie 320. with 2 to 4 florets; glumes shorter to longer than the florets, 5-9.5 mm, with 3 to 7 nerves; callus rounded or truncate, villous, less than 1/2 the length of the rachilla internode; lemmas 9-veined, dorsally with a felt of short hair in the lower half, apices tridentate to lobed, then lobes shorter than the lemma body, often fused to the central awn, setae absent; lemma central awn varying from very short (central point of tridentate lemma), generally poorly developed with a twisting base, to exceeding the lemma lobes; paleae lorate to linear, pubescent to villous on the backs in the lower half; lodicules cuneate, glabrous; ovary glabrous. Caryopsis turbinate, embryo 1/3 and the linear hilum ca. 1/2 as long as the caryopsis. Nomenclatural note. Veldkamp (1980, 1981) proposed Plinthanthesis tenuior Steud. as lectotype, but this was rejected as superfluous to Blake’s lectotypification by Connor and Edgar (1981) and later by Jacobs (1982). Cytology. Unknown. Anatomy. The leaves are orthophyllous, expand- ed; adaxial ribs convex, poorly developed; adaxial sclerenchyma as strands, massive T-shaped girders, or y Koeha shaped gu. Maec e all phloe islands of clear cells in the chlorenchyma + Siles adaxial bulliform cells sometimes present. Distribution and habitat. These three species are restricted to the coastal plains and sandstones of the Australian east coast, where they occur in heathland, usually on oligotrophic soils. Discussion. Plinthanthesis is closely related to Notochloe by the empty cell spaces in chlorenchyma, a short callus with a horizontal joint to the rachilla, very short awns, and a turbinate caryopsis. However, Plinthanthesis is very distinct in appearance, with much shorter spikelets that have at most four florets (with at least seven in Notochloe) and lemmas that are lobed and awned, rather than finely tridentate. Characteristic in Plinthanthesis, too, is the feltlike short indumentum on the lower half of the backs of the lemmas and paleae Included species. Three species are included in this genus; these were revised for the floras of New South Wales (Jacobs, 1994) and Australia (Linder, 2005) 1. Plinthanthesis paradoxa (R. s ha T. Blake, Contr. Queensland Herb. 14: 3 2. Plinthanthesis rodwayi (C. E. Hubb.) S. T. Blake, Contr. Queensland Herb. 14: 3. 1972. . Plinthanthesis urvillei Steud., Syn. Pl. Glumac. 1: 14. 1853 XI. Notochloe Domin, Repert. Spec. Nov. Regni Veg. 10: 117. 1911. TYPE: Notochloe microdon (Benth.) Domin (= Triraphis microdon Benth.). Figure 13. Plants forming perennial tussocks with diverging straight culms, 0.3—1 m tall. Sheaths persistent, shiny and white; ligule ciliate; leaf blades orthophyllous, persistent on the sheaths. Inflorescences paniculate, open. Spikelets elongated, generally with 7 to 9 florets; glumes shorter than the florets, scarcely overtopping the basal lemma, with 3 nerves, 4.5- 5.5 mm; callus rounded or truncate, shortly villous, less than 1/2 the length of the rachilla internode; lemmas 7-veined, glabrous, apically tridentate, thus without lobes or central awn; paleae linear, glabrous except for the scabrid keels; lodicules 3-lobed, shortly ciliate along the upper margin, without microhairs; ovary glabrous. Caryopsis turbinate, the embryo 1/3 and the linear hilum ca. 1/2 as long as the caryopsis. Annals of the Missouri Botanical Garden Figure 13. Piin. mma back. —C. Palea. Drawn by lear: Pirie 326. wn by Jasmin Baumann from Notochloe mier —A. Spikelet. —B, Cytology. Unknown. y. The leaves are orthophyllous, e - ed, not ribbed adaxially; midrib flank aps ai with adaxial bulliform cells; 1 adaxially with narrow e; ; oem with a thickened sheath; mesophyll ith islands of colorless cells between M US bundles, Distribution and habitat. This species is restrict- ed to the sandstones of the Blue Mountains inland from Sydney, where it occurs along the banks of streams | Discussion. Notochloe is related to Plinthanthesis by the empty cell spaces in chlorenchyma, a short _ callus with a horizontal joint to the rachilla, very short awns, and a turbinate caryopsis. The empty spaces in the chlorenchyma are unusual for Danthonioideae, d where the chlorenchyma is generally quite compact. x These cavities seem to form from large, empty cell — | that then disintegrate, leaving rather ragged cavities. In its appearance, Notochloe is very different from Plinthanthesis, with much longer spikelets that have at least seven florets, and lemmas that are finely ` tridentate, rather than lobed and awned. Unusual for > the subfamily, the lemmas are glabrous in Notochloe. — e diaeresis use in Notochloé, which implies that - the two vowels are pronounced separately, and which was used in the Flora of Australia (Linder, 2005), is explicitly permissable under Article 60.6 (McNeill et al., 2006). However, the original spelling was without the diaeresis, as “Notochloe,” and this is to be retained (Rule 60.1) unless there is an orthographic error. The permissable retention of the diaeresis under Article 60.6 most likely does not constitute a correctable error. Included species. The genus is monotypic; the species is described in the floras of New South Wales (Jacobs, 1994) and Australia (Linder, 2005). 1. Notochloe microdon (Benth.) Domin, Repett. Spec. Nov. Regni Veg. 10: 117. 1911. XII. Chimaerochloa H. P. Linder, gen. nov. TYPE: Chimaerochloa archboldii (Hitchc.) Pirie & H. P. Linder (= Danthonia archboldii Hitchc.). Fig- ure 14, Genus novum quod a Cortaderia Stapf lobis lemmatum ` U bene evolutis, a Danthonia DC. lemmatibus 3-nerviis recedit. Plants forming tough, perennial tussocks, gyno- dioecious; culms 0.25—1.4 m tall. Sheaths brown and - x persistent; leaf blade abscissing from the sheath; 3 U ligule ciliate; leaf blades sclerophyllous, tough. expanded, glabrous. Inflorescences paniculate, open A i to lobed. Spikelets with 2 to 7 florets, all similar; — glumes shorter than the florets, 6-9 mm, with 1 to 3 x nerves; central nerve much better developed than the lateral nerves; callus rounded or truncate, villous, longer than the rachilla internode; lemmas with 3 pes dorsally pilose; lemma lobes acute, shorter than ` lemma body, closely adjacent to the central awn, — extended into short terminal setae; lemma central awn exceeding the lemma lobes, weakly differentiated into a flat, corkscrewed base and a straight, hairlike apical part; paleae lorate to linear, margins glabrous; lodicules rhomboid, with microhairs and bristles; E Volume 97, Number 3 2010 Linder et al. 347 Classification of Danthonioideae Figure 14. Chimaerochloa arc —A. Spikelet. —B. Lemma pr —C. Palea. eet " Jasmin Baumann from Robbins 62 ovary glabrous. Caryopsis lorate, embryo about 1/2 and the linear hilum about 1/3 of the caryopsis length. mrt 2n = 72 (Borgmann, 1964). The leaves are sclerophyllous, expand- a adaxial ribs massive, separated by deep cleftlike furrows; adaxial sclerenchyma as massive T-shaped or inversely anchor-shaped girders associated with all vascular bundles; midrib flanked adaxially by bulli- form cells. Distribution and habitat. This genus is restricted to the mountains of New Guinea, where it is a common element in the alpine grassland Discussion. This peculiar genus is linked to the Danthonia clade by the possession nodioecious sexual system. The disarticulating aye link this genus to Chionochloa, but it can be separated by the rous palea margins and by the generally pilose lemma backs, It can be separated from Cortaderia by the relatively well-developed lemma lobes with short setae (in Cortaderia the setae are generally better "Anab. sí ài x ki x 3k uu Posi qum more clearly differentiated into a column and limb. ccording to the molecular phylogeny, the closest relationship is to Danthonia, which has a dramatically different lemma construction and i à Etymology. The species takes on the appearance of different genera, depending on which character set is investigated. Thus, it can be regarded as a grass that changes its appearance, a chimaera. Included species. Only a single species is included in this p It is also treated in this sense in the Alpine Flora of New Guinea (Veldkamp, dig However, it is possible that the synonymized Dant, nia macgregorii Jansen should also be medi at specific level. 1. Chimaerochloa archboldii (Hitchc.) Pirie & H. P. Linder, comb. no ionym: Danthonia nobles Hitchc., on 2: 114. 1936. Cortaderia archboldii (Hitchc.) Connor & Edgar, Taxon 23: 596. 1974. Chionochloa archboldi; (Hitche.) Conert, Senckenberg. Biol. 56: 156. 1975. TYPE: New Guinea. Central Division: Wharton Range, Murray Pass, 2800 m, 12 June 1933, L. J. Brass 4194 (holotype, US not seen). Danthonia macgregorii Jansen, Fonwardtia 2: 262, bg 6. 1953. TYP Stanley Range, 1889, W. MacGregor s.n. J (holotype, MEL!; isotypes, BM not seen, C not seen, L not seen). . Danthonia DC., Fl. Franc. (DC. & Lamarck), ed. 3, 3: 32. 1805, nom. cons. Merathrepta Raf., E Bot. (Geneva) 1: 221. 1830, nom. superfl. Danthonia spicata (L.) P. Beauv. ex Roem. a Schult. (= Avena spicata L.), typ. cons. Figure 15. — Bernh., Syst. Verz. a 20, 44. 1800. achatera Desv., Nouv. Bull. Sci. Philom. Paris 2: ue 1810, nom. superfl. Wili Pfl. Gebirgsart. Mari 38. 1837, nom. superfl. Brachyanthera Kunze in Post, Lexicon 77. 1903, nom. superfl. TYPE: Sieglingia decumbens (L.) Bernh. (= Festuca decumbens L.), nom. rejic. Plants perennial, caespitose, culms 0.1—1.2 m tall, often with cleistogenes in the axils of the upper leaves. Sheaths white or brown, persistent or decay- ing, leaf blades persistent; ligule ciliate; leaf blades orthophyllous, expanded, glabrous or villous, rarely with a web of hair adaxially above the ligule. nflorescences racemose to paniculate, open to contracted. Spikelets with 2 to 10 similar florets; glumes shorter to longer than the florets, 7-30 mm, with 3 to 9 nerves; callus rounded or truncate, villous, shorter to much longer than the rachilla internode; mas with 5 to 9 veins, dorsally pilose or Annals of the Missouri Botanical Garden igure 15. Danthonia inte by Jasmin Baumann from Elmer 1662. indumentum restricted to the lemma margins, apically tridentate to more commonly lobed; lemma lobes acute, shorter to longer than the lemma body, usually extended into terminal setae; lemma central awn exceeding the lemma lobes, differentiated into a flat, rewed base and a straight, hairlike apical part; paleae lorate to linear, keels sinuose, scabrid, rarely Cytology. 2n — 18, 24, 36, 48, 72, 98 (Stebbins & Love, 1941; de Wet, 1953, 1954; Bowden, 1960; Live & Live, 1961; Bowden & Senn, 1962; Packer, 1964; SE SS 7, Un yi WAIA SS s A WJ \ ia subsp. intermedia. —A. Spikelet. —B. Lemma back. —C. Palea. —D. Anthers. Drawn Quinn & Fairbrothers, 1971; Davidse & Pohl, 1972; Baeza, 1996b). Anatomy. The leaves are orthophyllous or rarely sclerophyllous, expanded; adaxial ribs usually poorly developed; adaxial sclerenchyma as small scleren- chyma strands, or with T-shaped or inversely anchor- shaped girders, associated with all vascular bundles; bulliform cells usually present. Distribution and habitat. Danthonia is wide- spread in the temperate parts of South and North America, with two species present in Europe. In North America and Europe, the’ species are associated with a mesic meadows, open woodlands, coastal meadows, OS and marshes. Volume 97, Number 3 2010 Linder et al. Classification of Danthonioideae Discussion. The genus Danthonia is related to pean, Chimaerochioa, Plocensis, "i Na: chloe, t t characterize this relationship. Danthonia š is distinct by being basically hexaploid, and by many of the species having cleistogenes in upper leaf axils. It differs from Plinthanthesis and Notochloe by the longer awns and well-developed lemma lobes, and from Austroderia by the masny-ycined nen sad dune k. lobes. , Danthonia has soleado fat spikelets, i.e., spikelets that are rather wide in comparison to their length. Included species. There is no global revision of the 25 included ips available. The North American species have been treated in the Flora of North America (Darbyshire, 2003), but the South and Central American species have not benefited from a careful critical treatment. 1. Danthonia alpina Vest, Flora 4: 145. 1821. 2. Danthonia — P. M. Peterson & Rugolo, Madroño 40: 71. 3. Danthonia araueana Phil., Anales Univ. Chile 94: 31. 1896 4. Danthonia boliviensis Renvoize, Gram. Bolivia 5. Danthonia breviseta Hack., Oesterr. Bot. Z. 52: 192. 1902 6. Danthonia californica Bol., Proc. Calif. Acad. Sci. 2: 182. 1863 6a. Danthonia californica Bol. var. californica. 6b. Danthonia californica Bol. var. americana (Scribn.) Hitche., Proc. Biol. Soc. Wash. 41: 160. 1928. 7. Danthonia chaseana Conert, Senckenberg. Biol. 54: 308, fig. 5. 1975. 8. Danthonia chiapasensis Davidse, Novon 2(2): 100. 1992. 9. Danthonia chilensis E. Desv., Fl. Chil. (Gay) 6: 360. 1854 9a. Danthonia chilensis E. Desv. var. chilensis. 9b. Danthonia chilensis E. Desv. var. aureofulva (E. Desv.) C. M. Baeza, Sendtnera 3: 32. 1996. 9c. Danthonia chilensis E. Desv. var. glabriflora Nicora, Darwiniana 18: 82. 1973. 10. Danthonia cirrata Hack. & Arechav., Anales Mus. Nac. Montevideo 1: 367, t. 40. 1896. 11. Danthonia compressa Austin, Rep. (Annual) New York State Mus. Nat. Hist. 22: 54(-55). 1869. 12. Danthonia decumbens (L.) DC., Fl. Franc. (DC. & Lamarck), ed. 3, 3: 33. 1805. 13. Danthonia domingensis Hack. & Pilg., Symb. Antill. (Urban) 6: 1. 1909. 13a. Danthonia domingensis Hack. & Pilg. subsp. domingensis. 13b. Danthonia domingensis Hack. & Pilg. subsp. obtorta (Chase) Conert, Senckenberg. Biol. 56: 301. 1975. 13e. Danthonia domingensis Hack. & Pilg. subsp. shrevei (Britton) Conert, Senckenberg. Biol. 56: 301. 1975. 14. Danthonia holm-nielsenii Laegaard, Fl. Ecua- dor 57: 17. 1997. 15. Danthonia intermedia Vasey, Bull. Torrey Bot. Club 10: 52. 1883. 15a. Danthonia intermedia Vasey subsp. inter- media. 15b. Danthonia intermedia Vase p. riabus- chinskii (Kom.) moe Zlaki En 610. 1976. 16. Danthonia malacantha (Steud.) Pilg., Notizbl. Bot. Gart. Berlin 10: 759. 1929 17. Danthonia melanathera (Hack.) Bernardello, Kurtziana 10: 249. 1977. 18. Danthonia montevidensis Hack. & Arechav., Anales Mus. Nac. Montevideo 1: 369. 1896. 19. Danthonia parryi Scribn., Bot. Gaz. 21: 133. 1896. 20. Danthonia rhizomata Swallen, Comun. Bot. Mus. Hist. Nat. Montevideo 39: 2. 1961. 21. Danthonia rugoloana Sulekic, Darwiniana 37: 341. 1999. 22. Danthonia secundiflora J. Presl & C. Presl, Reliq. Haenk. 1: 255. 1830. 22a. Danthonia secundiflora J. Presl & C. Presl subsp. secundiflora. 22b. Danthonia sec J. Presl & C. Presl subsp. charruana d Roseng, B. R. Arrill. & Izag., Gram. Urug. 55. 1970. 350 Annals of the Missouri Botanical Garden p 16. Tenaxia stricta. —A, Spi ien M pikelet. —B. Lemma back. —C. Palea. —D. Lodicules. Drawn by Jasmin Baumann 22c. Danthonia secundiflora J. Presl & C. L. 25. D. subsp. mattheii C. M. Baeza, Sendinera anthonia unispicata Eco Me Cat. Canad. Pl. Endogens 2: 215. 1888. XIV. Tenaxia N. P. Barker & H. P. Linder, gen. nov. eo . TN == Nutt., Gen. N. Amer. PL TYPE: Tenaxia stricta (Schrad.) N. P. Barker & H. P. Linder (= Danthonia stricta Schrad.). Figure 16 23. 24. Danthonia spicata (L.) P, Beauv. ex R Schult., Syst. Veg, ed 15 bis e š Hoc genus Schismo P. Beauv. maxime simile, sed ab eo Schultes), 2: 690. 1817 habitu i renni et lemmatibus semper lobatis arista centrali excedente tinguitur. Volume 97, Number 3 2010 Classification of Danthonioideae Linder et al Plants wiry, perennial tussocks without stolons, culms 0.12-0.9 m tall. Basal sheaths shiny and persistent; ligule ciliate; leaf blades occasionally with a web of interlocking hairs adaxially above the ligule, often rolled or planes rarely expsaded, Ta ores- Cences in sha libiar to open and tx anded, sarind, or Toun Spikelets with 2 to 7 florets; glumes usually at least as long as the florets, 7-25 mm l to 11 veins, glabrous or scaberulose on the keile callus rounded, villous, shorter to longer than the rachilla internode; emmas 7- to 9-veined, indumentum variously orga- nized, from pilose to tufted, tufts usually + marginal, from 1 to several; lemma lobes at most as long as the lemmas, acute, setae when present either terminal or rom the inner lobe geniculate, the column twisted, the apical portion straight, much longer than the lem lorate, narrowly t. or ette except for the scabrid gins; lodicules cuneate to more usually Du m bristles as well as microhairs; ovary glabrous. Fruit a nutlet or caryopsis, lorate; embryo between 1/3 and 1/2 and the linear, elliptical, or punctate hilum 1/5 to 4/5 of caryopsis length. margins; lemma central awn Cytology. 2n = 12, 36, 56 (De Wet, 1954; Spies & du Pissis. 1988). Anatomy. Leaves sclerophyllous, expanded or setaceous; adaxial ribs variously developed; adaxial sclerenchyma as strands, T-shaped girders, or in- versely anchor-shaped girders associated with both 1- and 3-order vascular bundles; abaxial sclerenchyma girders or rarely linked to form a continuous asoita layer; leaves in several species asym- metrical, with more veins in 1/2 than the other; bulliform cells sometimes present. Discussion. The new genus Tenaxia is associated with the Rytidosperma clade, in which it is grouped by both the molecular plastid and nuclear partitions. The only morphological character linking these species to the Rytidosperma clade is the generally short, punctate hilum on the caryopsis. The genus can be y a combination of several characters. The leaves are often (but not in T. cumminsii (Hook. f.) N. P. Barker & H. P. Linder) rolled and sclerophyllous, and the plants form persistent, small, tough, wiry insii). The lemma variation is useful for distinguishing the species. However, the regular 2-row pattern of lemma indumentum common in Ryti is not found here. The lemmas in Tenaxia are deeply lobed, and the lobes are extended into acuminate, setalike ices. These setae are consequently usually poorly differentiated from the lemma lobe and shorter than the lobes (except in T. disticha (Nees) N. P. Barker & HE wes The inflorescences are more or less tracted, sometimes even spikelike, or with the ical rus much reduced; the glumes have several veins. In two species (T. disticha and T. stricta), the setae originate in the lemma sinus, as is characteristic in Pentameris, but these two species can be separated from Pentameris as they have more than two flowers per spikelet. Finally, in several species the leaves are asymmetrical, with more veins in one half than the other. This strange attribute is also found in Merxmuellera s. str. and Capeochloa. However, none of these characters are unique to Tenaxia. Distribution and habitat. The species of Tenaxia are typical montane grasses, widespread in the African mountains, and reaching the Himalayas. This is the dominant grass on the higher and cooler mountains in the Great Karoo of South Africa, but is rare in the Ethiopian uplands. The species are often found in dry, or at least seasonally dry, grassland. In this it differs from the other Afromontane genus of danthonioid grasses, Merxmuellera s. str., which is more typical of wetter grasslands. There are excep- tions to this pattern and several species are found in permanent bogs. ymo. He name refers to the ugh. leaves us. Such to ugh nd are quite emnt à in the aides: Mores, in Tenaxia, the plants form tough tussocks capable of withstanding drought and are often found in rather harsh habitats. Included species. The eight species included in the new genus Tenaxia were previously classified in Merxmuellera and Danthonia. The species have been taxonomically treated in various floras, in particular the southern African grass account (Gibbs Russell et al., 1990) and the Flora of Ethiopia and Eritrea (Phillips, 1995). However, although there have been several regional treatments, a critical treatment of Tenaxia in the Himalayas that considers the taxa across the whole region still ns to be done 1. Tenaxia aureoc (J. G. Anderson) N. P. Barker & H. P. Linder, comb. nov. Basi Danthonia aureocephala J. G. Anderson, Bethe: lia 8: 170. 1964. Merxmuellera aureocephala (J. G. Anderson) Conert, Senckenberg. Biol. 51: 132. 1970. TYPE: South Africa. KwaZulu-Natal: Annals of the Missouri Botanical Garden Cathedral Peak Forest Research Station, s.d., D. J. B. Killick 1727 (holotype, PRE!) 2. Tenaxia eachemyriana (Jaub. & Spach) N. P. Barker & H. P. Linder, comb. nov. Basionym: Danthonia cachemyriana Jaub. & Spach, Ill. Pl. Orient. 4: 46, pl. 331. 1851. TYPE: India. “ad rupes editissimas Emodi Cachemyriani legit Jacquemont, 8/1831,” V. Jacquemont s.n. (holo- type, P not seen). 3. Tenaxia cumminsii (Hook. f.) N. P. Barker & H. P. Linder, comb. nov. Basionym: Danthonia cumminsii Hook. f., Fl. Brit. India (J. D. Hooker) 7: 282. 1896. Danthonia jac rahe Bor, Kew Bull. 7: 80. 1952, nom. superfl. TYPE: India. Bhotan, Gnatong, Sikkim frontier, s.d., Cummins s.n. (holotype, K not seen). Danthonia cachemyriana Jaub. & S Spach var. minor Hook. f., Fl. Brit. mda -D D. Hooker) 7: 282. 1896. Danthonia ar. minor (Hook. f.) Bor, Kew Bull. 7: 81. India. “Alpine Himalaya, rachey & Winterbot- honia schneideri Pilg., Repent. S> Nov. Regni Veg. 17: 131.1921. TYPE: China. “Yunnan, auf alpinen Wiesen an der Südsiete der Berge bei Lichiang, 4200 m.," Sep. 1914, C. Schneider 2. lotype, B; isotypes, FR!, K!, US 776504 not seen). Bor (1952) proposed Danthonia ; Jacquemontii as a replacement name for D. cachemyriana Hook. f., which he realized was misapplied. However, he iind t D. cumminsii Hook. f. was an abnormal form of D. cachemyriana var. minor Hook. f., thus rendering his own D. jacquemontii superfluous. Co ently, D. jacquemontii var. minor (Bor) Hook. f. is ‘lec invalid. 4. Tenaxia disticha (Nees) N. P. Barker & H. P. Linder, comb. nov. Basionym: ticha Nees, FI. . Mess. disti colla — Conert, Sencken- [South Alrica.] “in pes ae d it, ae ectotype, by Conert [1970- sien HEGI, isotype, SI). 5. Tenaxia dura (Stapf) N. P. Barker & H. Linder, comb. nov. Bas Basionym: t ym: Danthonia dura Stapf, Fl. Cap. (Harvey) 7: 527. 1899. Men muellera dura (Stapf) ut Senckenberg. 9l: 132. 1970. : South du PA Danthonia brachyacme "q Bot. Jahrb. Syst. 44: 114. 1909. TYPE: South Africa. Calvinia, “Suedost Hang des Roepmyniet,” 1000. m, 15 Sep. 1900, Diels 676 (holotype, B not seen; isotype, B fragm. at FR!). 6. Tenaxia guillarmodiae (Conert) N. P. Barker & H. P. Linder, comb. nov. Basionym: Merxmuel- lera guillarmodiae Conert, Senckenberg. Biol. 56: 145. 1975. TYPE: Lesotho. Butha-Butha, Ischlanyana Valley, s.d., A. Jacot Guillarmod 2320 (holotype, RUH!; isotype, FR not seen). 7. Tenaxia stricta (Schrad.) N. P. Barker & H. P. Linder, comb. nov. Basionym: Danthonia stricta Schrad., Mant. 2 (Schultes), 383. 1824. Penta- meris stricta (Schrad.) Nees, Linnaea 7: 310, 313. 2. Chaetobromus strictus (Schrad.) Nees, Fl. Afr. Austral. Ill. 341. 1841. Merxmuellera stricta (Schrad.) Conert, Senckenberg. Biol. 51: 133. 1970. TYPE: South Africa. Cape Town, s.d., C. H. F. Hesse s.n. (holotype, GOET 2247!; isotype, C!). 8. Tenaxia subulata (A. Rich.) N. P. Barker & H. P. E: Ethiopia. "crescit in montosis provinciae Ouodgerate," s.d., A. Petit s.n. (holotype, P not seen; isotype, P fragm. at KI). Danthonia candida Hochst. ex Steud., Syn. Pl. Glumac. 1: 1854. TYPE: Ethiopia. Debra Eski, 9000', Nov. W. G G. Schimper s.n. DE fragm. at FRI, P fragm. a P. Beauv., Ess. Agrostogr. 73, Pl. xv, - Schismus fig. iv. 1812. Elecira. Panz., Ideen Rev. Gráse 49. 1813; Denkschr. Kónigl. d. Miinchen 4(3): 299. 1814, nom. superfl. Schismus calycinus (Loefl.) K Chase [1925: 181]. Figure 17 TRAC gonatodes Steud. (— Schismus barbatus (L.) Thell.). Plants small, tufted, softly herbaceous, annual or perennial, without stolons; culms 0.05-0.35 m tall. es ciliate; leaves o orthophyllous, often rolled, ov., not seen; isdtypil P r Akad. Wiss. E: . Koch (= Festuca calycina Loefl.) (lectotype, designated by Niles & Steud., Flora 12: 490. 1829. TYPE: Hemisacris glabrous or pilose. Inflorescences sparsely to widely ` paniculate, Rc contracted or open. Spikelets Scattered or as marginal tufts or in longitudinal lines, i linear or rarely clavate; lemma apex tridentate to lobed; lemma lobes rounded t to acute or acuminate, Khel Rd du oo EF ine (holotype, K not seen: seen; isotype, SÌ). Volume 97, Number 3 Linder et al. Classification of Danthonioideae Figure 17. Schismus barbatus —A. Spikelet. Lemma back. —C. Palea. Drawn br Jasmin Baumann Moore 8205. —B. from muticous or with short apical setae; lemma central awns usually minute or small, scarcely taller than the lobes, occasionally well developed with a twisted column and a long straight limb; paleae obovate to lorate, sometimes with tufts of hairs on the margins es square to cuneate, usually with both bristles and microhairs. Caryopsis lorate, elliptical to obovate, embryo about 1/2 and the ovate to punctiform hilum about 1/5 as long as the caryopsis. Cytology. 2n = 12, 24, 36, 48, 72 (Gould, 1958; Live & Live, 1961; Bowden & Senn, 1962; Faruqi & Quraish, 1979; du Plessis & Spies, 1988; Spies & du Plessis, 1988). Leaf orthophyllous, expanded or folded, adaxially scarcely grooved; adaxial and abaxial sclerenchyma as small strands or poorly developed girders; bulliform cells absent. Distribution and habitat. This is an African and southern European genus, with a remarkable trans- African disjunction: one species is restricted to the shores of the Mediterranean, a second species is disjunct between South Africa and the northern margins of the Sahara, and the romaine ui» are South African. Most peci to dry habitats. Two species (Schismus arabicus Nees and S. erben (L.) Tel p —— worldwide = j weeds, mostly associated f wheat. Discussion. Schismus is linked to the Rytido- sperma clade by a caryopsis with a punctate-ovate hilum and the small tufted growth form. Within this clade the genus can, to some extent, be diagnosed by the very short central awn, which is generally shorter than the lemma lobes. However, S. schismoides (Stapf ex Conert) Verboom & H. P. Linder is an exception, in that it has an articulated central awn more typical for danthonioid taxa. Another unusual feature is that the glumes are relatively short, but this attribute also occurs occasionally in other genera of the Rytido- sperma clade. Included species. We include five species in the genus Schismus. The species in this genus were carefully and critically revised by Conert and Tii (1974), and subsequent floristic treatments followed the Conert and Tiirpe classification. 1. Schismus arabicus Nees, Fl. Afr. Austral. Ill. 422. 1841. 2. Schismus barbatus (L.) Thell., Bull. Herb. Boissier, ser. 2, 7: 391. 1907. 3. Schismus inermis (Stapf) C. E. Hubb., Fl. Trop. Afr. (Oliver et al.) 10: 147. 1937. 4. Schismus scaberrimus Nees, Fl. Afr. Austral. Ill. 423. 1841. 5. Schismus schismoides (Stapf ex Conert) Verboom & H. P. Linder, comb. nov. Basionym: Danthonia schismoides Stapf ex Conert, Senckenberg. Biol. 46: 180. 1965. Karroochloa schismoides (Stapf ex Conert) Conert & Türpe, Senckenberg. Biol. 50: 299. 1969. TYPE: South Africa. Great Buschman- land, sed s.d., R. Schlechter s.n. (holotype, K not seen; isotypes, E!, L not seen, Z!). XVI. Tribolium Desv., Opusc. Sci. Phys. Nat. 64. 1831. TYPE: Tribolium hispidum (Thunb.) Desv. (= Dactylis hispida Thunb.). Figure 18. Lasiochloa S € Gramin. 2: 556. 1 Allagosta m. Steud., Nomencl. Bot. s ed. 2, 1840, n nom. nud., nom. superfl. TYPE: Lasiochloa agli (Schrad) Kunth (= Ga pe Sc (Thunb.) Des rad., = Tribolium hispi — Steud., Nomencl. Bot. (Steudel), ed. 2, 2: IL 1841, val., in s Tribolium echinatum ) enin Hystringium acuminatum Trin. ex Steud., Nomencl. fu et Bid 1841. nom. inval., pro syn. ciliaris K: — Stapf, Fl. Cap. are) 7:3 a ee 701. 1898, 1900, illeg., non Brizopyrum Link, 1827. Plagiochloa Annals of the Missouri Botanical Garden Figure 18. Tribolium echinatum. —A. Spikelet. from n 745. Adamson & Sprague, J. S. African Bot. 7: 89. 1941. TYPE: Brizopyrum capense (Spreng.) Nees (= Cyno- uniolae L. f.) surus E Urochlaena Nees, Fl. Afr. Austral. Ill. 437. 1841. TYPE: Urochl. ; Karroochloa Conert & Türpe, Senckenberg. Biol. 50: 290. 1969, syn. nov. TYPE: curva (Nees) Conert & Türpe (= Danthonia curva Nees) Plants small, tufted, herbaceous, annual or peren- nial, culms 0.03-0.6 m tall, glabrous or variously pilose or hispid, often with long stolons. Ligules ~B.: Glume. —C. Lemma back. —D. Palea. Drawn by Jasmin Baumann ciliate; leaves orthophyllous, expanded or setaceous. Inflorescences racemose to paniculate, secund or not, spicate, contracted, capitate or rarely + expanded and open, in one case disarticulating below the. inflorescence. Spikelets with 2 to 10 florets; glumes shorter to longer than the florets, 2-7.5 mm, with 3 to 5 veins, glabrous or hispid with tubercle-based hairs; callus rounded, villous, shorter or longer than the rachilla intemode; lemmas with 7 or 9 veins; lemma dorsal indumentum either pilose or tufted with tufts in various patterns, hairs either simple or clavate; lemma Volume 97, Number 3 2010 Linder et al. Classification of Danthonioideae apically acute, tridentate or lobed; lemma lobes rou or acute or acuminate, rarely with short apical setae; lemma central awns poorly developed as the continuation of the acuminate lemma, or as a short central point in a tridentate lemma, or as a geniculate structure with a corkscrewed basal column and a iai apical part; paleae obovate to lorate, apically emarginate or bilobed; keels scabrid, often "i tufts of hair on the margins, between the keels glabrous, EREN or villous; jodid cuneate, bristles and microhai times present; ovary glabrous. id lorate, elliptical, or obovate; wall Az $ 1:1 LI C th A K y sep ; yo 1/3 to 2/3 and the ovate to punctate hilum less than 1/3 of the caryopsis len Nomenclatural note. Karroochloa has to be in- cluded in Tribolium, as three of the four species assigned to the genus (including the type) are nested within Tribolium according to the molecular phylog- eny (Verboom et al., 3008. The fourth pocis, K. ismoides, is nested in 1 t Cytology. 2n = 12, 24, 36 (de Wet, 1954, 1960; Spies & du Plessis, 1986, 1988; Visser & Spies, 1994c, d, e; Baeza, 1996b). Anatomy. Leaf anatomy orthophyllous; adaxial ribs absent or weakly developed, rounded; adaxial sclerenchyma usually as small strands, rarely T- shaped or as inversely anchor-shaped strands, associated with all vascular bundles; abaxial scleren- chyma as strands or small girders; bulliform cells sometimes present Distribution and habitat. This genus of small- statured grasses is typical of the winter-rainfall area of southern Africa. The annuals in the genus are mostly localized along the coastal platform of the western and northern Cape, on coastal sands, limestone, granite, or less commonly shale. Several species of Tribolium extend in the semi-arid Karoo summer rainfall area, where they are generally associated with the cooler, higher mountains. Discussion. Tribolium is clearly a member of the Rytidosperma clade by the punctate hilum and the habit as small herbaceous tufts (Verboom et al., 2006). The genus has a number of attributes, none of which are found in all of the species, which are rare or unique in the danthonioid grasses. These include stolons, by which the plants spread to form extensive clones. These stolons are often clearly visible on herbarium specimens. There are often tuberculate hairs on »" n with these often visible as rw a hispid appearance. These may also be found on the leaves. The lemma lobes are often fused to the central awn, resulting in an acute or acuminate lemma. The central awn is often not geniculate, but a simple straight structure, and usually associated with the acute lemmas. Finally, the inflorescence is often condensed, and in the two species of section Uniolae, the inflorescence is a spicate, secund structure. To accommodate the variation in the genus, we recognize sections. XVIa. Tribolium Desv. sect. Tribolium. This section includes plants with hispid glumes, often with large cushion-based hairs. Included species. Only five species are included in section Tribolium; these were all revised critically by Linder and Davidse (1997) and studied cytologically and embryologically by Visser and Spies (1994a, b, c, d, e). l. Tribolium ciliare (Stapf) Renvoize, Kew Bull. 40: 799. 1985. 2. Tribolium echinatum (Thunb.) Renvoize, Kew Bull. 40: 798. 1985 . Tribolium € (Thunb.) Desv., Opusc. Sci. Phys. Nat. 64. 183 Tribolium pusillum (Nees) H. P. Linder & Davidse, Bot. A e Syst. 119: 295. 1997. 5. Tribolium utriculosum (Nees) Renvoize, Kew Bull. 40: 798. 1985. XVIb. Tribolium Desv. sect. Acutiflorae N. C. Visser & Spies ex H. P. Linder & Davidse, Bot. Jahrb.. 119: 477. 1997. TYPE: Tribolium acuti- florum (Nees) Renvoize (= Brizopyrum acuti- florum Nees). Plants with stolons characterize section Acuti/ within the genus. rae Included species. The seven species in this section were previously described in or assigned to either Tribolium, Schismus, or Karroochloa. These were all taxonomically and nomenclaturally revised by Conert and Tiirpe (1969) or Linder and Davidse (1997). Tribolium acutiflorum (Nees) Renvoize, Kew Bull. 40; 798. 1985. 2. Tribolium curvum (Nees) Verboom & H. P. Linder, comb. nov. Basionym: Danthonia curva Nees, Fl. Afr. Austral. Hl. 328. 1841. Karro- ochloa curva (Nees) Conert & Tiirpe, Sencken- Annals of the Missouri Botanical Garden berg. Biol. 50: 295. 1969. TYPE: [South Africa.] "Uitenhaag, Zwartkopsrivier, Thal und angren- zende Hügel von Villa Paul Maré bis Uitenhaag, 50-500 ft. (loc 2),” Nov., C. F. Ecklon 4529b (lectotype, designated by Conert & Tiirpe [1969: 298], HBG!; isotypes, S!, Z!, ZT!). Danthonia bachmannii Hack., Bull. Herb. Boissier 3: 385. 1895. TYPE: South Africa. Cape Province: Malmesbury division, near Hopefield, Sep. 1885, F. E. Bachmann 1018 (holotype, Z!; isotypes, B not seen, B fragm. at FR!, K!). Tribolium obliterum (Hemsl.) Renvoize, Kew Bull. 40: 798. 1985. 4. Tribolium Bull. 40: 799. 1985. 5. Tribolium pleuropogon (Stapf) Verboom & H. P. Linder, comb. nov. Basionym: Schismus pleuropogon Stapf, Bull. Misc. Inform. Kew 1916: 234. 1916. TYPE: South Africa. Damp places near Riversdale, s.d., R. Schlechter 1759 (holotype, K not seen; isotypes, GRA!, Z!). 6. Tribolium purpureum (L. f.) Verboom & H. P. Linder, comb. nov. Basionym: Avena purpurea L. f.. Suppl. Pl. 112. 1781. Danthonia purpurea (Thunb.) P. Beauv., Ess. Agrostogr. 160. 1812. Karroochloa purpurea (L. f.) Conert & Türpe, Senckenberg. Biol. 50: 303. 1969. TYPE: South Africa. sd, © P Thunberg (holotype, UPS 2620!; isotype, S!). Conert and Tiirpe (1969) indicate that the origin of the type collection was erroneously attributed to Martinique, West Indies, by Linnaeus fil. As already noted by Willdenow (1797: 450), the place of origin was the Cape of Good Hope in South Africa. i (Nees) Renvoize, Kew T. Tribolium tenellum (Nees) Verboom & Hr Linder, comb. nov. Basionym: Danthonia tenella Nees, Fl. Afr. Austral. Ill. berg. Biol. 50: 308. 1969. TYPE: South Africa, “inter Buffelrivier (Koussie) flumen et Zilverfon- tein in elice ab aquis relicta inter montium," 2000 ft, Aug, J. F. Drége s.n. (holotype, B not seen; isotypes, HBC!, Ss». XVIe. Tribolium Desv. sect. Uniolae N. C. Visser & Spies ex H. P. Linder & Davidse, Bot. Jahrb. 119: 471. 1997. TYPE: Tribolium uniolae (L. f.) Renvoize. Tribolium sect. Uniolae is characterized with secund, spicate inflorescences by plants Included species. Only two species are included in this section, and these were also discussed by Linder and Davidse (1997) and studied cytologically and embryologically by Visser and Spies (1994, b, c, d, e) l. Tribolium brachystachyum (Nees) Renvoize, . 1985. Kew Bull. 40: 798. 1 2. Tribolium uniolae (L. f.) Renvoize, Kew Bull. 40: 797. 1985. XVII. Rytidosperma Steud., Syn. Pl. Glumac. 1: 425. 1854. TYPE: Rytidosperma lechleri Steud. Figure 19. Danthonia sect. Eudanthonia Benth., Fl. Austral. 7: 591, 592. 1878, nom. inval. IT. Notodanthonia Zotov, New Zealand J. Bot. 1: 104. 1963 E: Notodanthonia (Raoul) Zotov = Danthonia unarede Raoul). Erythranthera Zotov, New Zealand J. Bot. 1: 124. 1963. TYPE: Erythra australis (Petrie) Zotov (= Triodia australis Petrie). hera Zotov, New Zealand J. Bot. 1: 125. 1963. TYPE: Pyrrhanthera exigua (Kirk) Zotov (= Triodi irk exigua Kirk). Joycea H. P. Linder, Telopea 6: 611. 1996. TYPE: Joycea pallida (R. Br.) H. P. Linder (= Danthonia pallida R. Br.). Thonandia H. P. Linder, Telopea 6: 612. 1996. TYPE: Thonandia longifolia (R. Br.) H. P. Linder (= Dan- thonia longifolia R. Br.), nom. superfl. pro Notodantho- ia Zoto nia Zotov. Austrodanthonia H. P. Linder, Telopea 7: 269. 1997. TYPE: Austrodanthonia caespitosa (Gaudich.) H. P. Linder (= Danthonia caespitosa Gaudich.). Plants perennial, tufted, cushion-forming, mat- forming, or loosely to densely caespitose, or as solitary , shoots from long spreading rhizomes; culms to 1.6 m tall, but most species substantially less than 1 m tall; innovation buds intravaginal or extravaginal, stolons rarely present. Ligule ciliate; leaf blades orthophyl- lous or sclerophyllous, persistent or rarely disarticu- lating from the sheaths, glabrous or pilose, rarely villous, sometimes with a web of interlocking hairs adaxially above the ligule. Inflorescences usually Paniculate, rarely racemose or spicate, contracted (mostly) or expanded; florets chasmogamous or clei us, some species have both. Spikelets with 2 to 7 florets; glumes shorter to usually longer than the florets, with 1 to 13 veins, without tubercle- based hairs, 1.3-23 mm; callus blunt, villous, shorter than to much longer than the rachilla internode; lemmas with 5 to 9 veins; lemma dorsal indumentum rarely absent, more commonly scattered over the lemma back, or organized into 2 horizontal rows of Volume 97, Number 3 2010 Linder et Classification of Danthonioideae 357 Figure 19. Rytidosperma caespitosum. —A. Spikelet. —B. Lemma back. —C. Palea. Drawn by Jasmin Baumann from Whibley 2707. tufts, which can be variously complete; lemma apex rarely acute, tapering into the central awn, more often lobed, the lobes shorter than to longer than the lemma body, + acute, generally tapering into setae; lemma central awns generally geniculate, the column cork- serewed, the apical portion straight; paleae broadly obovate to linear, shorter to longer than the lemma, apically rounded to bilobed, the keels scabrid, the area between the keels and the palea flaps glabrous or villous; lodicules cuneate or rhomboid, generally with bristles and microhairs; ovaries glabrous. Caryopsis lorate, elliptical, or obovate, the wall rarely separate from the seed; embryo 1/3 to 2/3 and the punctiform or elliptical hilum 1/10 to 1/3 the caryopsis length. Cytology. 24, 48, 72, 96, 120, 156 (Calder, 1937; a 1959; Brock & Brown, 1961; Borgmann, 1964; Connor & Dawson, 1993; Baeza, 1996b; Murray et al., 2005). Anatomy. Leaves generally orthophyllous or rare- ly sclerophyllous; adaxially scarcely ribbed, rarely with massive ribs; adaxial sclerenchyma as small strands, girders, or inversely anchor-shaped girders; abaxial sclerenchyma as small strands to massive girders, rarely forming a continuous subepidermal layer; bulliform cells generally present. Distribution and habitat. Rytidosperma is very widespread and indeed common in temperate and cool-temperate habitats in New Guinea, Australia, New Zealand, and South America. On the Australian Tablelands and in the Murrumbidgee—Murray Basin, this genus can dominate the grassland flora. Species are found over a vie habisst na "m meen and/or rocky t boggy $i i y A £ snaue In Oper habitats (but never in tropical habitats); and tides the arid margins of Central Australia to the wet grasslands of New Zealand’s Westland. Discussion. Typically, the species of Rytidosperma = punctiform hila and are “small, herbaceous, and še xa tal y lp -— D in the New ‘Gam alpine lora (e.g., R. oreoboloides (F. Muell.) H. P. Linder), or are somewhat usi etti y a (e. E LE putos! (R. M ) A. e by means a pt m (R. nie (Kirk) H. F. Linder). Most species have a lemma indumentum ed basically in two parallel rows of tufts, without or rarely with scattered hairs between the rows. This indument pattern can be variously reduced, until in ce In — species, the tufted petes distributed on ine ana back. This mte means can "be diagnosed by patterns d jawa indumepban against, e.g., Tribolium or Schismus, although the molecular signal is strong. Included species. Here we include 73 species in the genus Rytidosperma. This is a much broader circumscription of the genus than that used by Linder and Verboom (1996). It is similar to the circumscrip- tion used by Veldkamp (1980) and Connor and Edgar (1979), but the interpretation of Clayton and Renvoize (1986) was much wider, including the African species as well. Our species treatment follows the three most Annals of the Missouri Botanical Garden Ausyasdkuaukanik, Joycea, Rytidosperma, and Noto- danthonia, sensu Linder [2005]), from New Zealand (including rogó and Rytidosperma [Edgar & Connor, 2000], and also from South America under R (Baeza, 1996a). However, there is not yet a global revision of the entire genus. 1. Rytidosperma acerosum O ja & Edgar, New Zealand J. Bot. 17: 33 2. Rytidosperma alpicola (Vickery) Connor & Edgar, New Zealand J. Bot. 17: 331. 1979. 3. Rytidosperma auriculatum (J. M. Black) Connor & Edgar, New Zealand J. Bot. 17: 322. 1979. 4. Rytidosperma australe (Petrie) Clayton & Renvoize ex Connor & Edgar, New Zealand J. Bot. 25: 166. 1987 5. Rytidospe (Zotov) Connor & Edgar, New Zealand J. Bot. 17: 324. 1979. 6. Rytidosperma bipartitum (Kunth A. M. Humphreys & H. P. Linder, comb. nov. Basionym: Avena bipartita Link, Hort. Berol. (Link) 1: 113. 1827. Austrodanthonia bipartita (Link) H. P. Linder, Telopea 7: 270. 1997. Devthánia linkii Kunth, Enum. Pl. (Kunth) 1: 315. 1833, nom. superfl. C EM linkii D D & Edgar, N 17: 332. 1979, nom. Notodanthonia linkii ab Veldkamp, Taxon 29: 296, , nom. illeg. TYPE: Australia. NSW, 9 mi. [14.4 km]. WNW of Newcastle NSW, 27 : b Story 7220 (neotype, designated here, CANB!). The original type was presumably at B, but has not been found despite repeated searches by several persons. Presumably, it was destroyed during World War II. In order to prevent any confusion, a suitable neotype is selected. + um (Jansen) Veld- Rytidosperma bonthainie kamp, Reinwardtia 12: 139. 2004 8. Rytidosperma buchananii (Hook. f.) Connor & Edgar, New Zealand J. Bot. 17: 320. 1 1979. 9. Rytidosperma e aespitosum (Gaudich.) e & Edgar, New Zealand J. Bot. 17: 325. 1979. 10. Rytidosperma «c i (F. 11. Rytidosperma clavatum (Zotov) Connor & Edgar, New Zealand J. Bot. 17: 326. 1979. 12. Rytidosperma clelandii (Vickery) Connor & Edgar, New Zealand J. Bot. 17: 332. 1979. 13. Rytidospe orinum Connor & Edgar, New Zealand J. i 17: 317. 1979. 14. Rytidosperma eraigii (Veldkamp) H. P. Lin- der, Telopea 6: 613. 1996 15. Rytidosperma dendeniwae (Veldkamp) H. P. Linder, Telopea 6: 613. 1996 16. Rytidosperma diemenicum (D. I. Morris) A. M. Humphreys & H. P. Linder, comb. nov. Basionym: Danthonia diemenica D. I. Morris, Muellera 7: 153. 1990. Notodanthonia diemenica (D. I. Morris) H. P. Linder, Telopea 6: 616. 1996. Austrodanthonia diemenica (D. I. Morris) H. P. n Mri 7: 271. 1997. TYPE: Australia. Tas a: Ouse River, Wild Dog Plains, s.d., A. Haast 1292 (holotype, HO 65782!). 17. Rytidosperma dimidiatum (Vickery) Connor & Edgar, New Zealand J. Bot. 17: 332. 1979. 18. Rytidosperma duttonianum (Cashmore) Con- nor & Edgar, New Zealand J. Bot. 17: 332. 1979. 19. Rytidosperma erianthum (Lindl.) Connor & Edgar, New Zealand J. Bot. 17: 323. 1979. 20. Rytidosperma exiguum (Kirk) H. P. Linder, Telopea 6: 614. 1996 21. Rytidosperma fortunae-hibern ae (Renvoize) Connor & Edgar, New Zealand J. ped 17: 332 1979. 22. Rytidosperma fulvum (Vickery) A. M. Hum- phreys & H. P. Linder, comb. nov. Basionym: Danthonia linkii Kunth var. fulva Vickery, Contr. New South Wales Natl. Herb. 1: 50. ytidosperma linkii var. Te (Vickery) ‘Console & Edgar, New Zealand J. Bot. 17: 332. 1979. Notodanthonia bipartita (Link) Veldkamp var. fulva (Vickery) Veldkamp, Taxon 29: 296. 1980. Notodanthonia fulva (Vickery) H. P. Linder, Telopea 6: 616. 1996. Austrodanthonia fulva (Vickery) H. P. Linder. Telopea 7: 271. 1997. TYPE: Australia. New South Wales: Flemington, 31 Mar. 1929, G. B. Vickery — NSW 1573!; isotypes, K not seen, L not seen 23. Rytidosperma geniculatum (J. M. Black) Connor & Edgar New Zealand J. Bot. 17: 323. Volume 97, Number 3 Linder et al. 359 2010 Classification of Danthonioideae 24. rma gracile (Hook. f.) Connor & 42. Rytid rma nudum (Hook. f.) Connor & Rytidos Edgar, New Zes Zealand J. Bot. 17: 330. 1979. Rytidosperma horrens Connor & Molloy, New Zealand J. Bot. 43: 726. 2005. Rytidosperma indutum (Vickery) Connor & Edgar, New Zealand J. Bot. 17: 332. 1979. . Rytidosperma javanicum — ex em H. P. Linder, Telopea 6: 614. 1 Rytidos laeve (Vickery) Connor & Edgar, Now Zn Zealand J. Bot. 17: 325. 1979. Rytidosperma lechleri Steud., Syn. Pl. Glu- mac. 1: 425. 1854 Rytidosperma lepidopodum (N. G. Walsh) A. M. Humphreys & H. P. Linder, comb. nov. Basionym: Danthonia lepidopoda N. G. Walsh, Muellera 7: 384. 1991. Joycea lepidopoda (N. G. Walsh) H. P. Linder, Telopea 6: 612. 1996. TYPE: Australia. Victoria: Bullens Land, Court- neys Rd., N of Ash Reserve, 15 Jan. 1987, N. G. Walsh 1709 (holotype, MEL!; isotypes, BRI!, NSW). Rytidosperma longifolium (R. Br.) Connor & Edgar, New Zealand J. Bot. 17: 332. 1979. - Rytidosperma maculatum (Zotov) Connor & Edgar, New Zealand J. Bot. 17: 320. 1979. Rytidosperma mamberamense (Jansen) Con- nor & Edgar, New Zealand J. Bot. 17: 332. 1979. Rytidosperma merum Connor & Edgar, New Zealand J. Bot. 17: 328. 1979. Rytidosperma monticola (Vickery) Connor & Edgar, New Zealand J. Bot. 17: 332. 1979. Rytidosperma montis-wilhelmii (Veldkamp & Fortuin) H. P. Linder, Telopea 6: 614. 1996. R perma nardifolium (Veldkamp) H. P. Linder, Telopea 6: 614. 1 Rytidosperma nigricans (Petrie) Connor & Edgar, New Zealand J. Bot. 17: 331. 1979. Rytidosperma nitens (D. I. Morris) H. P. Linder, Telopea 6: 614. 1996. a mivicola (Vickery) Connor & Edgar, New i edan 1, Bot. 17: 332. 1979. Rytidosperma nudiflorum (P. F. Morris) Connor & Edgar, New Zealand J. Bot. 17: 332. 1979. (H ait “New Ze: Zealand J. Bot. 17: 322. 1979. Rytidosperma occidentale (Vickery) Connor & Edgar, New Zealand J. Bot. 17: 332. 1979 Rytidosperma oreoboloides (F. Muell.) H. P. Linder, Telopea 6: 614. 1996. Rytidospe H. E Linder & N. G. Walsh, Mai 8: 283. 199 46. Ryti rma pallidum (R. Br.) A. M. Hum- ur: $1 H. P. Linder, comb. nov. Basionym: ia pallida R. Br. Prodr. Fl. Nov Holland. 177. 1810. Avena brownii Spreng., Syst. Veg., ed. 16 (Sprengel) 1: 336. 1825. Noto- danthonia pallida (R. Br.) Vamo. Taxon 29: 297. 1980. Danthonia penicillata (Labill.) P. Beauv. var. pallida (R. Br.) Rodway, Tasman. Fl. 267. 1903. Chionochloa pallida (R. Br.) S. W. L. Jacobs, Taxon 31: 742. 1982. Joycea pallida (R. Br.) H. P. Linder, Telopea 6: 611. 1996. TYPE: Australia. New South Wales: Port Jackson, s.d., R. Brown 6232 (holotype, BM not seen; isotype, K not seen, K fragm. at PERTH!). 43. 44. 45. Rytidospe ea ay pad C. M. Baeza, Gayana, Bot. 47: 83-84. 1 Rytidosperma pauciflorum (R. Br.) Connor & Edgar, New Zealand J. Bot. 17: 332. 1979. Rytidosperma penicillatum (Labill.) Connor & Edgar, New Zealand J. Bot. 17: 327. 1979. Rytidosperma petrosum Connor & Edgar, New Zealand J. Bot. 17: 317. 1979. 50. 51. Rytidosperma pictum (Nees & Meyen) Nicora, Darwiniana 18: 91. 1973. 5la. Rytidosperma pictum (Nees & Meyen) Ni- cora var. pictum. 51b. iptum pictum (Nees & Meyen) Nicora var. bimucronatum Nicora, Darwiniana e ^2: 91. 1973. 52. R perma pilosum (R. Br.) Connor & Edgar, New Zealand J Bot. 17: 326. 1979. 53. Rytidosperma popinensis (D. I. Morris) A. M. " & H. P. Linder, comb. nov. Basio- ym: Danthonia popinensis D. I. Morris, Muel- leria 7: 157. 1989. Notodanthonia popinensis (D. L Morris) H. P. Linder, Telopea 6: 616. 1996. Austrodanthonia popinensis (D. I. Morris) H. P. Linder, Telopea 7: 273. 1997. TYPE: Australia. Tasmania: 0.5 km N of Kempton, 16 Jan. 1987, Annals of the Missouri Botanical Garden D. Morris 8556 (holotype, HO 92651!; a AD!, NSW)). 54. Rytidosperma pulehrum (Zotov) ved & Edgar, New Zealand J. Bot. 17: 321. 1 55. Rytidosperma pumilum (Kirk) Connor & Edgar, New Zealand J. Bot. 25: 166. 1987 56. Rytidosperma quirihuense C. M. Baeza, Novon 12: 31. 2002. 57. Rytidosperma racemosum (R. Br.) Connor & Edgar, New Zealand J. Bot. 17: 327. 1979. 57a. Rytidosperma racemosum (R. Br. ) Connor & gar var. racemosum. 57b. Rytidosperma racemosum (R. Br.) Connor & Edgar var. obtusatum (Benth.) Connor & Edgar, New Zealand J. Bot. 17: 332. 1979. ytidosperma remotum (D. I. Morris) A. M. Humphreys & H. P. Linder, comb. nov. Basionym: Dant: . Morris, E nia remota (D. L Morris) H. P. P. Linder, Telopea 6: 617. 1996. A mota (D. I. Morris) H. P. Linder, bem T 273. 1997. TYPE: Australia. Tasmania: summit of Hibbs Pyramid, 3 Feb. 1980, A. M. Buchanan 2878 (holotype, HO 91392)). 59. Rytidosperma richardsonii (Cas more) Con- nor & Edgar, New Zealand J. Bot. 332. 1979. 60. Rytidosperma semiannulare (Labill.) Connor & Edgar, New Zealand J. Bot. 17: 332. 1979. 61. Rytidosperma setaceum (R. Br) Connor & Edgar, New Zealand J. Bot. 17: 332. 1979. 62. Rytidosperma setifolium (Hook. f.) Connor & Edgar, New Zealand J. Bot. 17: 316. 1979. 63. Rytidosperma sorianoi Nicora, Darwiniana 18: 89. 1973. 64. Rytidosperma telmati telmaticum Connor & Molloy, New Zealand J. Bot. 43: 721. 2005. 65. Rytidosperma tenue So Cone & Edgar, New Zealand J. Bot. 17: 3: 66. Rytidosperma tenuius chi O. E. Erikss., A. Hansen € Fl. Macaronesia Check]. Vase. Pl. pt. 1, ed. 2, 93. 1979. 67. thomsonii (Buchanan) Connor & Edgar, New Zealand J. Bot. 17: 322. 1979. 68. Rytidosperma unarede (Raoul) um & Edgar, New Zealand J. Bot. 17: 328. 1979. 69. Rytidosperma vestitum (Pilg.) Connor & Edgar, New Zealand J. Bot. 17: 332. 1979. 70. Rytidosperma vickeryae M. Gray & H. P. Linder, Austral. Syst. Bot. E. 244, 1999. 71. Rytidosperma violaceum (E. Desv.) Nicora, Darwiniana 18: 91. 1973 72. Rytidosperma virescens (E. Desv.) Nicora, Darwiniana 18: 93. 197 72a. Rytidosperma virescens (E. Desv.) Nicora var. virescens. 72b. Rytidosperma virescens (E. Desv.) Nicora var. parvispiculum Nicora, Darwiniana 18(1, 2): 95. 1973. 72c. rium virescens (E. Desv.) 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Mucina js M. C. Rutherford = The Vegetation of South ca, Lesotho South African National lionis Institute, [wenn Reeder 1977. Ch numbers in western d i Bot. 64: 102-110. Reimer, E. & J. H. Cota-Sanchez. 2007. An SEM survey of i thonioid grasses (Poaceae: oekologischer Dicen Oesterr. Bot. Z. 111: 193-207. NOMEN A. P. € N. S. Probatova. 1978. Chromosome rs of some ginem eggs of the USSR flora Il. Bot. Zhurn. S.S.S.R. 63: 1247-1 Spies, J. J. & H. du Plessis. 1986. Chromosome studies on African plants. 1 16: 8 & 1988. Chromosome gales on African plants. 6. Bothalia 18: 111-114. & R.R Roodt. 2001. The basic chromosome number of J: sk l. 91. T4I 146. LH du Plessis, N. P. Barker & S. M. C. van Wyk. s Chaetobromus 990. Cytogenetic studies in the genus c. Arundineae). Genome 33: 646-058. HE s L F. po & H. = — 1994. Cytogeneti Pentaschistis aids and s potula TL ae: vae neae). Pp. 373-383 in J. H. Seyani & A. C. Chikuni (editors), Proceedings a the XII Plenary ire of AETFA . Malawi, 2-11 April 1991. Herbarium ind Botanie Garden of M Sprague, T. A. 1922. Plant nomenclature. À e J. Bot. 60: — . 1899. Graminae. Pp. dio o in arm T. Thiselton- Dyer, Flora — Vol. 7. Lovell Reeve, London. Stebbins, G. L. & R. M. Love. 1941. A cytological study of California forage grasses. Amer. J. Bot. 28: Steudel, E. G. 1841. Nomenclator a a A Cotta, m 1853-1854. Synopsis Plantarum Glumacearum, Vol. 1. J. B. es Stuttgart Swofford, D. L. 2002. PAUP*: Phylogenetic dap qe Tie Parsimony es other methods), Versi . Sinaue Associates, Sunderland, Massachusetts Annals of the Missouri Botanical Garden Tateoka, T. 1957. Miscellaneous papers on the d of of Poaceae. J. Jap. Bot. 32: 275-287. ————.. 1965. Chromosome numbers of some grasses from adagascar. Bot. Mag. (Tokyo) 78: 306-311. is. Pp. 171-229 in M. J. A. Ecology of Southern ca. Dr. tods N. N. 1984. Grasses ol de Soviet Union. Balkema, Rotterdam. Veldkamp, J. F. 1979. Poaceae. Pp. 1035-1224 in P. van Royen Esa The Alpine Flora of New Guinea. J. Cramer, V E Conservation of Notodanthonia Zotov (Gra- E Taxon 29: 293-298. . 1981. "Validation of Blakeochloa Veldk. (Grami- NM Taxon 30: 477-478. Verboom, G. A. & H. P. Linder. 1998. A re-evaluation of species limits - OMM ae ae Poaceae). Nordic J. Bot — N. F 0 1994. Haustorial synergids: An important character in the systematics of danthonoid (Arundinoideae: Poaceae)? Amer. J. Bot. 81: 1601-1610. — Ntsohi : Barker. Molecular phylogeny of Africa Brtidogema-alilised dánthonioid grasses rev reveals generic polyphyly and convergent evolu- tion in spikelet morphology. Taxon 55: 337-348. Visser, N. C. & J. J. AE 1994a. Cytogenetic studies in the genus Tribolium (Poac ae: Danthonieae). I. A taxonomic overview. S. African J. "Bot. 60: 127-131. . 1994b. C Cytogenetic studies in the ren (Poaceae: ; Danthonicae). genus IL A report on embryo UccCuirence of apomixis in diploid specimens. S. African J. Bot. 60: 22-26. — 1994c Cytogenetic studies in the genus Tribolium (Poaceae: Danthonieae eae). III. Section Tribolium S. African J. Bot. 60: 31-39, & —. "e uM c studies in the genus Tribolium (Poaceae: eae). IV. Section Acutiflorae, related gene s, and Secun S. African J. Bot. 60: EN — studies in the genus gerentes e Danthonieae V. Section Uniolae. S. African J. Bot. 60: um P. 1991. Vn of New Zealand. Cambridge University Press, Willdenow, C. L. 1797. Mean Plantarum, Vol. 11). 6. c. Nauk, Berlin. Zotov, V. D. 1963 Synopsis of the grass subfamil Arundinoideae in New Zealand. New Zealand E bcr 78-136. E eu LUE the simplified phylogeny. See Table 1 and Figure 2. cH not = 0. 5. Leaf lamina persistent on sheath = 0; abscising from a persistent sheath = 1; persistent sheath often soldi - 2. 6. Keels on leaf blades absent — 0; pee s simple — 1; present as with ge d keels 7. Leaf blades asymmetri ymmetric. Mu 8. Mesophyil islands of di dud cells absent — 0; pei = 1. 9. Microhairs in leaf-grooves non-overlapping = 0; over- lapping = 10. Spikelets x disriculating — TOM — 0; below = 1; above glumes 1E e of florets per RE 1 or 2 — 0; 3 or more 12. Le of Pii veins up to 9 — 0; 7 or more — L 13. Lemma indum transverse v = zd scattered tufts — 2; totally absent = 3. 14. Lemma setae inserted at the tips of a lobes = 0; in the sinus between the lemma lobes = 15. Lemma awn differentiated into a Ae get column and sine hairlike apical part — 0; not differentiated into two parts — 1. 16. Tufts of Ei hair on the palea margins absent = present = 17. Palea adig rmal — 0; inrolled — 1. 18. Lodicule idc absent — ‘0; present = 1. 19. Lodicule microhairs present = 0; absent = 1. is hilum linear = 0; punctiform = 1. 21. Leaves blades sclerophyllous = 0; orthophyllous = 1. - Generic groups recognized within the Danthonioideae. Pus are presented in this order in the paper, reflecting their current known relationships. a. Merxmuellera basal “sesi L. Merxmuellera Cone IL. Geochloa H oe er & N arker M. Copeochloa H. P. Linder & E B Barker b. Pentameris clade IV. Pentameris P. Beauv. €. Chionochloa clade V. Chionochloa Zotov Chaetobromus-Pseudopentameris clade R IX. Austroderia N. P. Barker & H. P. Linder X. Plinthanthesis Steud XI. Notoc Domin XII. Chimaerochloa H. P. Linder Danthonia DC. f. Rytidosperma clade XIV. Tenaxia N. P. Barker & H. P. Linder XV. Schismus P. Beauv. XVI. Tribolium Desy. XVII. Rytidosperma Steud. — REVISIÓN TAXONÓMICA DE LAS Nataly O’Leary,? Maria Ema Miilgura? y rrone? ESPECIES DEL GÉNERO VERBENA (VERBENACEAE). II: SERIE VERBENA’ Osvaldo Mo. RESUMEN Verbena L. (Verbenaceae) comprende 44 — de distribución a v. americana, con dos — ies sudamericanas distribuidas en áreas cálido-templadas. de ambos hemi rios: V. officinalis L. y supina L. Las espec Verbena ser. Bey ido Skaner e Verbena respectivamente. al el I tratamiento se describen los taxones de Verbena ser. Verbena; esta serie copiado 26 especies divididas en Verbena, Has detalladas de todos los taxones, c poo para ninaka i od una sinonimia (véase Medos 3), y se discuten relaciones entre taxones gracilescens (Cham.) Herter var. swifiiana or N. O'Leary y V. simplex Le V. brac nueve d y- e Lag. & domingens , V. officinalis Small & e Heller y Y. urticifolia | L. var. simplex Farw Link, V. roemeriana ABSTRACT Verbena L. (Verbenaceae) is represented by 44 species, mainl tatae y Bracteosae. . Se proporcionan descripci iones veil oaa con 56 nuevos sinónimos afines. Se NA dos nuevas combinaciones: Verbena ar. orcuttiana (L. M. Perry) N. et teosa Michx. var. € A. Gray, V. carolina L., V. ar. gracilescens s: D ee L., V. hirsuta M. Martens & Gales V. riparia s seis neotipificaciones: V. ehrenbergiana Schauer, V. lasiostachys Scheele, V. simplex Lehm., V. qune E y V. xut hm. y distributed in America, with two species distributed in regions from both era V. officinalis L. and y supina L. South American species are pot temperate different from North American species erbena, respectively. In = TTA aten, Verbena ser. placed in three Veris taxon, as well as eee a Rina 3), and diseussions of ‘elation ips between closely related taxa. Two new “combin ations swiftiana (Moldenke) N. O’Leary and V. simplex Lehm. var. orcuttiana (L. M. Perry) «1 O'Leary; nine (Cham.) H are placed in two separate series: € ser. Pachys taxa are tachyae Schauer series . This series includes 26 1 species, Verbena tae, and Bracteosae. Detailed morphological ida are given for each itl (Appendix introduc V. gracilescens Pins are v cried Y, bracteata Lag. & Rodr., V. bracteosa Michx. var. brevibracteata A. e E rr V. is var. gracilescens "m Link, words: AA America, Verbena, Verbenaceae. domi V. offici Cham., V. hastata L., V. e M. Martens & Galeotti, V. riparia ex Small $ & T Heler, d V. urticifolia L. var. simplex Farw.; and six s; neotypi . roemeriana Scheele, V. simplex Lehm., V. spuria L., and V. Y iaa Lehm. ified: Y. pra dt Schauer, V. El género Verbena L. (Verbenaceae) comprende 44 especies que crecen en áreas cálido-templadas del continente americano, con unos pocos representantes distribuidos en regiones cálido-templadas del resto el mundo Históricamente el género Verbena se ha d en dos a ocho secciones, series o grupos i principalmente sobre la base de caracteres seb: gicos de las inflorescencias, de las hojas y del tipo de pubescencia, caracteres anatómicos y de distribución (Schauer, 1847; Briquet, 1895; Small, 1933; Tron- coso, 1974; Sanders, 2001). Actualmente dentro de Verbena se reconocen dos series: la serie Pachystachyae Schauer (O'Leary et al., 2007) y la serie Verbena, aquí tratada. La serie Pachystachyae incluye 18 especies agrupadas en dos subseries: Pachystachyae y Pseudoracemosae N. O'Leary (O'Leary et al., 2007). Sanders (2001) sugirió que esta serie seria monofilética y estaria basada en caracteres apomórficos como flores y frutos densa- = 2I 1 (W), Mark Spencer (BM), dor Olof P Willemse (L), entre otros. También se agradece a Vl al CONICET por la Bec de Botánica Darwinion, noleary@darwin.edu.ar. doi: 10.3417/2007070 Debra Toek (CAS), Marina Galimberti (TO), Jean Ya ke (R. D ás y Francisco Rojas por las excelentes láminas, y por último llevar a cabo esta Ann. Missouri Bor. Garp. 97: 365-424. PUBLISHED ON 10 OCTOBER 2010. Annals of the Missouri Botanical Garden L d fl breves, cilíndricas compactas, muchas veces agrupadas en panículas ramificadas. En el presente trabajo se aborda el estudio de las especies de Verbena ser. Verbena incluyendo descrip- ciones, ilustraciones y claves para la identificación de todos los taxones que integran la misma, completán- dose de esta manera, la revisión taxonómica del género Verbena, iniciada anteriormente con la serie Pachystachyae (O'Leary et al., 2007). MATERIALES Y MÉTODOS Se estudiaron aproximadamente 1470 ejemplares, depositados en los herbarios ARIZ, BA, BAF, C, CAS, CORD, CTES, IEB, K, LP, MO, NY, P, SI y (abreviaturas según Holmgren et al., 1990). Las n de las especies y variedades aceptadas y de los ejemplares examinados se proveen en los Apéndices l y 2. Para la descripción morfológica se siguió la terminología propuesta por Lindley (1951), Hickey (1974: 9), Martínez et al. (1996) y Lawrence (1951: figs. 308, 309). Para los estudios anatómicos se utilizó meee de beria y se e realizaron cortes a mano ggio de Argüeso (1986). TRATAMIENTO TAXONÓMICO Verbena L., Sp. Pl. 1: 18. 1753. TIPO: Verbena officinal is L. (lectotipo, designado por Britton & Brown [1913: 94]). Le Monn. ex Rozier, Intr. Obs. Phys. Hist. Nat. 1: 367. 1771. TIPO: Obletia verbenalacaea Le ozier. Billardiera Moench, Methodus: 369. 1794, nom. illeg., non Billardiera Sm., 1793, non Billardiera Vahl, 1796. : Billardiera explanat rm rums rdi ge Hist. Nat. Veg. 9: 838. TIPO: olia (Jues.) a mia Verbena onn. ex i Sei. Acad. Imp. Sci. Saint-Péters- 840. TIPO: Uwarowia chrysanthemifolia AL ian Fl. SE. U.S. [Small], ed. 1: 1011. 1903. quadrangulatus A. Heller [= Heller. anthus quadrangulatus (A. Heller) Small] rea Hierbas anuales o perennes, o sufrútices, muchas veces hemicriptófitos, de hábito erecto, decumbente a procumbente; tallos te a poligonales, a veces algo cilíndricos en la base, desde desde glabros a pu- bescentes con pelos adpresos a dn simples o glandulares; braquiblastos desarrollados opuestas decusadas, lámina lobada, partida, o sectada; márgenes muy variados generalmente serrado-dentados a irregularmente cre- nados; base sésil o peciolada; ápice agudo u obtuso; pubescencia en ambas caras pero menos densa en la cara adaxial, a veces subglabras. In, politélica formada por pleiobotrios heterotéticos, — E una florescencia principal siempre e y una zona be simp e o ramificados, sinflorescencia brac- teosa o frondosa, florescencias cilíndricas densas o e enriquecimiento con para- filiformes laxas, pedunculadas a sésiles, multifloras, flores densamente imbricadas o dispuestas laxamente, A A z^ A + Š 1 csm fl 1 Flores perfectas, en general pequeñas, sésiles, a veces sobre icelos breves, corola levemente zigomórfica, bráctea floral presente, cáliz cilíndrico-tubular, 5- angulado, con 5 dientes desiguales; corola infundibu- liforme o hipocraterimorfa, de color blanco, azul, rojo y sus diferentes gamas, con tubo cilíndrico recto o a veces algo curvado, con o sin pubescencia en la fauce y en la garganta de la misma, con 5 lóbulos poco desarrollados, desiguales; estambres 4, didínamos, subsésiles, generalmente insertos en la mitad superior el tubo corolino, filamento muy breve o ausente; anteras ovoides, dehiscencia longitudinal; ovario súpero, bicarpelar, cada carpelo bilocular con un óvulo por lóculo inserto en el borde del carpelo; estilo breve, menos de tres veces la longitud del ovario, base del estilo no ensanchada, de inserción apical, esti generalmente bilobado, con un lóbulo algo redon- deado y papiloso y el otro agudo y liso. Fruto esquizocárpico formado por rà clusas uniseminadas, ilíndricas de sección subtrígona, ápice obtuso y base no angostada, de igual longitud o algo menor que el cáliz fructífero. VERBENA SER. VERBENA L. Las especies de la serie Verbena presentan corte transversal del tallo con parénquima clorofiliano de disposición continua, generalmente no interrumpién- dose en los ángulos por la presencia de cordones de esclerénquima. La serie Verbena posee distribución más amplia que la serie Pachystachyae (O'Leary et al., 2007); todas las especies nativas de América del Norte pertenecen 4 esta serie, únicamente dos especies son nativas del Viejo Mundo, V. officinalis y V. supina L., originarias de Europa (Munir, 2002). Actualmente las especies de la serie Verbena se encuentran distribuídas en regiones cálido-templadas de todo el mundo: África, Asia, Europa, Australia y Polinesia (Munir. 2002), siendo en Norte América donde se presenta la mayor concentración de especies. A su vez, la serie Vi comprende más especies que la serie Pachystachyae. Volume 97, Number 3 O'Leary et 367 Revisión Tawa de Verbena Tabla 1. Agrupación propuesta para las 26 especies de Verbena ser. Verbena. Verbena ser. Verbena Grupo Verbena Grupo Hastatae Grupo Bracteosae V. carolina L. V. californica Moldenke V. ehrenbergiana Schauer V. gracilescens (Cham.) Herter V. halei Small V. hastata V. menthifolia Benth. V. officinalis L. V. scabra Vahl V. neomexicana (A. V. urticifolia L. V. perennis Wooton V. plicata Greene V. recta Kunth V. simplex Lehm. V. stricta Vent. V. xutha Lehm. V. caroliniana Michx. V. cloverae noe E hai Link V. macdougalii A. Heller Gray) Small V. bracteata Lag. & Rodr. V. . canescens Kunth V. demissa Moldenke V. gracilis V. supina L. siendo 26 especies en la primera y 18 especies en la segunda. Schauer (1847) divide la serie Verbena (sub. nom. serie Leptostachyae, nom. invál.; McNeill et al., 2006: Art. 22) en dos pos, segün tuvieran las hojas enteras o divididas. Small (1933) divide en tres grupos las especies de la serie Verbena, basados en la división de la lámina foliar y tipo de incisión del margen, la longitud de las brácteas florales con relación al cáliz y el hábito. Sanders (2001) sugiere que esta serie sería parafilética y la divide en cinco pos morfológicos, basados en la incisión de la lámina, el ancho y longitud de las florescencias y su disposición en inflorescencias. En el presente tratamiento se reconocen tres grupos informales dentro de la serie Verbena, basándose principalmente en la morfología de la inflorescencia y las florescencias, el hábito y la división de la lámina foliar, entre otros caracteres. Una lista completa de todas las especies de Verbena ser. Verbena tratadas en este trabajo, incluídas en los respectivos grupos informales, se resume en la abla 1. Grupo Verbena en Verbena ser. Verbena. En este grupo se incluyen ocho especies (Tabla 1). Las mismas se caracterizan por poseer florescencias filiformes, elongadas, gráciles, con frutos remotos, reunidas en parac ros o multímeros, paniculosos o no; sinflorescencia bracteosa, brácteas florales no prominentes, nunca sobrepasando en longitud al tubo — ouod amd sin pelos andulares en las p anatomía caulinar con parénquima scene de disposición continua. Small (1933) reúne en el grupo informal “Offici- nale" plantas de hábito erecto, con hojas pinnadas o bipinnadas y brácteas florales más breves que el cáliz, y ubica en este grupo los mismos taxones que aquí se tratan dentro del grupo Verbena. Sanders (2001) define el segundo y tercer grupo morfológico para agrupar aquellos taxones con florescencias filiformes reunidas en panículas desarrolladas, frutos remotos, hojas profundamente lobadas o pinnatisectas; o los mismos taxones aquí reunidos dentro del grupo Verbena más Verbena neomexicana (A. Gray Small, que aquí se trata dentro del grupo Hastatae. Grupo Hastatae en Verbena ser. Verbena. En este grupo se incluyen 13 especies (Tabla 1) con florescencias cilíndricas, elipsoidales, no filiformes, con frutos remotos o congestos, agrupadas en sinflorescencias no paniculosas constituídas por paracladios trímeros o multímeros; las brácteas florales sobrepasando en longitud al tubo corolino o no, con o sin pelos glandulares en las piezas florales; las hojas pane ser enteras o divididas. Son generalmente hierbas o sufrütices erectos. EI parénquima p €— continua excepto en ifornica Moldenke, V. Moldenke, V. Small (1933) emplea el nombre Hastatae para agrupar todas las plantas con hojas de lámina entera y n inciso-dentado; por eso incluye en el mismo a Verbena litoralis Kunth, que pertenece a la serie Pachystachyae (O'Leary et al., 2007), y también a V. urticifolia L. y V. scabra Vahl, die tratadas aquí dentro del grupo informal Verbena. Por otro lado, Annals of the Missouri Botanical Garden Sanders (2001) trata los taxones aquí reunidos dentro z margen serrado o biserrado, ovadas, elípticas u obovadas, profundamente trilobadas y florescencias “tipo Plantago”, a veces solitarias. Grupo Bracteosae en Verbena ser. Verbena. En este € se incluyen cinco especies (Tabla 1), siendo las mas hierbas o sufrútices postrados o a veces semierectos con tallos ascendentes hacia el ápice, generalmente rastreras, menores de 60 cm de altura. florescencias cilíndricas ^ elipsoidales, i paniculosas, frondosas; brácteas florales conspicuas o no; hojas predominantemente pinnatipartidas, pinnatilobadas, tripartidas o trilobadas, presencia de un pecíolo ensanchado hacia la base. Verbena demissa Moldenke se incluye en este grupo únicamente por su hábito. Anatomía caulinar con parénquima clorofi- liano de disposición continua. El nombre Bracteosae fue utilizado por Small en 1933 para agrupar plantas de hábito postrado o decumbente, hojas pinnadas o bipinnadas y flores con brácteas €— más largas que el ces Sanders (2001) t rata lo , dentro del grupo mrkar número 5, que reúne be plenas de hojas inciso-lobadas, tallos decumbentes, florescen- cias solitarias con brácteas florales que exceden en longitud al cáliz; incluye en el mismo a Verbena carolina L. que aquí se trata bajo el grupo Verbena. CLAVE PARA iro GRUPOS INFORMALES DENTRO DE VERBENA SER. VERB, l. Florescencias filiformes, elongadas, graciles, con frutos remotos; sinflorescencia paniculosa o bracteosa; brácteas florales > no prominentes, nunca sobrepasando en longitud al tubo tubo corolino; sin — en las piezas florales (excepto en V. QNUM) ees cce Re or ee Grupo Verbena 1”. Florescencias cilíndricas m nunca fili- formes, breves o elongadas, n unca gráciles, con frutos congestos o remotos; sinflorescencia no panic prominentes sobrepasando en longitud al tubo Pic no noi eon o sin pelos glandulares en las Bids o sufrütices Postrados, generalmente rastreras, a veces dentes hacia el ápice he = hojas no enteras (excepto en V. demis- MR ete ei xac eiu LV I. 2”. Hierbas o sufrútices erectos, a edd algo decumbentes en la base luego ramas siempre erectas, hasta de 13 m de luca rne enteras o divididas ..... Grupo Hastatae CLAVE PARA LAS ESPECIES DE VERBENA SER. VERBENA 1. r... idee elongadas, gráciles, con frutos rı sinflorescencia paniculosa o no, bracteosa; 1 brácte eas florales no promi- nentes. O A corolino; sin pelos "e en las piezas florales aem en V. officinalis) ......... 2 E. Florescencias cilíndricas elipsoidales, nunca filiformes, breves o elongadas, nunca gráciles, 2(1). Plantas con abundantes pelos dim dulares en los pedünculos de las Torsceneins 2 s p su Hole. 0 m. V. officinalis 2 Plantas sin pelos glandulares, en pre- BONES ESCHSÜB. io ii ar AL ME 3(2. Plantas con todas las hojas de lámina entera, si dividida, únicamente las basales ........... a. Plantas con hojas de lámina dividida, si enteras, goce e asales 2... 227 4(3. Diente pa 1 Fingern n de color blanco, a veces E OON aka ceu I eee 25. V. urticifolia 4. es del cáliz fructífero io en j ión, flores de color violeta, lila, celeste o a veces blanco ................ 5 3(4. Superficie estigmática subtendida por una prolongación esté = plantas subglabras a híspidas, hojas generalmente sésiles a sub- sésiles a veces con un pecíolo breve, pine mente hasta de Don. u ulus da sia Stee 6 s Superficie estigmática m entre dos pro- longaciones estériles 2 n ilo a lóbulos obtusos; plantas con urine escabrosa, hojas con patie de 14 O a sona Y. scabra 6(5). Hojas con pubescencia variable, la ‘ni NONO OMM icerum EL aka 4. V. carolina 6’. "ond Ee la lámina entera o A en uc Bases A 9. V. gracile: 7(3). my siempre de lámina trilobada y margen entero a ligeramente inciso-serrado o dentado, y nunca profundamente AR. 8. V. ehrenbergiana lámina partida o sectada, y margen pinnado o 8(7. Hojas morfológicamente variables, las basales i ámi n pubérulas hacia el iie con pelos adpresos breves; tubo corolino de 0.4-0.65 em ....- 8. Hojas morfolégicamente no variables, de lám- ina tripartida, trisecta o pinnatipartida, margen irregularmente inciso-dentado; pues. ee pu- estrigosas; tubo corolino iur a 0.45 cm Ore, 15. V. ^ ini X1). ^ Hierbas o sufritices postrados, generalmente ~ Tastreras, tallos a veces semierectas Volume 97, Number 3 O'Leary et al. 369 2010 Revisión Taxonómica de Verbena ascendentes hacia el ápice, menores de 60 cm © canescente, con pelos glandulares abun- de altura; hojas no enteras (excepto mi E... O .. ..... ............... 20 SENE ee cee es ee 10 20(19) Hojas elí, i cias de y. Hierbas o sufrátices erectos, a veces con tallos 25-30(—40) X 0.6-0.8 cm, brácteas florales algo decumbentes en la base luego con ramas de longitud similar al cáliz; encia de hasta 1.8 m de altura; hoj , o glar escasa en las piezas enteren a dividida e rl Bes 0 ma Plantas con hojas ener ........ 7. V. demissa 20' Hojas ov: ; florescencias de 10-20 tas con noente _........... X 0.8-1 cm, ocioso florales siempre notor- E ee florescencias mayores de 1 em lat. repasando al cáliz en longi trilobadas divaricadas en pubescencia glandular en las piezas flor- bito. florales muy prominentes, ca. 0.7 p m S... uere 14. V. macdougalii recurvá y acrescentes en 21(14). D PAN —— eras llegando hasta 1.2 cem ......... V. bracteata eces pinnatilobadas ........ V. perennis 11”. Plantas con florescencias de 0.4-0.8 cm lat. y 21. Hojas de lámina desarrollada ............ 22 hojas pinnatilobadas, pinnatipartidas a - 22(21). Hojas de lámina entera, elíptica o dividida, tisectas o bipinnatipartidas; brácteas florales A EO 1- prominentes o no, pero siempre menores 3 em, ápice agudo o 6. V. neomexica 0.7 cm; inchso folificess 2... ............ 12 22. Hojas de lámina t trip szl hacia la 12(11). Brácteas florales de 0.1-0.2 cm, menores que — de3-12 X 1 E dee l cáliz; besconera veriable desde —— o ubobESD ........................ 23 híspidas, a .supina 23(22). Tallos con pubescencia adpresa o estrigosa 12’. Brácteas florales de longitud variable, siempre ; abundante, sin pelos gland: - - - 26. V. xutha mayores o iguales que el cáliz; plantas de 23'. Tallos i Mida e hinama ia hirsuto-canescente a subglabras, densa, con algunos pelos glandulares ....... 24 hana de lmm ....... .-.... ..... 13 24(23) Hi robustas con tallos y hojas con 13(12). cundi florales foliosas hacia la base del A ia hí ~ frut raquis; hojas pinnatipartidas a pinnatisectas, a te imbricados; jas con venación no pro- libel, nciso-dentado .... truyente abaxialmente ...... 13. V. lasiostachys o e 24 es con tallos y hojas con pubescencia 13’. Brácteas florales no T hojas pinnati hirsuta; flores densamente imbricadas badas, margen con 2 a 5 —— x appen sis y frutos remotos; venación bay es a R eno V. canescens protruyente abaxialmente ........-.--..- 25 14(9. Hojas d is 25(24). Brá les d ] longitud reducida; sinflorescencias bracteosas o frondo- que el cáliz, no acrescentes en la madures, sas, con o sin pelos glandulares en las piezas vena media no evi e ° ie NÉ Leod rop bts a ek d is 25 14'. Hojas predominantemente divididas, pinnati- al cáliz, acrescentes en la madurez, m vena partidas, pinnatilobadas o tripartidas das, triloba- medis POS ¿eones o o ar 9. V. plicata hacia la base; sinflorescencias e generalmente con glandulares en las . Verbena bracteata Lag. € Rodr., Anales Ci. 15(14) ne florales (excepto en V. xutha) pesse y 21 Nat. 4 (12): 260. 1801. TIPO: [s. loc.] “Verbena . Fruto muy en ” clusas; sufrútice de entrenudos breves en la bracteata Lagca. et Rodgz^, sd. s. coll. base, de aspecto semi-arrosetado, alargándose (lectotipo, aquí designado, MA 344637 no visto, hacia el el ápice MER. Rcs iu 5. V. caroliniana MA 344637 foto SI!). 15' B s 1 kisa o sufri nunca de spect area ee Mat. Fis. Soc. Ital. Soc. 9: 349. 16(15). Fl p 1802. TIPO: N nel Giardino di Pisa (holotipo, PI con frutos remotos .......... no visto, PI foto S SI). 16' Florescencias reunidas en AE edi Verbena bracteosa Michx., Fl. Bor.-Amer. (Michaux) 2: 13. 10s, trim 1803. Zapania bracteosa (Michx.) Poir. en Lam., ee dad 17 Encycl. 8: 843. 1808. E.E. U.U ien 17(16). Sinflorescencia ladios multí- Nashville, St. Vincent, s.d., s. coll. n 5 otipo, P T MC Lui ce 00307084 no visto, P 00307084 foto SU; isotipo, SU! iT, ra des a. ladios solitarios Ve vi a A. Gray, Syn. FL. N Ur os uo pi Amer. 201): 536. 1878, Verbena brevibracteata (A. Gray) 18(17). Paracladios laxos, hipotagma desarrollado . . . Eggert, Torreya 2: 124. 1902. Verbena bracte een ome Gwen 12. V. hastata brevibr ( y) — dup m ee T w i uper tirare 1979. TIPO: EE. UU. New i of Ric CMS INIM, HM. eA recta Grande, expedition from W Texas to El Paso, May-Oct win Mtr cre eene pec? 456 oitnipe; uduf a ma Te — — pa e 00135428 no visto, GH 00135428 foto SI). implex — i reene, Magen 1: 156. inen, syn. nov. w e 22. V. simp W of 370 Annals of the Missouri Botanical Garden (holotipo, GH no visto, GH foto SI!; pi NY no visto, NY foto SI!, US no visto, US foto SI!). rbena is Gree 1900. TIPO: E.E. U.U. New Mexico: p Co., Sen Juan Mtns., 30 Aug. 1897, E. O. Wott (holotipo, NDG 43276 no visto, NDG 43276 bie S SI!; isotipos, G no visto, MO no visto, NY no visto, NY foto SI!, US no visto, US M SID. Verbena rudis cert Pittonia 4: 152. 1 E. U.U. Colo rchuleta Co., Arboles, 18 Jude 1899, C. F. fie 56 564 MEAN NDG 43339 no visto, NDG 43339 foto SI!; vun F no visto, G no visto, MO no visto, NDG 43340 no visto, 43340 foto SI!, NY no visto, NY foto SI!, P no visto, P foto SI!, SI!, US no visto, US foto SI!). Verbena imbricata Wooton & Standl., Contr. U.S. Natl. Herb. 16: 166. 1913. Verbena bracteata f. imbricata (Wooton & Standl.) Moldenke, n 44: n 1979. TIPO: E.E. U.U. New Mexic armington, 8 Aug. 1904, E. O. Wetton 2831 (h PUN US no visto, US foto SI!). Hierba o sufrútice hasta 60 em de altura, raíz gruesa, hábito rastrero, ramas postradas o erectas, muy ramificadas desde la base, toda la planta con pubescencia híspida, tallos con pelos hasta de 1.5 mm. Hojas de 2-3 X 1-2 cm, sésiles, de lámina dividida, trilobada con 2 lacinias divaricadas en la base de la misma, angostas, lóbulo central de mayor tamaño y margen inciso-dentado, ápice agudo, base cuneado- angostada hacia el tallo, ambas caras con pubescencia híspida con pelos hasta de 3 mm sobre las venas de la cara abaxial, y escabrosos en la cara superior, la base foliar de hojas jóvenes híspida, casi lanosa. Sinflo- rescencia frondosa, formada por paracladios trímeros laxos, mayor a un orden de ramificación, las flore- scencias laterales no superan a la principal, breves y anchas de 10 X 1-12 cm, alargándose fructificación, pedunculadas. Brácteas florales con- spicuas, subuladas, más que el cáliz, de 0.7(-1.2) em, acrescentes y recurvándose con la maduración, ápice agudo, pubescencia escabrosa, margen ciliado, cáliz de 0.25 em, en la madurez de 0.3 em con 5 dientes breves, triangulares, conni- ventes, pubescencia hís pido-escabrosa, principal- mente a lo largo de las venas; corola de color rosa, rojizo o blanco, infundibuliforme, tubo corolino ca. 0.4 cm, angosto, glabro externamente, pubescente en desarrollado, estambres en la la garganta, limbo insertos hacia la zona media del tubo o comino Clusas de 2 mm, longitudi te estriado, cara comisural papilosa. Anatomía caulinar con parén- quima clorofiliano de disposición continua, presencia de cordones de esclerénquima en los cuatro ángulos onografía. Britton y Brown (1913: 96); Wilken u 1093); Diggs (1999: 1057, fig. 108); Felger (2000: 456). Distribución y ecología. Especie mu unn; distribuida en Estados Unidos de América, pr envie mente en los estados del sudoeste como Arizona, Nevada y Colorado; también en México (Perry, 1933). Se la encuentra. en campos Aleron y también en oci qu e cse eena r de rios f la tierra bicis. de 1 m de piamen Observaciones. Se trata de una especie muy abundante, que presenta variaciones en cuanto al hábito más o menos postrado, a la pubescencia y a la longitud de las brácteas florales. evidencian correlación geográfica atención nomenclatural (Perry, 1933). "El hábito postrado, el tamaño de las florescencias y la división de las hojas la asemejaría a una especie del género Glandularia J. F. Gmel.; sin embargo los caracteres florales no se corresponden con éste género, ya que el estilo es breve y el tubo corolino poco desarrollado, entre otras características. Los recuentos cromosómi- cos también indicarían que se trata de una Verbena ya que el número básico sería x = 7, con un 2n = 14 (Noack, 1937; Lóve, 1982a: 353; Ward, 1984). Por otro lado, Perry (1933) demuestra que el transcorte de clusa de V. bracteata se corresponde con la forma subtrígona típica de Verbena, en contraste con la forma subcilíndrica de Glandularia (Perry, 1933: pl. 13, figs. 18, 19). Verbena bracteata se puede confundir con V. gracilis Desf. dado que ambas poseen las brácteas florales conspicuas. Sin embargo, en V. gracilis las brácteas apicales son breves, de 0. Estas variaciones no aspecto y las dimensiones de una hoja vegetativa pequefia, de lámina dividida. Por el contrario, en bracteata las brácteas son siempre mayores a 0.7 cm y son acrescentes hacia la base pero nunca de aspecto foliáceo. Por otro lado V. bracteata no posee pelos ulares mientras que V. gracilis posee pubescen- cia glandular. Eh bracteata también se asemeja a V. canescens Kunth; esta última se diferencia porque posee florescencias angostas, hasta de 0.4 cm lat. y brácteas florales siempre menores a 0.7 cm Greene (1888) funda Verbena dd la diferencia de V. bracteata por las clusas de menor longitud, de dorso ligeramente estriado y la comisura más breve. Estos caracteres son muy variables en V. bracteata y no justifican la existencia de una especie diferente, por lo tanto V. subuligera se trata como sinónimo de V. bracteata ste taxón se incluye en el grupo informal Bracteosae por presentar los caracteres definidos anteriormente para el mismo. Tipificaciones y nomenclatura. La descripción del protólogo de Verbena bracteata se basó en una planta cultivada en el Jardín Botánico de Madrid. El protólogo dice *.. .se ignora su patria y florece por Volume 97, Number 3 2010 O'Leary et al. 871 Revisión Taxonómica de Verbena Julio y sisi ”. La mayoría " los ejemplares e ados ro aeo fueron arrojados al río rt (Sevilla por sus enemigos políticos en MA se encontraron seis ejemplares con la i de Lagasca, probables isotipos (Fernández Casas & Gamarra, 1993). Tres de ellos poseen una fecha posterior a 1801, dos poseen indicaciones de origen o colección que no concue con el protólogo. Consecuentemente, sólo uno de ellos es un correcto isotipo y es aquí deside Meth Gray (1878) no esp p var. brevibracteata, sól bleció áfica en el protólogo: “... Arizona to Texas and adjacenti Mexico”. En GH, nde se hallan depositados la mayoría de los tipos ~ fe se Pai iid eei e los cuatro ibles | : Qa sb lr Pš i : xd de conservación como lectotipo. Cockerell (1911) reconoce Verbena bracteata var. albiflora, tratada posteriormente por Moldenke (1946: 146) como f. albiflora; el ejemplar tipo es de Boulder, Colorado, Estados Unidos de América. En el trabajo de Ewan y Ewan (1981) sobre la biografia de los naturalistas de las montafias Rocosas, se menciona que las plantas coleccionadas por Cockerell fueron distribuidas internacionalmente en diversos herbarios como BM, COLO, K, NY, RM, US. Sin embargo todos estos herbarios fueron consultados y no se ha encontrado el ejemplar correspondiente a la variedad albiflora de Cockerell. Schauer (1847), Perry inae y Moldenke (1962: 267) tratan a Verbena squarrosa Roth (Roth, 1806) como sinónimo de V. bracteata; end ejemplar tipo de la especie de Roth no se ha localizado. Los tipos de Roth estarían depositados en B (ahora destruidos) y BM, sin embargo Steve Cafferty de BM (comun. pers.) dice que no existe material original de esta especie por lo cual sugiere que debería neotipificarse V. squarrosa. A pesar de que la mayoría de los tipos de Greene están depositados en NDG el ejemplar tipo de Verbena subuligera no está allí (Barbara J. Hellenthal, curadora NDG, comun. pers.) sino en GH, y hay dos isotipos en NY y US. M aterial roost examinado. E.E. U.U. 2 uu . Minnesota > 3341). Novales Clarck Co., (SD. Oklahoma: ltarmon Co., Itollis, Sunin 1051 (SD. , 2.8 mi. E Water pass, on US 20, Soth Dakota: Jones Co., NW of Murdo, l Co. CTES). Utah: mesa E of Monticello, a Co 9201 (NY). Wisconsin: Richland Co., center, Nee 1 13460 (CTES). 2. Verbena californica Moldenke, Known Geogr. , Keystone, 30 ho 1938, R. F. Hoover 3870 bon, UC no visto, UC foto SI!; isotipos, NY no visto, NY foto SI!, US no visto). Hierba hasta de 75 em de altura, hábito oe con pubescencia híspido-hirsuta, con pelos ca. pubescencia glandular poco abundante. Mio de lámina entera, obovada, de 5-10 X 2-4 cm, ápice , base subamplexicaule, margen serrado-den ab bicis la porción apical de la lámina; ambas caras con pubescencia escabrosa glandular. Sinflorescencia bracteosa, florescencias reunidas en cladios trímeros, mayor a primer orden de ramificación, las florescencias laterales no superan a la principal, cilíndricas de 10-20 X ca. 0.4 cm, alargándose en la fructificación, pedunculadas, frutos remotos, distan- ciados ca. 1 em. Brácteas florales ovadas, subuladas. de 0.35-0.45 em, de margen piloso; cáliz de 0.4— 0.5 em, con 5 dientes subulados de ca. 1 mm, conniventes en el fruto; ambas piezas con pubescen- cia estrigosa, con abundantes pelos glandulares breves; corola de color azul o violeta, infundibuli- i externamente glabro estambres insertos hacia la zona media del tubo lias Clusas ca. 2 mm, dorso liso a subreticulado, cara comisural lisa o ligeramente papilosa. Anatomía caulinar con parénquima clorofi- liano de disposición discontinua, presencia de seis cordones gruesos de esclerén Iconografia. Wilken (1993: 1093). Distribución y ecología. Verbena californica es endémica del ne se (awe en "ans me de América, ] Observaciones. Verbena californica es una especie amenazada (), sus poblaciones son escasas constituyendo un taxón poco frecuente. Se diferencia fácilmente del resto de las especies por sus hojas de margen serrado-dentado hacia la porción apical de la lámina y base subamplexicaule y las florescencias largas con frutos distanciados. En este último aspecto se asemejaría a Verbena carolini- ana diferenciándose porque en ésta última las hojas son sésiles y de margen finamente serrado-dentado a lo largo de toda la lámina. Este taxón se incluye en el grupo informal Hastatae por presentar los caracteres definidos anteriormente para el mismo. Material adicional examinado. E.E. U.U. California: Tuolumne Co., W base of Taylor hill, S Chinese Camp, 4 372 Annals of the Missouri Botanical Garden Hoover 9885 (NY); Tuolumne Co., 1 1/2 mi. SW Chinese Camp, Hoover 3613 (NY); Tuolumne Co., Chinese Camp, Moldenke 25758 (MO). 3. Verbena canescens Kunth, Nov. Gen. Sp. (quarto ed.) 2: 274, t. 136. 1817 [1818]. TIPO: México. Guanajuato: “Marfil et fodinam Bel- grado, alt. 1000-1250 hex”, fl. Sep., A. Bonpland s.n. (holotipo, P 00108609 no visto, P 00108609 foto SI!; isotipos, P 108610 no visto, P 108610 foto SI!, SI!). Verbena roemeriana Scheele, Linnaea 21: 755. 1848, syn. nov. Verbena canescens var. roemeriana (Scheele) L. M. Perry, Ann. Missouri Bot. Gard. 20: 302. 1933. TIPO: E.E. U.U. Texas: Comal Co., 1 mi. W New Braunfels, 21 Apr. 1946, B. Warnock 46244 (neotipo, aquí designado, NY!). Verbena neei Moldenke, Phytologia 2: 241. 1947. TIPO: ntina. Pampas de Bue: ires, L. Née, Iter 108, ires, Exped. Malaspina (holotipo, MA no visto; isotipos, NY no visto, NY foto SI!, SII). Verbena canescens f. albiflora Moldenke, Phytologia 9: 500. 1964, syn. nov. TIPO: México. Puebla: ruta Tehuacá— Orizaba, 18 July 1961, C. E. Smith, F. A. Peterson & N. Tejeda 3940 (holotipo, US no visto, US foto SI”. Hierba semi lige te r l tallos ascendentes hacia el ápice, hasta de 50 cm, general- mente multiramosa desde la base, pubescencia íspido-canescente, pelos hasta de 1 mm, algunos glandulares. Hojas de 1-5 x 0.5-2 cm, de lámina oblonga angosta, dividida pinnatilobada, sésiles, base subamplexicaule a modo de pecíolo ensanchado, margen subrevoluto con 2 a 5 dientes breves a cada lado de ápice agudo; textura ligeramente cartácea a rugosa, envés con pelos de 0.5 mm, escabrosos sobre las venas prominentes, en la cara adaxial pubescencia escabrosa uniforme de pelos de base bulbosa, canescente, con algunos pelos glandulares. Sinflo- rescencia frondosa, formada por paracladios trímeros, las florescencias laterales superando a la principal florescencias de 13 X 0.4 cm, flores densamente imbricadas en antesis, distanciadas ca. 0.5 cm en su madurez, a veces con pelos glandulares en raquis y 3 ; n ciliado; cáliz de menor o igual longitud, de 0303. € t dientes triangulares, pubescencia velutino-villosa, con algunos pelos glandulares; corola de color azul violeta, lila o blanco, infundibuliforme, tubo sols breve, de 0.4-0.65 cm, externamente glabro, interior villoso en la garganta; estambres insertos hacia la zona media del tubo corolino. Clusas de 2-2.5 mm con dorso reticulado y cara comisural papilosa. Anatomía caulinar con parénquima clorofiliano de disposición continua, presencia de numerosos cordones de esclerénquima. n = 7, 2n = 14 (Lewis & Número cromosómico. Oliver, 1961). Iconografía. Kunth (1818: t. 136); Diggs (1999: 1059, fig. 108); Rzedowski y Rzedowski (2002: 121). Distribución y ecología. Se distribuye desde el sudoeste de Estados Unidos de América, en el estado de Texas, hasta Colombia (Rzedowski € Rzedowski, 2002), encontrándose la mayor cantidad de especí- menes en los estados del centro de México. Crece en terrenos erosionados, calcáreos, arcillosos o salinos, muchas veces rodeada de vegetación halófita. Observaciones. Verbena canescens se caracteriza por su porte bajo y compacto, su pubescencia hirsuto- canescente, sus flores pequeñas de cáliz menor de 0.35 cm y su tubo corolino menor de 0.65 cm. Las brácteas florales son generalmente acrescentes hacia la base de la florescencia, llegando a 0.65 X 0.35 em, en algunos casos tornándose algo foliáceas (ej., Rose 8971, US). Este taxón se diferencia de Verbena gracilis porque éste último posee brácteas florales foliáceas, princi- palmente hacia la base de las florescencias, hojas con pubescencia estrigosa o escabrosa, no canescente, lámina pinnatipartida a pinnatisecta con margen inciso-dentado, siendo pinnatilobadas y el margen con dos a cinco dientes a cada lado en V. canescens. Verbena neomexicana es la especie más fácilmente confundida con V. canescens. Se diferencian en el hábito, siendo V. neomexicana plantas más grandes y erectas, las hojas son muchas veces pinnatipartidas con base subamplexicaule cuneada hacia un pecíolo ancho, marginada; mientras que en V. canescens las hojas suelen ser de lámina entera o pinnatilobada con el margen dentado. Además las flores de V. canescens suelen ser de dimensiones menores (hasta de 0.65 cm long. vs. hasta de 1 em long. en V. neomexicana). Verbena canescens también es afín a V. plicata, pero este ültimo taxón posee hojas de lámina elíptico- redondeada, pecíolo ancho extenso, cara i prominentemente marcada por la venación y brácteas florales más desarrolladas, de 0.15-0.4 cm lat. acrescentes en la madurez. Perry (1933) explica que V. canescens estaría estrechamente relacionada con V. neomexicana y V. plicata, pero que se diferencia de aquellas por poseer las hojas elongadas de base semiamplexicaule y su hábito algo compacto. erbena canescens f. albiflora se trata bajo la sinonimia de V. canescens ya que la única diferencia Se encuentra en el color blanco de las corolas, carácter taxonómicamente irrelevante. Volume 97, Number 3 2010 O'Leary et 373 R evisión a de Verbena Perry (1933) sugiere que la variedad roemeriana se diferencia por ser densamente hirsuta, casi sin pelos glandulares, y las brácteas florales más grandes con ápice abruptamente acuminado. Moldenke (1963a: 475) también reconoce esta variedad. A € del continuo de valores, habiendo ejemplares con brác- teas de casi 0.7 cm (Lundell & Lundell 10162, NY) hasta ejemplares con brácteas de 0.3 em (Lundell & Lundell 9796, NY), pasando por estados intermedios (Hill & Taller 3993, NY). Perry (1933) también encuentra ejemplares que representarian fases inter- ias o transicionales entre la especie y su variedad. Por lo tanto la variedad r sinonimia de V. canescens variedad ti roemeriana se trata bajo la Este taxón se incluye en grupo Bracteosae por wee los caracteres definidos anteriormente para el mi Tipificaciones y nomenclatura. Se trató de locali- zar el ejemplar tipo de Verbena roemeriana, según el protólogo: “Auf steinger Prairie bei Neubraunfels, Römer” pero se desconoce donde están depositados los tipos de Adolf Scheele. A partir del protólogo el tipo sería un ejemplar coleccionado por Römer, por lo tanto se preguntó a los herbarios BRNU, GH, L y W, también se consultó a TEX porque V. roemeriana fue publicada en la Flora of Texas. En ninguno de los mencionados herbarios se pudo localizar el material original. Perry (1933) no citó el tipo de este taxón en su monografía de Verbena para Norteamérica. Se encontraron ejemplares de la misma área geográfica citada en el protólogo, que coinciden plenamente con a descripción en el mismo, por lo cual se eligió uno de ellos como a Troncoso (196: 29) e examinó E material tipo de Verbena neei ra a 1947: 241) depositado en MA y comprobé que no es una a Argentina como erróneamente dice la etiqueta (como tantos otros ejemplares de Née que sufrieron confusión de rótulos) y que se trata de un ejemplar de México que corresponde a V. canescens. Material adicional examinado. COLOMBIA. Cundina- marea: cerca Bogotá, San Cristóbal Andes, Feb. 1908, re s.n. (SI 3343), € Mar. 1908, Apollinaire sn. (SI 3427). E.E U.U. New Mexico: San Miguel Co., O'Connor Trust Ranch, A & Levandoski 12070 (NY). Texas: Bexar Co., 25 mi. S of San Antonio, Schulz 526 (US); Runnels Co., N Ballinger, Zu Lundell & Lundell 10162 (NY); Starr Co., E Rio Grande city, Lundell & Lundell 9796 (NY); Val Verde Co., Red Arrow Campground, Hill & Taller 3993 (NY). MÉXICO : near Aguascalientes, Rose Ae £5 e 15 km W C. del Oro, Stanford aol 0). Hidalgo: Rancho Mazatepec, 1 km omás, Hernández Magaña 4890 (MO); near Ixmiquilapas, Rose et x a Nuevo León: Galeana, Hac. San José de Raíces, Mueller 2305 (MO). Oaxaca: Elba, Estación Las Sedas, Conzatti 4194 (US). Puebla: Pay ga oe Arséne 48 (BAF); ranza, Balls 5266 (US). San Luis sine 33.4 mi. E Salinas, Kral 2720 (MO). Tamaulipas: e los Armadillos, ca. San José, Bartlett 10186 (US). ruin llanos de Alchichica, Gómez-Pompa 3817 (MO). 4. Verbena carolina L., Syst. Nat., ed. 10, 2: 852. , 1732 (lectotipo, aquí designado, Dillenius [1732: t. 301, fig. erbena veronicifolia Kunth, Nov. Gen. Sp. (quarto ed.) 2: 275. 1818, sphalm. “veronicaefolia”. TIPO: México. Hidalgo: Morán, s.d., F. W. Humboldt & A. Bonpland s.n. (holotipo, P no visto, P foto SI!). erbena polystachya Kunth, P Gen. Sp. (quarto ed.) 2: 274. 1818. Verbena carolina [sphalm. caroliniana] var polystachya (Kunth) ae Repert. Spec. Nov. Regi Veg. 9: 362. s< ge México. Michoacán: ladera acil Xorullo, s.d., F. W. A. and lotipo, P no pape, P foto SI!; isotipo, SI!). Volo biserrata Kunth, Nov. Gen. T {g zn > Vi 1818. TIPO: México A Hi & A. mgr P. no dai T foto SI!; isotipo, SI!). Verbena paucifolia M. Martens & ym on v Jer Sci. — "m 324 s.d., H. Elbe 773 ta dae m no o vito, BR Mio SI! Verbena hirsuta M. M Mariee & Galeotti, Bull. Acad. Roy. Sci. & idee Moldenke, Phytologia 47: 330. 1981. TIPO: México. Veracruz: Xalapa, June-Oct. 1840, H. Galeotti 735 (lectotipo, aquí designado, BR no visto, BR foto SI! Verbena alli M. Martens & Galeotti, Bull. Acad. gu Sci. Verbena San , Apr. 1840, H. Galeotti 737 po, BR no m BR foto SI). Verbena long folia a M. Martens & Galeotti, Bull. Acad. Roy. Sci. Bruxelles 11(2): 323. 1844, syn. nov. TIPO: México. Michoacan: oo d'Ario, Aug. 1840, H. otipo, BR no yie, BR foto SI; no visto, Pí foto SK, SI”). i genini i Moldenke Phytologia 2: 27. ~ syn. nov. TIPO: M Sierra Monterrey, Qda. de ott Gentry 592: 3 (holotipo, Lh pos, MICH no visto, MICH H foto Si, Mot SI, US no = 2 foto SI!). Moldenke, Phytologia 2: . TIPO: E lina, s.d., H. Herb G. A one (holotipo, 55, syn. nov. o SI"). dula Moldenke, Phytologia 5: 229. 1 ve TPC : nicae Bowman Ecuador. Islands: Island, Sta. Cruz, 15 Feb. 1953, R. (holotipo, UC no visto, UC foto SI!; e LL no is) Verbena longifolia f. e. ie Phytologia 1961. syn. nov. o. Oaxaca: Patio i ds near Cerro I S jad 2900 m, 7 Aug. 1950, B 374 Annals of the Missouri Botanical Garden Hallberg 813 (holotipo, MICH no visto, MICH foto SI!; isotipos, CTES!, SI!, TEX no visto, TEX foto SI!, US no visto, pdas foto SI!) Ve sag orn Moldenke, i ane 7: 430. White 3379 (holotipo, MICH no visto, MICH foto SI!). Verbena nii var. pubescens Moldenke, ene 13: 966, syn. nov. TIPO: México. Oaxaca: Pto. BE 30 Aug. 1965, D. Bede. 12292 lotipo, TEX no visto, TEX pio SI; isotipos, MICH no visto, MICH foto SI!, SI!). Verbena glabrata T var. tenuispicata gener p gia 14(5) 283. 1967, syn. nov. Galápagos Islands: Villamil, ema, 6 eas ft, 23 Aug 1905, A. Stewart 3317 (hol , NY no visto, NY foto SI!; isotipos, US no I US foto SR, SI). Verbena sedula var. darwinii Moldenk Phytologia 16: 34 syn. nov. TIPO: UPG alápagos Islands: James Island, Oct. 1835, C. Darwin s.n. (holotipo, CGE no visto, CGE foto SI!). sedula var. agn ie npa 18: 211. -— Š ‘erbena 1969, sy v. rugs Islands: Chatham Island, n Y 1964, L. A. Fournier 269 holoti no visto, TEX foto SI!; Aie NY no po, TEX visto, NY - um SI”. th f. magnifolia seg Phytologia T syn. nov. TIPO: Ecuador. Napo: Tena alacios 4188 (hclotins, TEX no Sinto, ?. hrenbergia ar. richardsonii rem "iis 38: 4 s. 1978, = nov. TIPO: Méxic z Farias area, 29 Ma 1969, A Hilda 1234 ( ukpa. TEX n no visto, TEX foto SI!; isotipo, SI!). Hierba erecta, de 0.3-1 m, tallos solitarios o ramificados desde la base, pubescencia variable, subglabros o híspidos, a veces hirsutos y ásperos al tacto. Hojas de lámina entera, oblongo-elíptica, de 3— e X 0.5-1(-4) cm, sésiles a et de base margen entero a i crenado o nas, ápice agudo, pubescencia M Sinflo- rescencia bracteosa, formada por paracladios trímeros laxos, mayor a la principal, de 10-30 x 02-045 em, ormes en la antesis, alargándose en la fructifica- ción, con frutos remotos; flores sésiles a subpedice- ladas en la fructificación. Brácteas florales ovadas, de dorso y cara comisural lisos. Anatomía a parénquima clorofiliano de disposición continua, presencia de numerosos cordones de esclerénquima. Número cromosómico. = 7, 2n = 14 (Lewis & Oliver, 1961). Iconografía. Gibson (1970: 231, fig. 46). Distribución y ecología. Verbena carolina habita desde el sur de Estados Unidos de América hasta Ecuador, con el mayor número de representantes en México y América central. Crece en bosques y laderas húmedas. Observaciones. En Verbena carolina la oe cia es un carácter muy variable, ontrándose ejemplares subglabros (ej., McVaug a "18865, US; Howell et al. s.n., MO; Smith et al. 3701, US; Matuda 16217, US), hasta ejemplares hispidos con pelos hasta de 1 mm (ej., Balls 4667, US; Bourgeau 119, US; Tucker 1307, NY, US). Puede haber pelos glandulares breves en cáliz y raquis (ej., Rueda 12931, MO). Lo más frecuente es que en Verbena carolina las hojas sean de base subpeciolada, sin embargo se observaron ejemplares con pecíolos desarrollados hasta de 2 cm (ej.. Palmer 1156, US; Bowman 81, ejemplar tipo de V. sedula), siendo este carácter poco frecuente. Verbena carolina es morfológicamente afín a V. urticifolia y V. scabra por poseer además de las florescencias filiformes, hojas de lámina entera, o las Verbena urticifolia se diferencia porque los dientes del cáliz son no conniventes y V. scabra se distingue porque las hojas son pecioladas y la pubescencia es escabrosa artens y Galeotti i (1844) fundan Verbena long- ifolia Fa ma como un taxón subglabro, con jas brevemente pecioladas, elongadas, de ápice agudo y margen serrado y florescencias filiformes. À partir del análisis del material tipo y de numerosos ejemplares de herbario se observó que los caracteres T mencionados no permiten diferenciar à V. longifolia de V. carolina, consecuentemente en el presente tratamiento este taxón se trata bajo la sinonimia de V. carolina. A su vez, V. longifolia var. pubescens se diferenciaría por la pubescencia más abundante, siendo éste un carácter muy variable en V. carolina, por lo cual este taxón se considera sinónimo de la misma. El ejemplar tipo de Verbena longifolia f. albiflora, así como el de V. carolina f. albiflora sólamente se diferencian del tipo de V. carolina por el color blanco de las corolas, siendo color violeta en el ejemplar tipo. Este carácter se considera insuficiente para definir una variedad, por lo tanto estos dos taxones son tratados bajo la sinonimia de V. carolina. Volume 97, Number 3 2010 O'Leary et al. Revisión Taxonómica de Verbena Moldenke (1946: 147), en el protólogo de Verbena curtisii comenta que es una especie afín a V. carolina e difere por la pubescencia casi inconspicua. | hind: Moldenke sinonimiza V. curtisii bajo V. carolina sin dar explicaciones. Verbena ehrenbergiana var. richardsonii posee hojas enteras no divididas; el análisis del material tipo permitió verificar que este taxón es un sinónimo de V. r Gentry e México. Lo define como cercano a V. urticifolia, pero sin las hojas pecioladas de ésta ültima especie. A partir del análisis del material tipo se deduce que el mismo no se diferencia de V. carolina, por lo cual se incluye en la sinonimia de la misma. Moldenke (1977) funda Verbena laesit f. magni- folia indicando que se diferencia de V. litoralis forma típica (taxón de la serie Pachystachyae, tratado e O'Leary et al., 2007) por sus hojas mayores de margen irregularmente serrado-dentado. El análisis del ejem- plar tipo de la forma magnifolia evidencia que se corres e con V. carolina y en el presente tratamiento se coloca bajo su sinonimia. Stewart (1911: 134) en su trabajo para la flora de las Islas Galápagos menciona la presencia de Verbena carolina. Posteriormente, Moldenke (1955: 229) funda V. sedula para las Islas Galápagos, definiéndola como un taxón subglabro de hojas con lámina entera, pecioladas. El sop “kl mares tipo de v. sedula y la dos és taxón no puede oli de Y. je por lo cual en este trabajo se trata como sinónimo de esta última especie. Las dos variedades de Moldenke, V. sedula var daruinii y V. sedula var. fournieri se diferenciarian de la variedad tipo por la pubescencia: en el primer caso pone, larga, dones y en y en el segundo caso vegetativas y densa en A cara abaxial de las hojas: Sin embargo, V. carolina es un taxón muy variable este carácter, como se comentó anteriormente, por lo tanto, ambos taxones se tratan como sinónimos de V. carolina. Moldenke (1967) funda Verbena glabrata var. tenuispicata basada en el ejemplar Stewart 3317 que lenuispicata como sinónimo de embargo, el ejemplar Stewart 3317, si bien es un paratipo de V. townsendii, no se corresponde con la descripción de la especie ni el tipo de la misma, ya que posee hojas de lámina entera, desarrollada, homogéneas en toda la planta, muy diferente de lo que ocurre con el tipo de V. townsendii, donde las hojas son bipinnatipartidas, trisectas, a lineares. Consecuentemente, este ejemplar se corresponde con arolina, por lo cual V. var. tenuispicata es tratado como sinónimo de V. carolina. Este taxón se incluye en el grupo informal Verbena por presentar los caracteres definidos anteriormente para el mismo. Tipificaciones y nomenclatura. En el protélogo de carolina la única referencia a un ejemplar tipo es “Habitat in America septentrionalis”. Se consultaron los herbarios BM-LINN y UPS (comun. pers. Mark — BM y Mats Hjertson de UPS) y no se encontró al original. Moldenke (1963a: 495) designó *Herb. ‘Linn 35.17” (LINN) como tipo de V. carolina. Sin embargo este ejemplar no fue visto por Linnaeus y proviene de Jacquin en 1761, por lo cual al., 2006: Art. 9.10). Charlie Jarvis, del Linnaean Plant Name Typification Project, coincide que la ilustración en Dillenius (1732) es la correcta elección del lectotipo por lo cual aquí se acepta esta opinión. Martens y Galeotti (1844) mencionan dos sintipos en el protólogo de Verbena hirsuta: Galeotti 735 y Galeotti 790. El ejemplar Galeotti 790 presenta un desarrollo anormal de la inflorescencia, por lo cual el ejemplar Galeotti 735 es aquí elegido como lectotipo por corresponderse con el protólogo de la especie. Material adicional examinado. COLOMBIA marca: Usaquén, cerca Bogotá, Diaél 3419 (SD. ECUA- DOR. Islas Galápagos: San Cristóbal Island, cerca El amn van der Werff 2208 (MO). EL SALVADOR. San : s. loc., Jan. 1922, Calderón 794 (US). w € E PE P. Standley 21331 (MO). Santa Ana: jos, E cerro de los Naranjos, Tucker 1307 K o prs UU. Arizona: Cochise Co., Blumer 1783 (MO, NY, US). Florida: Inter TRR et St , s.d., Rugel s.n. (MO) GUA + Cal Türckheim 101 (BAF). Baja — ga _ les (MO, ong Guatemala: Mixco, Las Hoj , Castillo 1568 MO). Izabal: cerca La Amates, gri Re Montagua, MO). Mo 24443 (MO). Quiché: Nabaj. Proctor 25004 ( San Marcos: San Rafael, Kellerman 6540 (US). Santa n Santa Rosa, an & Lux 3019 (US). HONDURAS. rancisco E agua, Siguatepeque, Yuncker et i 5625 (MO, NY). MÉXI ICO. Chiapas: Mt. Ovando, Escuintla, Matuda 16217 (US); Oxchuc, 1 km N del centro, Gómez Santiz 233 (MO, NY). Chihuahua: s . loc., Aug. 1885, Palmer 364 (N ima: s. loc, Palmer 1156 (US). : s. loc., May 1896, Palmer 339 (US) juato: Salvatierra “Rancho Cruces”, Flores . SD. H. (BA Moldenke 19837 ‘as Nayarit: 8 mi. W Tepic, McVaugh == (US). Nuevo León: Hacienda Pablillo, Galeana, M. 376 Annals of the Missouri Botanical Garden Taylor 238 (NY). Oaxaca: 13.6 km N Ixtlan de Juarez, B. Bartholomew et al. 3291 (NY). Puebla: Tehuacán, above Calipan, Smith 3701 (US). Sinaloa: Rosario, Oacalotán, Gonzalez Ortega 4123 (US); Concordia, Sta. Lucia, Dehesa 1551 (US). d río Mayo, Mesa La Lagunita, s.d., Howell et al. s.n. (MO 4656255). Veracruz: Los Molinos, Perote 4667 (US) NICARAGUA. Estelí: cerca Tomabá, Rueda et al. 12931 (MO). 5. Verbena caroliniana Michx., Fl. Bor.-Amer. (Michaux) 2: 14. 1803. TIPO: E.E. U.U. “Hab. in Carolina”, s.d., A. Michaux s.n. (holotipo, P 00307093 no visto, P 00307093 foto sI”). Figura 1. Sufrútice erecto hasta de 70 cm de altura, poco ramificado, entrenudos breves, de aspecto semi- arrosetado, alargándose hacia el ápice; pubescencia hirsuta de pelos breves y algunos pelos glandulares, homogéneamente distribuidos en tallos y hojas. Hojas de lámina entera, elíptico-obovadas, de 4-8 X 1.5- 2 cm, ápice obtuso y base cuneada, sésiles, margen finamente serrado-dentado a lo largo de toda la lámina, con pelos hirsuto-estrigosos en ambas caras, principalmente sobre las venas en la cara abaxial. .32 cm, margen piloso; cáliz de 0.4-0.5 em, con 5 dientes triangulares evidentes de 1 mm, subconni- ventes en la fructificación; ambas piezas de pu- bescencia hirsuto-glandular; corola E di T rosa o azul, infundibuliforme, tubo corolino de l cm, con pubescencia externa abundante, interna- mente la garganta pubescente, limbo des arrollado mayor a 0.5 mm lat.; estambres insertos hacia la zona media del tubo corolino. Fruto se separa tardíamente en cuatro clusas cada una de 3 mm , de dorso longitudinalmente estriado. Autos des con énquima clorofiliano de disposición discontinua, presencia de numerosos cordones de esclerénquima. Distribución y ecología. Esta especie crece en el Sudeste de Estados Unidos de América, desde el estado de Carolina del Norte hasta Florida, al sur, y al oeste hasta Kansas. Se la encuentra en lugares secos y arenosos. Observaciones. La separación tardía del fruto un carácter únicamente presente en esta especie del género Verbena. Esta característica motivó que diversos autores la consideraran dentro de géneros generalmente monotípicos, fundados ad hoc: Phryma caroliniensis Walter (Walter, 1788), Stylodon scabrum Raf. (Rafinesque, 1825), Styleurodon caroli- nianum Raf. (Rafinesque, 1836), nde ania (Walter) Small (Small, 1933) y Stylodon carneus (Medik.) Moldenke (Moldenke, 1937). Michaux (1803) fue el primer autor en considerar este taxón dentro de Verbena como V. caroliniana. Verbena carnea Medik. (Medikus, 1783), citado por Schauer rry (1933) como taxón válido dentro de Verbena, carece de tipo y por la descripción del protólogo resulta imposible determinar de que especie se trata, Moldenke (1937) asoció este taxón bajo el género Stylodon Raf. Este taxón se incluye en el grupo informal Hastatae por presentar los caracteres definidos anteriormente para el mismo Material adicional examinado. E.E. U.U. Alabama: mi. NE Grangeburg, Mac Donald 11100 Marion Co., Irvine, Moldenke 1091 (MO). Georgia: Co., cerca Valdosta, Chase 34 (MO). Kansas: cerca Eustis, an. 1894, Hitchcock s.n. (MO). Louisiana: Chopin, Natchitoches Parish, Palmer 7564 (K). D Carolina: Southeastern, s.d., W. Ashe s.n. (MO). South Carolina: Georgetown Co., cerca Georgetown, Godfrey pe (MO). erbena cloverae Moldenke, Amer. Midl. Nat- 1934, E. U. Clover 1618 (holotipo, NY no visto, NY foto SI!; IU MICH no visto, MICH foto SI!). Figura e. c: var. lilacina oe Phytologia 2: 23. : as: alle Co., near vingt 9 Apr. 1941 Lu LI d & A. A. Lundell 10142 (holotipo, NY no visto, NY foto SI!; isotipos, MICH no visto, MICH foto SI!, TEX no visto, TEX foto SI”). Verbena cloverae f. oc P Wrightia 2: A Lm syn. nov. TIPO: E - Texas: Zapata Co., 83.8 mi. a CL Lado E "3 ‘A. Lundell 15055 (holetipe, TEX no visto, TEX foto SII). Sufrútice de base leñosa, de 30-70 cm de altura, tallos erectos ascendentes, pubescencia hirsuto-glan- dular. Hojas de 3-7 X 1.5-3 cm, de lámina entera a trilobada, lóbulo central no dividido de margen inciso- dentado; pecíolo ancho hasta de 2 cm reduciéndose hacia la base subamplexicaule, ápice obtuso, textura rugosa, con pelos hirsutos e híspido-escabrosos sobre la cara adaxial, con algunos pelos glandulares, cara abaxial muchas veces con venación protruyente. Sinflorescencia frondosa, formada por florescencias solitarias o en paracladios trímeros, florescencias de 30 X 0.6 cm, densas en antesis, frutos remotos en la fructificación. Brácteas florales ovadas, de 0.3- 0.45 cm, ápice agudo y margen ciliado; cáliz de 0. - em, con 5 dientes agudos de 1 mm, subconniventes en la fructificación; ambas piezas hirsuto-pubescentes con pelos glandulares; corola de Volume 97, Number 3 O'Leary et al 377 Revisión Taxonómica de Verbena planta. —B. Flor con bráctea. —C. Fruto. A—C de Moldenke 1 "Mr Verbena caroliniana. —A. Aspecto general de la color azul, purpüreo, lila o blanco, M comisural verrucosa. Anatomía caulinar con parén- tubo corolino ca. 1 cm, externamente subglabro, quima daiam de disposición discontinua, pre- internamente con pubescencia vilosa y in moni- sencia de seis cordones gruesos de esclerénquima. liformes en la garganta, limbo extenso de 0.6-1 cm ; estambres insertos hacia la zona media del tubo Número cromosómico. n corolino. Clusas ca. 2.8 mm, dorso liso o estriado, cara 1961). x 7 (Lewis & Oliver, 378 Annals of the Missouri Botanical Garden Figura 2. Verbena cloverae. —A. to aag t 7 m general de la planta. —B. Detalle de pubescencia del tallo. —C. Flor con Volume 97, Number 3 2010 O'Leary et al ` 379 Revisión Taxonómica de Verbena Distribución y “ecología. Verbena cloverae es endémica del estado de Texas, Estados Unidos de América. Observaciones. Verbena clouerae se caracteriza por sus hojas de lámina trilobada con ápice subobtuso. Las flores son vistosas, de tubo corolino largo, ca. 1 cm à limbo desarrollado, RA Puede presentar las nas de la cara más gruesas y protruyentes " Lundell 9866, US) principalmente las terminales de cada diente de o lámina, — a lo Aes ocurre en V. plicata. Se diferencia porque en V. plicata las cies A son acrescentes en la A y sobrepasan el cáliz en gran medida y notoria vena media. Moldenke (19412) funda la variedad lilacina re la base de ejemplares con flores lilacinas. Posteriormente Moldenke (1963b: 34) sinonimiza su vari jo la variedad tipo, explicando que existen muchos tipos de gradaciones de color, desde el blanco al violeta. Por lo tanto, la forma alba de dell que se diferenciaria por poseer flores blancas, también se trata aquí como sinónimo de la forma tipo Este taxón se incluye en el grupo informal Hastatae por presentar los caracteres definidos anteriormente para el mismo Tipificaciones y nomenclatura. En el protélogo -Moldenke (1940b: 751) escribe “Verbena cloveri” pero como este epíteto específico se basa en el apellido de mujer, según el Art. 60 del código de Viena (Mene et al., 2006) debe ser “cloverae”. Material adicional examinado. E.E. U.U. Texas: Brooks Co., Encino, Lundell 10823 (NY); Starr Co., 3 mi. W Sullivan City, Lundell & Lundell 9886 (US). 7. Verbena demissa Moldenke, Phyiolepe 4: 183. 1953. TIPO: Ecuador. Cañar: NE Azogues, Man arcos, 1 Apr. E 2510 (holotipo, NY no visto, NY foto Sn isotipos, SI!, US no visto, US foto SI!, W no visto). Figura 3. Verbena demissa f. alba Moldenke, Phytologia 36: 51. 1977. TIPO: Ecuador. ger ha: hoot €—— crater Pululagua, 23 Jan : -Palacios 4200 (holotipo, TEX no ot TEX a M vise SI). Hierba de hábito postrado, ramas subleñosas y numerosos tallos decumbentes surgiendo de un mismo Punto, entrenudos largos o no; pubescencia adpresa escasa con algunos pelos glandulares breves. Hojas de lámina entera, elíptica, de 1-2 X 0.5-1 cm, subsésil, ápice subobtuso, base cuneada, márgenes con dientes x la porción más ancha de la lámina bacia el ápice, con pubescencia meae poco densa. Sinflorescencia frondosa, formada por florescencias solitarias o reunidas en paracladios trímeros laxos, las laterales superan a la principal, florescencias cilíndricas laxas, de 0.3-7 cm en la fructificación; brácteas ovadas, de 0.15-0.2 cm, a subestrigosas con márgenes pilosos; cáliz de 0.2-0.25 cm, pubescencia subestrigosa, a veces algunos pelos glandulares, con 5 dientes triangulares breves poco evidentes, subconniventes en la fructifi- cación; corola de color azul o lila, infundibuliforme, tubo corolino breve de 0.3-0.4 cm, externamente glabro, con pelos moniliformes en la garganta; insertos hacia la zona apical del tubo corolino. Clusas de 1.8 mm, dorso y cara comisural isos. Anatomía caulinar con parénquima clorofiliano de disposición continua, presencia de numerosos cordones de esclerénquima. Distribución y ecología. Este es un taxón endé- mico del centro de Ecuador, crece en las provincias de Azuay y Cañar. Observaciones. Verbena demissa es un taxón escasamente coleccionado y poco conocido. Se caracteriza por su hábito postrado y sus florescencias breves con flores ligeramente pedicela La forma alba de Moldenke únicamente se diferenciaría por el color de las flores, por lo cual habiendo visto que el material tipo no difiere de la forma tipo en ningún otro carácter, se la trata como sinónimo de la misma. Este taxón se incluye en el grupo informal Bracteosae por presentar los caracteres definidos anteriormente para el mismo. Matadero, 17801 (G, K, NY, P, SI, ge Cuenca, m 22851 (NY); Río Tarqui, 4—18 km S — em 1 (K, NY). Cañar: cerca El Tambo, Játiva 2 & Epling 260 ehrenbergiana Schauer, Prodr. 11: 548. 1847. TIPO: México. Veracruz: Prov. Huasteca, Wartenberg, near Tantoyuca, 1858, C. Ehrenberg 153 (neotipo, aqui designado, P no visto, P foto SI!). Figura 4. Hierba erecta, hasta de 1 m, pubescencia hispido- estrigosa. Hojas de lamina trilobada, de 6—8(-10) X 2-3(-5) em, de base cuneada angostándose hacia un breve pecíolo de 1-2 cm, ápice agudo, margen entero a ligeramente inciso serrado o dentado, nunca ai pubescencia estrigosa en am aras. Sinflorescencia de aspecto paniculoide, mayor a un orden de ramificación, bracteosa, fo por c Annals of the Missouri Botanical Garden í (2 Z | AN AN —A. Aspecto general de la Figura 3. Verbena demissa. pubescencia del raquis de la inflorescencia. —D. paracladios multímeros laxos, con gran profusión de florescencias, las laterales no superan a la principal florescencias delgadas, filiformes y gráciles, de 10—15 Xx 02-03 A A £ < $ peciaua piloso; cáliz de 0.18-0.2 cm, estri i ; - goso, dientes triangulares, subconniventes en la fructificación; C planta. —B. Detalle de nudo con dos hojas. —C. Detalle de Flor con bráctea. A-D de Asplund 17801 (NY). corola de color blanco o lila, infundibuliforme, tubo corolino breve, apenas más extenso que el cáliz, de 0.22-0.28 cm, extema e internamente glabro, limbo poco desarrollado; estambres insertos hacia la zona apical del tubo corolino. Clusas de 1.2-1.5 mm, dorso y cara comisural lisos. Anatomía caulinar con Parénquima clorofiliano de disposición continua, presencia de numerosos cordones de esclerénquima. 381 Revisión Taxonómica de Verbena O'Leary et al. Volume 97, Number 3 2010 — ——] t q h ez aS e >g : ` š x DAN e. Mi s - Ss m E K. X RN N E Ë D ot E f M m m - Tu ` 9 >t N. S M NY = — eR Z »- A — Oe meg tof — B. Detalle de pubescencia del tallo. —C. Flor con de Pringle 1948 (MO). general de la planta. 9305 (MO); cto —D. Detalle de cáliz fructífero. A de Croat 3 gura 4. Verbena ehrenbergiana. —A. Aspe bráctea, Fi Annals of the Missouri Botanical Garden 14 (Lewis & Oliver, Nümero cromosómico. n — 1961). Distribución y ecología. Verbena ehrenbergiana es endémica del este de México, donde se la ha encontrado en suelos arenosos o arcillosos. Observaciones. Verbena ehrenbergiana se asemeja a V. urticifolia y a V. carolina por poseer florescencias filiformes agrupadas en me bracteosas y flores eñas, remotas; difiere porque V. ehrenbergiana posee hojas laa siendo las hojas enteras en V. urticifolia y V. c Además, V. ehrenbergiana y V. REA poseen áreas de distribución diferentes, la primera es endémica de los estados del este de México, mientras que la nda es endémica de los estados del noreste de Estados Unidos de América. Verbena ehrenbergiana también podría confundirse con V. menthifolia Benth., siendo ambos taxones simpátricos; se diferencian porque en ésta última el margen de las hojas es irregularmente inciso-dentado y las flores poseen limbo corolino evidente, siendo las hojas regularmente inciso serradas o dentadas y las flores muy pequefias de corola inconspicua en V. ehrenbergi Este taxón se incluye en el grupo informal Verbena por presentar los caracteres definidos anteriormente para el mismo. Tipificaciones y nomenclatura. El tipo de Verbena ehrenbergiana: “México. Los Reyes, Ehrenberg 713” estaba depositado en B y fue destruido. El dato “Los . Reyes” es ambiguo, existiendo en México muchas localidades y pueblos con ese nombre (Rzedowski, comun. pers.) Actualmente se cuenta con la foto de la serie de MacBride del Field Museum neg. 17414. En los consultados (BM, C, GH, ILL, JEPS, K, KIEL, MICH, P, STR, US, W) no se encontraron isotipos. Por lo tanto, se seleccionó como neotipo el ejemplar Ehrenberg 153 que coincide con la descrip- ción en el protólogo, coleccionado en el estado de Veracruz, donde esta planta es frecuente. Material adicional examinado. MÉXICO. Hidalgo: Jacala, Fisher 3762 (US); man Rancho Viejo, Fisher 46169 (US); Rte. 85, entre Tamazunc y Jacala, "aed Palomas, 39305 (MO); Rte. 85, we Tauqa, Jacala, cerca Palomas, Croat 39343 39343 (MO). Nuevo no >. o Pringle 1948 (MO, NY). Puebla: Pahuatlan, . Salazar s.n. (US 1169860). Pinal d Pas Ahuacatlán, R. He et (NY). fec Luis Potosi: Rio Verde, Orcutt 5423 (MO); minas de San — Purpus 5451 (MO). : iquihuana, rd. almillas, — 89] Veracruz: Santa d 9. Verbena gracilescens Ves Herter, Revista Sudamer. Bot. 4: 186. 1 n L. var. gracilescens . TIPO: Brasil. s.d., ru aquí designado, K no dido, K foto SI!). 937. Basónimo: Verbena ee Linnaea 7: Figura 5. Hierbas de aspecto grácil, erectas de 0.2-1 m, a veces decumbentes en la base, tallos glabros, al igual que las ramas y pedünculos de las florescencias, a veces escabrosos en las aristas. Hojas de lámina entera o las hojas basales tripartidas, los márgenes enteros o serrado-dentados, base en hacia un pecíolo hasta de 1 cm, n ambas cara venación no pronunciada. Sion Pa, e ramificación, formada por no superan la florescencia principal subsésil, flo- rescencias laxas, filiformes. Bráctea floral ovada, más breve que el cáliz, de 0.1-0.2 cm, glabra, margen piloso; cáliz de 0.16-0.24 cm, apenas pubescente con pelos cortos y adpresos, con 5 dientes triangulares breves, subconniventes en la fructificación; corola de color azul, violáceo, lila o blanco, infundibuliforme, breve ca. 0.3-0.55 cm, externamente glabra, pelos moniliformes en la garganta; estambres insertos hacia la zona apical del tubo corolino. Clusas de 1-1.5 mm, dorso longitudinalmente estriado poco marcado, cara comisural lisa a esparcidamente papilosa. Anatomía caulinar con parénquima clorofiliano de disposición continua, presencia de numerosos cordones de esclerénquima. Distribución y ecología. Verbena gracilescens se distribuye por Sudamérica, encontrándose en Argen- tina, Bolivia, Paraguay, Uruguay y sur de Brasil. Habita suelos fértiles y húmedos, se la encuentra creciendo en pasturas y a lo largo de caminos. Observaciones. Verbena gracilescens es fácilmente reconocible por su aspecto grácil y sus florescencias laxas, filiformes, con flores pequeñas poco evidentes. Es morfológicamente similar a V. officinalis, motivo por el cual Chamisso (1832) la consideró una variedad de ésta; pero V. officinalis se diferencia porque posee pelos glandulares en las piezas florales, además su rango de distribución es diferente, superponiéndose Ünicamente en Sudamérica de donde V. gracilescens es endémica. De la Peña y Pensiero (2004: 286) refieren para este taxón los nombres vulgares en Argentina: *yerba de Santa Ana, yerba de Santa María, yerba amarga". Este taxón se incluye en el grupo informal Verbena por presentar los caracteres definidos anteriormente para el mismo. Volume 97, Number 3 O'Leary et Revisión “. de Verbena Ss M Ta „AD. Verbena gracilescens va: var. Pe —A. Aspecto general eiim —B. Flor con bráctea. —C. oe posició! € swiftiana. ae Aspecto ees de la planta. Schwarz 6207 (NY). Tipificaciones : nomenclatura. El holotipo de Verbena officinalis var. gracilescens “E Montevideo misit Sellowius” ble 1832: 254) estaba depo- sitado en Berlín y el mismo fue destruido durante la oe Guerra Mundial. En K se encontraron . fjemplares coleceionados por Sellow en Brasil con n de estambres y ventral. — F. Flor con bráctea. 234 DA Cola s al. 24141 (SD; E.F de etiquetas e ex Berlín, isotipos a ionge destruido. > e y se , encuentra en buen estado de conserva- ción. Este oap poste una escritura en lápiz "V. *, pero este nombre no fue publicado. disais el ejemplar posee otra escritura Annals of the Missouri Botanical Garden en lápiz donde dice que podría ser un ups de V. var. gracilescens officinalis la aclaración (K, Lesley Wahinsham, comun. Pete). CLAVE PARA LAS VARIEDADES DE VERBENA GRACILESCENS NOROESTE Y NORESTE DE ARGENTINA, BOLIVIA, PARAGUAY, URUGUAY Y SUR DE BRASIL l. Hojas basales de lámina tripartida, las apicales de lámina entera, elíptica no angosta y margen serrado- A tad, n. . lic on £ m re tubo corolino hasta de 0.45 cm . 9a. var. gracilescens Y. Hojas basales y apicales de Me. entera, elíptico- n entero; florescencias hasta de 5 em en fructificación; tubo corolino geag a CASH o h ar. swiftiana 9a. Verbena gracilescens var. gracilescens. Fig- ura 5A-D Hierbas hasta de 1 m. Hojas basales de lámina tripartida, de 3 X 2 em, base angostándose hacia un pecíolo hasta de 1 cm, los márgenes serrado-dentados con dientes acuminados; las hojas superiores de menor tamaño y lámina entera, los márgenes serrados, ocasionalmente con 1 ó 2 dientes a cada lado en la base de la lámina, nunca márgenes enteros. Flo- rescencias de 15-20 cm en la fructificación; brácteas florales de 0.1-0.15 cm. Cáliz de 0.16-0.2 cm long., tubo corolino breve ca. 0.3(-0.45) cm. Nümero cromosómico. 2n — 42 (Schnack, 1942). Iconografía. Troncoso (1979: 234, fig. 105). Distribución y ecología. Esta variedad se distri- buye por el noroeste y noreste de Argentina, Bolivia, Paraguay, Uruguay y sur de Brasil. Se la encuentra en abundancia en el monte ribereño y en barrancas arenosas de ríos; crece como maleza en cultivos y campos de pastoreo, donde la vegetación natural es herbácea o arbustiva. Observaciones. En el noroeste argentino se en- cuentra una forma, que no merece valor taxonómico, qu enteras de margen inciso-dentado en la base de planta, no tripartidas (ej., Cabrera 241 x » SE Zuloaga & Deginani 3404, SI). La Figura 5A-D se basa en un ejemplar de estas características. Hooker (1829) se refiere a Perkosa officinalis var. x Gillies & Hook. ex Hook. (Bot. Misc. 1: 160. 1829. TIPO: Argentina. “In Pampas ad urbe ad Mendozam" [holotipo, G no visto] y V. var. B Gillies & Hook. ex Hook. (Bot. Mise. l: 160. 1829. TIPO: Argentina. “Apud Rio Saladillo, ad limites occidentales planitiei Pampas dictae, et ad margines aquarum in Provinciae Mendozae". . - neca usque - officinalis el rio del Sala: orilla western bound ar. B... Gillies [holotipo, K no visto; "iras K e sn. El análisis de los ejemplares citados evidencia que se trata de sinónimos de V. gracilescens var. gracilescens. Estos dos taxones variedad son nombres inválidos que no merecen validarse. Material adicional examinado. ARGENTINA. et Aires: Pdo. Gral Viamonte, Los Toldos, s.d., Crovetto s.n. (CTES). Catamarca: Dpto. El Alto, ibo Venturi 7160 (SI). Chaco: Dpto. Bermejo, Las Palmas Jorgensen 2467 (SI). Córdoba: Dpto. Colón, Ascoehinga; roncoso 316 (SI). Corrientes: Dpto. Bella Vista, Toropí, Schinini & Cristóbal 9865 (CTES, SI). Entre Ríos: Salto Grande, casa de Piedra, S. Renvoize 2944 (NY, SD. ormosa: Dpto. oe Ing. Juárez, Arenas fuic (SI). Jujuy: Dpto. Dr. grano, Laguna de Yala, Rodeo, a & E 3404 (SI); La Almona, ind et al. 24141 (SI). La Pampa: Dpto. Capital, Anguil, Steibei aa Biurrun & . Conesa, China Muerta, J. H. Hunziker 487 (CORD). Salta: Alva Gde., Venturi 5504 (SD; Dpto. Anta, San ud Saravia Toledo 1705 (SI). San Juan: - Valle Fértil, Usno, Kiesling 3071 (SI). San Luis: Dok. dedi. Ae Burkart 13997 (SI). Santa Fe: Dpto. 9 de Julio, Nochero, Pensiero & Faurie 3396 (SI). Santiago s finca Sarita, ca aye wierd 86 I Dpto. Robles, Lázaro, Maldonado 454 I). Chicligasta, E Burkart 26605 iy a: Luis Calvo, El Salvador, lag. y Saravia Toledo 13681 (CTES). Cochabamba: Krapovickas & Fuchs 6961 (SD. ae oe allero Marmori 1515 Menno, Arenas 439 (SI); Pto. Casado, Rojas 2526 (NY, SI). Concepción: Valle Mi, Kiesling et E 9770 (SI). P. i : Dpto. BOLIVIA. ba Pérez 2832 i: nte Hayes: Patifio, Schinini & — 25911 m. URUGUAY. Artigas: San ta Rosa uareim, Herter 1058 (SI). Cerro Largo: R apren Purse et al. IO (SD. Florida: Timote, Callinal et al. 2618 (SD. Poe 10 Oct. 1975, Marchesi 11338 (SI). San José: a, Frechard 9 (SI) Tacuarembó: Rivera, Cabrera & cam 32414 (SV). 9b. Verbena gracilescens var. swiftiana ann denke) N. O'Leary, comb. Basónimo Verbena swiftiana Moldenke, owiha 2: 427. 1948. TIPO: Argentina. Misiones: San Ignacio, 19 Sep. 1946, G. J. Schwarz 3402 (holotipo, S no visto, S foto SI!; isotipos, NY no visto, NY foto SI!, SI!). Figura 5E, F. Hierba hasta de 30 cm, muchas veces de base subleñosa, de "pete ulii. Hojas pequeñas ca. 2 cm; lami liptico-angosta y margen entero, base subpeciolada. Resin hasta de 5 cm en la fructificación, terminales, solitarias o reunidas en paracladios trímeros; brácteas florales de 0.15- 0.2 cm. Cáliz de 0.2-0.24 cm; tubo corolino de 0.45- 0.55 em. Volume 97, Number 3 O'Leary et al 2010 Revisión Taxonómica de Verbena acilis. Aspecto general de la planta. —B. Flor con bráctea. —C. Cáliz fructífero con bráctea. A de Din 8411 KN B. C de Pau 6539 (US). den y ecología. Esta variedad presenta : note restringida al noreste de Argentina n la provincia de Misiones y sur de Brasil en el estado de Rio Grande do Sul la La variedad swiftiana se diferen- la variedad tipo por las flores más grandes y las 2 más pequefias, de lámina poco desarrollada, as veces de aspecto subafilo. Pe (1948) describe Verbena swiftiana como x taxon de aspecto gracil, de hojas pequefias y orescencias breves con flores remotas. El análisis de material de io no permite distinguir dicha : entidad E nivel específico, haligndose una — Continua en los cara > Argañarás 86, SI; Arenas 439, Sl; Venturi 5504, hoj tpa 69, SI). Sin embargo la presencia de ile de margen liso y las florescencias nunca | — de 5 cm, referidos por Moldenke (1948: 427) propios del taxón V. swiftiana, siempre se a ionados entre sí. Consecuentemente, en ; | presente trabajo se incluye V. swiftiana bajo la sinonimia de V. gracilescens, reteniendo una dife- rencia a nivel varietal. ARGENTINA. Mi- E (NY). B Oliva, B. eom 30975 cet 10. Verbena gracilis Desf., Cat. Pl. Horti Paris., ed. 3: 393. 1829. TIPO: “Verbena gracilis herb paris”, s.d., s. coll. (holotipo, FI no visto, FI foto SI!, FI foto P!). Figura 6. Verbena remota Benth., Pl. Hartw. 21. 1839. TIPO: México. — “in arvis, 1839", K. T. (holotipo, K no visto, K foto SI!; isoti isto, N no visto, NY foto SI!, P 00371001 no visto, P 0037100 foto SI!, SI!). arizonica À. Gray, Proc. Amer. Acad. Arts 19: 95. arizonica 1883, non Ve .. Annuaire Conserv. Jard. Bot. Ve erbena Geneve 10: 102. 1907. TIPO: E.E. U.U. Annals of the Missouri Botanical Garden Arizona: near Fort Huachuca, 1882, J. G. Lemmon 2858 (holotipo, GH no visto, GH foto SI!). erba o sufrútice hasta de 40 cm de altura, de más glabros. Hojas de 1-3 X 1-1.5 cm, pecioladas, lámina dividida, pinnatipartida a pinnatisecta a veces trilobada con dos lacinias basales oblongas de ápice agudo y lóbulo central mayor, dividido, base cuneada, ápice agudo, margen revoluto variablemente inciso- dentado; cara abaxial con pelos híspidos o estrigosos y cara adaxial con pubescencia escabrosa uniforme, con pelos glandulares. Sinflorescencia frondosa, formada por paracladios laxos, los basales no sobrepasan al terminal, florescencias de 8-12 X ca. 0.5 cm, las flores densamente imbricadas en antesis, distanciadas en fruto. Brácteas florales conspicuas, las basales foliáceas, reduciéndose a medida que se aproximan al ápice de la florescencia, las apicales de forma ovado- angosta a sublinear, de longitud muy variable desde 0.3 cm hasta A —— d un hoja pequeña ca. 1.5 cm, con ciliado con pel ] Jul áliz d que las brácteas, de 02-03 cm con nbaciadí híspida, algunos pelos glandulares, con 5 dientes triangulares breves, subconniventes en la fructifica- ción; corola de color azul, lila o rosa, infundibuli- forme, tubo corolino ca. 0.4 cm, angosto, glabro externamente, pubescente en la garganta, limbo esarrollado, estambres insertos hacia la zona media del tubo corolino. Clusas de 1.5-2 mm, dorso reticulado, cara comisural lisa o papilosa. Anatomía caulinar con parénquima clorofiliano de disposición continua, presencia de umerosos cordones de esclerénquima 120 E miar m Distribución y ecología. Verbena gracilis se la encuentra en México y sudoeste de Estados Unidos de América, en los estados de Arizona y Texas. Crece en ambientes disturbados, terreno arenoso-limoso, ped- regoso con vegetación matorral, o pastizal degradado. Observaciones. Verbena gracilis muchas veces posee uno o dos nudos con hojas opuestas luego remata en la florescencia, donde las brácteas florales scens; Perry (1933 les sobre la base de las brácteas florales, la morfología foliar y también la pubescencia (véase observaciones bajo V. canescens). Verbena gracilis se reconoce por sus brácteas florales foliosas y sus clusas pequeñas de dorso reticulado en toda su superficie. Existen ejemplares como Pringle 9135 (MO) con escasa pubescencia, y otros como Correl 21530 (MO) muy pubescentes. , Este taxón se incluye en el grupo informal Bracteosae por presentar los caracteres definidos anteriormente para el mismo. Tipificaciones nomenclatura. Según Perry (1933: 300) TA gracilis fue descripta por Desfontaines a partir de un ee cultivado en el “Jardin des Plantes de Paris” y probablemente depositado en P. El único s i. que se ha hallado en P bajo este nombre es P 00307089, que posee una etiqueta que dice isotipo. Pero este ejemplar no puede ser un isotipo ya que es un ejemplar del herbario de E. Cosson donado a París por su bisnieto, el Dr. Durand, en 1904, fecha muy posterior a la fecha en que Desfontaines publicó su especie. Rzedowski y Rze- dowski (2002) dicen que el tipo de V. gracilis es un ejemplar que perteneció al herbario Desfontaines que se encuentra depositado en FI. l examinado. E.E. U.U. Arizona: Blumer 1612 (NY). Texas: Jeff Davis Co., Davis Mtns., erg 14346 . MÉXICO. Chihuahua: 12 mi. E Parral, Rte. 45, Correll rs (MO). Coahuila: 5 km NE Jimulco, Standjord et al. 126 (NY). Distrito Federal: Villa de Obregon, Fisher 35208 ME US); Pedregal, Pringle 6539 (MO, US); Tizapan, lava fields, Pringle 9135 (MO). : Coyotes, hacienda, 63 mi. Durango, Maysilles 7497 (NY); 56 km W Durango, Detling S). Guanajua ó rial Chiricahua Mtns., e, 2 (MO). Gue Tinajas, Hinton 5847 (NY, m Hidalgo: Huichapan, 4 km N Huichapan, hacia ‘Tecozautla, Hernández Maga (MO). Nuevo I Mueller 2392 (MO). San Luis Fotosi: Salinas Hi E Veraeruz: Perote » Valsequi o, SI). Zacatecas: 9.7 mi. NW Chauhtemoc, Taylor 5945 (US). 11. Verbena halei Small, Bull. Torrey Bot. Club 25: 617. 1898. Verbena officinalis subsp. halei (Small) S. C. Barber, Syst. Bot. 7(4): 454. 1982. Verbena officinalis var. halei (Small) Munir, J. Adelaide Bot. Gard. 20: 93. 2002. TIPO: E.E. .U. Louisiana: s. loc., s.d., J. Hale 245 (lectotipo, designado por Moldenke [1963c: 162], NY no visto, NY foto SI!). Figura 7. Verbena leucanthemifolia Greene, Pittonia 5(27): 1 1903. TIPO: E.E. U.U. Texas: Taylor Co., Abilene, 19 May 1902, S. es EN 7996 (holotipo. NDG foto SI i no visto, NY foto SI!, TEX no visto, TEX foto SI!, US no visto, US foto SI!). arego var. gaudichaudii Briq., Annuaire Con- sery. . Genéve 10: 105. 1907, syn. nov- Volume 97, Number 3 O'Leary et al. 387 2010 Revisión Taxonómica de Verbena j A say, Bug d y i — š zz | O. : Detalle de pubescenci del tallo. ies T. Verbena halei. —A. Aspecto general de la planta. —B. Flor con as ct a eN "EC de Nee & Taylor 26747 (NY). Annals of the Missouri Botanical Garden Verbena gaudichaudii (Briq.) P. W. Michael, Telopea 7(3): 295. 1997. TIPO: Australia. New South Wales: Sydney, Port Jackson, s.d., C. Gaudichaud Beaupré 144 (holotipo, G no visto, G foto SI!). Ë roseiflora Verbena officinalis Benke, Rhodora 35: 45. 1933, syn. nov. Verbena halei f. roseiflora n mn Phytologia 1 940. TIPO: Pan U.U. = Kleberg, Kingsville, (holotipo, F no visto, F foto SI; nii i no visto, TUS foto SI!). Verbena halei f. parviflora "s e 34: 20. 1976, syn. nov U.U. Texas: Galveston Island, State m M. C. Johnston 12436b (holotipo, TEX no v TEX foto SI!; isotipo, NY no visto). Hierba grácil, erecta, raramente postrada, de 20— 120 cm; tallos ramificados a veces desde la base, glabros o algo pubérulos hacia el ápice con pelos adpresos breves, a veces pelos glan dulares breves y a a b ] is de la i ojas variadas en cuanto a forma y tamaño dentro de la misma planta, de 5-12 X 0.4-2.5 cm, pubescencia subestrigosa, adpresa en ambas caras, más marcada sobre las venas de la cara abaxial; las hojas basales generalmente de lámina entera, elíptico-oblonga; las hojas medias de lámina tripartida, trisecta o irregu- larmente pinnatisecta, margen profundamente inciso- dentado con dientes de ápice agudo, base atenuada hacia un pecíolo de 1.5-3 cm; hojas apicales de lámina sublinear a linear. Sinflorescencia frondosa, hojas del raquis lineares, formada por paracladios trímeros laxos, mayor a un orden de ramificación, florescencias laterales no superan la principal, filiformes, de 20(-25) X ca. 0.35 cm en fructificación. Brácteas florales ovadas, de ápice agudo, general- mente menores que el cáliz, de 0.15-0.28 cm, con escasa pubescencia adpresa y margen piloso; cáliz de 0.22-0.35 cm, pubescencia con 5 dientes triangulares muchas veces de coloración violácea, no conniventes en la fructificación; corola de color azul, violáceo, lila o blanco, infundibuli- forme, tubo corolino de 0.4-0.65 cm, pubescencia externamente pilosa, pelos moniliformes en la gar- ganta, limbo de 0.4(-0.6) cm; estambres insertos hacia la zona apical del tubo corolino. Clusas de 2-2.3 mm, dorso longitudinalmente A cara comisural lisa o ligeramente verrucosa. parénquima clorofiliano E di presencia de numerosos natomía caulinar con Sposición continua, cordones de esclerénquima. = 7, 2n = 14 (Dermen, r cromosómico. 1936; Lewis & Oliver, 1961), Iconografia. Michael (1997: 295, Verbena gaudichaudii); Diggs et al. (1999: 108); Felger (2000: 456): fig. 2 “apps Munir (2002: " oe (como V. officinalis var. ar. gaudichaudii). 9 Distribución y ecología. Verbena halei habita el sur de Estados Unidos de América y norte de México; Gibson (1970) la cita en la Flora of Guatemala y Munir (2002) refiere ejemplares para el este de Australia, donde sería un taxón introducido. Crece en áreas poco elevadas, con suelo arenoso, salino o alcalino; también en laderas montañosas y en terrenos aluvionales; muchas veces m una maleza a orillas de rutas y campos de cultivo. Observaciones. Se han observado ejemplares que poseen en la base hojas de lámina entera dispuestas de forma pseudo-arrosetada y la inflorescencia ificada, con numerosos paracladios partiendo de un único tallo, como por ejemplo en McAtee 1953, US y Hardin 531, US Verbena halei es morfológicamente afín a V. menthifolia, ambas se diferencian principalmente por la morfología foliar siendo en V. halei las hojas basales generalmente de lámina entera, las medias de lámina tripartida, trisecta o irregularmente pinnati- linear; y en V. menthifolia las hojas son homomorías, de lámina tripartida, trisecta o pinnatipartida. Moldenke (1958) sugiere que Verbena halei y V. officinalis serían piqpa d w un mismo PA basándose en la exi Sin embargo, a partir del estudio del matesal de herbario no se encuentran ejemplares intermedios que sugieran híbridos. Barber (1982 : A51) trata V. halei como subespecie de V. Qm Munir (2002) la trata como cdo de V. officinalis. En el presente Pond siendo que V. halei no posee pelos glandu- lares, lo cual es un carácter distintivo de V. officinalis. El análisis del ejemplar tipo de Verbena leucanthe- mifolia permitió verificar que posee las mismas características morfológicas que V. halei, con las hojas superiores reducidas; Perry (1933) fue la primera en tratar ambos taxones como sinónimos. Moldenke (19402) consideró a Verbena officinalis f. roseiflora como una forma de V. halei f. roseiflora, diferenciándola de la forma tipo por el color de las flores (Moldenke, 1963c: 175). El análisis del m tipo evidencia que la misma es un sinónimo V. halei, ve el color de las flores un carácter ees z e no tegoría taxonómica. addens (1976) caracteriza la forma parviflora por el limbo corolino reducido, ca. 3 mm en la antesis. Las medidas observadas en el ejemplar tipo se correspon- den con el rango de variación específica que puede encontrarse en Verbena halei, por lo cual esta forma se trata como sinónimo de V. halei. Según el protólogo del taxón Verbena halei Í albiflora de Davis (1945) éste ánicamente difiere de Volume 97, Number 3 2010 O'Leary et al. Revisión Taxonómica de Verbena la forma tipo por el color blanco de las corolas. No se ha localizado el ejemplar tipo del mismo, citado por el autor para Estados Unidos de América en el estado de Texas, Brooks Briquet (i602... efine Verbena officinalis var. gaudichaudii diferenciándola de V. officinalis var. officinalis por sus hojas angostas, elongadas, profun- damente inciso-dentadas, las superiores lineares, paucidentadas. Michael (1997) la eleva a rango específico como V. gaudichaudii. Munir (2002) la trata como variedad de V. "e al igual que V. halei como V. officinalis var. halei; diferenciando ambas variedades de la ae officinalis por la pubescencia inconspicua y glandulosa. Munir (2002) separa la vari gaudichaudii de la variedad halei por el grado de división de las hojas y la longitud relativa de la bráctea floral y el cáliz. En el presente tratamiento V. gaudichaudii se trata bajo la sinonimia de V. halei, siendo que el tipo de hojas descritas para V. gaudichaudii no difieren de las de V. halei al igual que las dimensiones de las brácteas y el cáliz. Este taxón se incluye en el grupo informal Verbena por presentar los caracteres definidos anteriormente para el mismo Material adicional examinado. E.E. U.U. : Barbour Co., 0.4 mi. NE rd. 57, Gil 2001121 (NY). Arkansas: S 67 & 1-30 at Fulton Exit, Thomas . Florida: Dixie Co., US 27, 1/2 mi. i MO). : _ Macintosh Co., Sapelo : : Cameron Co., near Cameron, McAtee 1953 (US); Parish Webster, e Thomas 138391 (MO, N ippi: Forrest Co., 8 mi. SŠ McDaniel 3501 (NY). Oklahoma: mone Co., N Lake Texoma, 1 mi. W Willis Dam, Nee et al. 44021 (NO, NY, South : Aiken Co., 3 mi. NE North . Ellison 1010 (NY). Texas: Houston Co., Houston, n grounds, Hardin 531 (US). MÉXICO. Coahuila: 2 km SE estación H Wendt et al. 10147 (MO, NY). México: HW 57, 30 mi. -= tollgate cerca Queretaro. et al. 99 (MO). Nuev : Monterrey, Frye 1 Frye 2474 (US). 341 (MO); 20 mi. S La Springs, Skehan 109 (MO); Tochik, cerca Vigueta, Nee & Taylor 26747 (NY). 12. Verbena hastata L., Sp. Pl. 1: 20. 1753. TIPO: shm Roy. Lugdb. 327 (lectotipo, aquí d designado, L 0141996 no visto, L 0141996 foto ). _ Verbena pinnatifida Lam. , Tabl. Encycl. 1: 57. 1791. Verbena var. pinnati .) Pursh, Fl. Amer. Sept. (Pursh) 2: 416. 1814. TIPO: E.E. U.U. “ex Ameri. _ Septentrionali”, P no visto, P foto s.d., s. coll, (holotipo, js ipee, P no visto, P foto SI!, SI). Verbena paniculata Poir. en Lam., Encycl. 8: 548. 1808. Verbena hastata var. paniculata (Poir.) Farw., Rep. (Annual) Commiss. Parks Boulevards Detroit 11: 82. 1900. TIPO: E.E. U.U. Amerique septentrional n° 240 (holotipo, P no visto, P foto SI!; isotipo, SI!). Verbena hastata f. albiflora Moldenke, Amer. Midl. Natural- ist 24(3): 752. 1940, syn. nov. E.E. U.U. jen York: Wyoming Co., Attica, 8 Aug. 1888, E. J. Hi 91888 (holotipo, ILL no visto, ILL foto SI!; isotipo, m no visto). Verbena hastata var. scabra Moldenke, Phytologia 9: 283. 1963, syn. nov. TIPO: E.E. U.U. Oregon: Hwy. 81, N Modoc-Lassen Co. line, 11 Aug. 1947, L. Mason 13502 (holotipo, UC no visto, Verbena hastata f. caerulea Moldenke, dw Midl. Naturalist 10(6): 490. 1964, syn. nov. TIPO: Canada. Ontario: ssex Co., Amherstburg, 28 Aug. Ls - Moldenke 1043 (holotipo, TEX no visto, TEX foto Hierba perenne, erecta, hasta de 1.5 m de altura, ramificada en la parte apical, tallos de pubescencia variable con pelos hirsutos, estrigosos. Hojas de lámina entera, de 7-10(-15) X 2-3(-4) cm, ovado- elongadas, las basales muchas veces de lámina hastada, trilobada a tripartida hacia la parte proximal de la misma, ápice agudo, base cuneada, pecíolo de 1-2(-3) cm, margen entero a irregular- mente inciso-serrado a biserrado, dientes acumina- dos, cara superior subglabra a adpreso-estrigosa con pelos cortos, poco densos, cara abaxial con pubes- cencia escabrosa sobre venas, a veces con algunos pocos pelos glandulares. Sinflorescencia bracteosa, florescencias reunidas en paracladios multímeros, laxos, hipotagma Sa laterales no su: i cilíndricas densas, k 5-10(-15) X 0.4-0.5 cm, igual o de menor longitud que el cáliz, con margen piloso, subglabro en el dorso; cáliz de 0.2-0.3 cm, con pubescencia adpreso-estrigosa, con 5 dientes triangulares de 0.5 mm, subconniventes en la fructificación; corola de color azul, violeta, lila o blanco, infundibuliforme, tubo corolino de 0.35- 0.5 cm, villoso externamente, con pubescencia de pelos moniliformes en la garganta, limbo poco desarrollado; estambres insertos hacia la zona apical T rm longi > estriado, cara comisural lisa, a veces caló escamosa. Anatomía caulinar con parén- quima clorofiliano de disposición continua, presencia de numerosos cordones de esclerénquima. úmero cromosómico. n = 7 (Noack, 1937); 2n = pre 1934; Dermen, 1936; Noack, 1937; Löve, 19820: 353). Iconografía. on y Brown (1913: 95); Jepson (1943: 381, fig. e Gleason (1952: 130). Distribución y ecología. El área con mayor número de representantes de este taxón es el sudeste de Canadá y noreste de Estados Unidos de América, en la zona de la cuenca de los grandes lagos; sin embargo su distribución llega hasta la costa oeste en el estado de Oregón y en el sur hasta los estados de Nuevo México y Texas. Se la encuentra en terrenos húmedos o pasturas. Observaciones. Según Perry (1933) Verbena has- tata tiene tendencia a hibridizar con algunos taxones en la región central de Estados Unidos de América, lo cual genera gran variabilidad en la densidad de las florescencias y en su profusión. Perry no encontró ninguna ión que variara en una dirección en particular y que justificara la existencia de categorías taxonómicas infraespecíficas para referirse a las mismas. Moldenke (1940b, 1964) describe las formas por lo cual ambas formas se consideran sinónimos de la forma tipo. En 1874 Coleman describe Verbena hastata var. rosea Coleman para el catálogo de la península de Michigan, diferenciándola de la variedad tipo por el color rosado de las flores. Sus ejemplares tipo se encuentran en BM y/o K, pero en estos dos herbarios no se ejemplares tipo de este taxón. La descripción en el protólogo de Verbena hastata var. ellongiflia Nutt. (Nuttall, 1819) se > besó en la observ lo cual en los berherios consultados como PH y LINN no se encontró ningún ejemplar. Nuttall (1818) la diferencia por poseer hojas oblongo-lanceoladas pro- fundamente serradas, de ápice agudo y florescencias paniculiformes, con flores pequeñas, color celeste. Moldenke (19634) funda la variedad scabra ined renciándola por poseer las hojas rígidas, mente escabrosas en la cara adaxial. El snilinis del del material tipo permite determinar que se trata de un sinónimo de Verbena hastata, siendo la pubescencia de las hojas, y rigidez de las mismas un carácter muy variable dentro de as oe, Fate taw ir info 1H por presentar los caracteres definidos anteriormente para el mismo. amarra awa la e LE los fines de | ut. designar un Annals of the Missouri Botanical Garden ejemplar a una lámina, como podría ser la lámina 242 Hermann mencionada en el protólogo. Se con- sultaron los herbarios H, SBT (Lars Gunnar Reinham- mar, comun. pers.), UPS (Mats Hjertson, comun. pers.) ra no se loin. witexisi original. En Leiden (D) dos ejemplares de van Royen: Heb. A. van Royen 913.30-210 y 913.30-198. Este último posee una etiqueta donde se lee: Roy. Lugdb. 327, por lo cual este ejemplar es designado lectotipo. Los ejemplares BM 000557563 (foto SPD y de LINN 35.12 (foto SI) podrían ser material original, pero se considera más correcta la elección del ejemplar de Leiden dado que en el protólogo no se hace ninguna referencia hacia estos ejemplares de BM y LINN. Charlie Jarvis, del Linnaean Plant Name Typification Project apoya esta elección. Material adicional examinado. CANADÁ. Ontario: cerca Ottawa, Macoun 81042 (NY). Quebee: Granby, Fabius 409 (NY). E .E. U.U River, Eastwood 41 (SI). Idaho: Nez Perce Co., Clearwater, Foster 1 NY). Mlinois 81 St., Chicago, (MO). ck Co., .8 mi. E Free 1933, Tolstead s.n. (MO 1225655). Kansas: & 9702881 (NY). Massachusetts: West Lynn, 26 July 1911, H. Davis s.n. (NY). Michigan: “saqin ee Co., Stephenson, Hyypio 2475 (NY). Minnesota: Becker Co., Itasca park, De Soto Lake, Grant 3073 (MO, NY). Missouri: . N Warrensburg, : Hillsboro Co., mack, Moldenke 19024 (SI). New Jersey: Somerset “sp Ner Moldenke 1339 (NY). New Mexico: Socorro Co., Mulecreek, Crain Bras Ranch, 14 July 1900, Wooton s.n. (US 562248). New York: Ontario Co., Geneva, Moldenke 20434 (MO). North Kent Co., Nooseneck oldenke 19038 (SI). Texas: Hemphill Co., m river toms, Cory 50298 (US). Utah: Utah Co., W Utah lake. betw. Goose & Pelican Points, 20 Sep. juo. 'elsh 684 (NY). Virginia: Clarke Co., Rte. 611, Artz € Krouse 57 (NY). Wisconsin: Richland Co., Richland center, Nee 43765 (SD. 13. Verbena lasiostachys Link, Enum. Hort. Berol. Alt. 2: 122. 1822. TIPO: E.E. U.U. California: Lake Co., Mt. Sanhedrin, 19 July 1902, 4. 4- Heller 5919 (neotipo, aquí designado, SI!). Greene, Pittonia 3: 309. 1898, TIPO: E.E. U.U. Colon Marin Co., Point pe el E shore and Pt. Tiburon, 20 July 1891, E. L m NDG oto SI lasiostachys var. se > Naturalist 24: 753. 1940, syn. nov. Verbena Volume 97, Number 3 2010 O'Leary et al. 391 Revisión Taxonómica de Verbena f. —— — Moldenke, Phytologia 44: 328. . TIPO: . California: Monterey, Aug. E 5. B. It. 1 s (holotipo, RSA no visto, RSA foto SI!; isotipo, UC no visto). Verbena lasiostachys var. n eme Amer. idl. Naturalist 24: 753. 1940, Verbena lasiostachys f. septentrionalis Moldenke) "Moldenke, Phytologia 44: 328. 1979. TIPO: E.E. U.U. Oregon: Jackson Co., Medford, Aug. 1922, C. C. Epling 5445 (holotipo, LA no visto, LA foto SI!). erbena lasiostachys f. albiflora Moldenke, Phytologia 9(7): 465. 1964, syn. nov. TIPO: E.E. U.U. California: San Mateo Co., 2 June 1914, L. R. Abrams 5109 (holotipo, CAS no visto, CAS foto SI!). Hierba erecta o algo decumbente en la base, hasa de 1.5 m altura, muy ramificada hacia el ápice, de aspecto robusto, con pubescencia híspida, densa con algunos pelos glandulares. Hojas de 3-10 X 2-4(-6) cm, de lámina trilobada con dos lóbulos basales y lóbulo central elíptico, margen irregular- mente serrado-dentado con dientes acuminados, ápice o base cuneada, pecíolo ancho hasta ambas caras híspido-pubescentes, con B plo pose la venación reticulada en la cara al. Sinflorescencia frondosa, formada por Bi rasa trimeros a multimeros, florescencias laterales no superan la principal, florescencias de 10-25 X ca. 0.6 cm, densas, flores y frutos densamente imbricados. Brácteas florales ovado- angostas de 0.25-0.35 cm, margen ciliado; cáliz de 0.3-045 cm con 5 dientes agudos de 1 mm, evidentes, subconniventes en la fructificación, pubescencia hispida, muchas veces con pelos glandulares; corola de color lila, tubo corolino de 0.5-0.7 cm, limbo 03-0.5 cm lat., con pubescencia corolino. Clusas de 2 mm, dorso longitudinalmente estriado, cara comisural papilosa. Anatomía caulinar con parénquima ans de disposición conti- nua, presencia de n cordones de esclerén- quima. onografía. Wilken (1993: 1093); Gleason (1952: u, nc (1943: 381, fig. 420). ión y ecología. Verbena lasiostachys se da en el oeste de Estados Unidos de América, en los estados de Oregón y California. Observaciones. Verbena lasiostachys se asemeja a V. cloverae en cuanto al tipo y tamaño de las flores y la morfología foliar, pero se diferencia porque y. lasiostachys son plantas de porte — muy Pubescentes con pelos híspidos hasta de 1 mm y florescencias densas. Verbena cloverae es un taxón endémico de Texas, y V. lasiostachys crece única- ente en California y pops Perry (1933) diferencia Verbena robusta de V. lasiostachys por el tipo de pubescencia y la longitud relativa de las brácteas florales. A partir del análisis del ejemplar tipo y de la descripción de ambos taxones en los protólogos se verifica que no existen tales diferencias morfológicas por lo cual V. robusta se trata como sinónimo de V. lasiostachys. LN n n E veined septentrionalis | nah r m 4.4 cm, + 45 1 tá d tro D PANE. M LA YAUIUCIIN! en ei d jener. “trabajo $ ne MM rm su Hin. ` i E k a ING ES L Er t en la cara adaxial de las hojas maduras, carácter que no justifiea el establecimiento de este taxón infra- específico. En 1964, Moldenke funda la forma albiflora para "- "e a ejemplares con | eve siendo el color de la corola un carácter taxonómica- mente irrelevante (Moldenke, 1964a). Jepson (1943) funda Verbena lasiostachys var. abramsii (Moldenke) Jeps.; este taxón se trata de es un iibi de ` neoteesicans var. hirtella L. M. 22. a ns taxón) A Perry (véase ba : Este taxón se inch en el grupo informal Hastatae por presentar los caracteres definidos anteriormente para el mismo. Tipificaciones y nomenclatura. Schauer (1847) y Perry (1933) son los primeros autores en tratar Verbena lasiostachys de 1822 y V. prostrata R. Br. (Brown, 1812) como sinónimos, aceptando como válido V. prostrata, que sería anterior en imo por (Savi, 1802; McNeill et al., 2006: Art. 53), sinónimo de V. bracteata Lag. & Rodr. Por lo tanto el nombre válido de este taxón es V. lasi hys Link. ; En el protólogo de Verbena lasiostachys Link dice “Habitat in California” como única referencia al mai is aaa ee ee a “ E e menciona la x de un jemplar de Verbena prostrata en no se noni este material (Lesley BM comun. pers.). Maid Í Uv. California: A ? : . Monterey reservation, Cook 140 (SI); Sonoma Co., W of e near Russian River, Hele 5785 (BAF). ‘Dryden, Piper 6160 (US). NE OM LE ARAS AR MS ON š x T x ———— nC ceruice MEE MEME MICI II ICI TT Annals of the Missouri Botanical Garden 14. a macdougalii A. Heller, Bull. Torrey Bot. Club 26; 588. 1899. TIPO: E.E. U.U. Arizona: near Flagstaff, 8 July 1898, D. T. MacDougal 249 (holotipo, NY no visto, NY foto SI!; isotipos, BKL no visto, GH no visto, GH foto SI! UC no visto, UC foto SI!, US no visto, US foto SI!). Figura 8C, D. erbena macrodonta L. M. Perry, Ann. Missouri Bot. Gard. 20- 289. 1933, nov. .E. U.U. California: La Laguna, 750 m, 20 Jan. 1906, E. W. Nelson & E. A. Goldman 7. i visto, MO foto SI! isotipo, US no visto, US foto Alamosa Canyon, 14 Sep. 1938, F. ro 16847 (holotipo, COLO 42339 no visto). Hierba perenne, erecta, de 03-1 m de altura, tallos ascendentes, ia densa hirsuta, pilosa, pelos Hojas de lámina entera, ovado-angosta, de 6- 10 X 2-3 cm, sésil a subsésil de base subcuneada, ápice agudo, margen inciso-biserrado, rugosas, grue - sas, — híspido-estrigosa en la cara adaxial meros, mayor a un orden de ramificación, las florescencias laterales no superan a la principal, I de 10-20 X 0.8-1 cm, pedunculadas flores densamente imbricadas en la antesis, faros remotos en la fructificación. Bráctea floral elíptico- angosta de ápice agudo, de 0.4-0.65 cm, de mayor longitud que el cáliz, margen ciliado; cáliz de 0.4— 0.5 em, con 5 dientes subulados de 1 mm, sub- conniventes en la fructificación; pubescencia híspido- estrigosa en ambas piezas, con abundantes pelos glandulares breves; femps de color purpúreo, violeta, e 9 blanco, infundibuliforme, tubo corolino de 0 6 cm, angosto, externamente pubescencia monili m aT "d ve NEAR asa ces Distribución y ecología. Se oe sudoeste de Estados Unidos de América, en los estados de Arizona, Nuevo México, Utah, Colorado Colorado y California, Wyoming y sur de vedete ck nabo rocoso, arenoso y árido. Observaciones. Verbena macdougalii es similar a V. stricta Vent. diferenciándose ésta última por las hojas eliptico-orbiculares en vez de ovado-angostas, las florescencias menos densas y mas anchas, las E S sS n 1 Al ek ] » que el cáliz, en lugar de sobrepasarlo notoriamente; la pubescencia de las piezas x no glandular o a veces con algunos pelos glandulares, siendo siempre pubescencia glandular conspícua en ugalii. Moldenke (1948) diferencia la ied albiflora por poseer corolas blancas, pero este carácter es muy variable habiendo ejemplares con corolas violetas oscuras, azules (Harrington 9667, MO; Lewis 5530, MO) hasta blancas (Spellenberg 2082, NY), por lo tanto taxonómicamente irrelevante. Se han encontrado determinaciones de Moldenke en ejemplares de herbario (Wooton s.n., US 736877) como V. macdou- galii f. albiflora, donde se basó en el color blanco de las corolas del ejemplar montado, pero sin indicarse este color en la etiqueta del mismo. Perry (1933) funda Verbena macrodonta y la diferencia de V. macdougalii porque presenta el hábito menos erguido, la pubescencia calicina más glandular y los frutos más remotos. Perry sólo menciona la colección tipo y no se han coleccionado más ejemplares con tales características, el análisis del mismo evidencia que se trata de un sinónimo de V. macdougalii. Este taxón se incluye en el grupo informal Hastatae por presentar los caracteres definidos anteriormente para el mismo. Material adici. examinado. E.E. U.U. Arizona: Apache Co., yde S rte. 60, Lehto et al. 11506 (US); Coconino Co., Kaibab Plateau, Grand Canyon, H 4691 (US); Coconino Co., MO). Barker 565 (MO). New Mexico: Colfax Co., $a mi. W Ute along Hwy. 64, Lr mig e Otero Co., 3 1/2 mi. W Cloudcroft, cerca Co., 5.6 mi. NW Cl MEE IN Otero Co. Sacramento Mins., Fresnal, 21 July 1899, Wooton s.n. (US 136871). Utah: Utah Co., Mammoth Crun, Jones 6026 (MO, CS Laramie Co., Platte Canon, Nelson 8354 15. Tui menthifolia Benth., Pl. Hartw. 21. 839, sphalm. “menthae : México. "iei 1839, K. T. Hartweg 175 dbilalipo, K no visto, K foto SI!; isotipos, NY no visto, NY foto SI!, P no visto, P foto SI!, SI!). Figura 9. & Galeotti, Bull. Acad. Roy. Sci. Bells i 321. 1844. TIPO: México. Hidalgo: REN enn. de Sabino y de Izmiquilpan. eo 778 (holotipo, K no visto, K foto domingensis Urb., Symb. Antill (Urban) 5: 484 1908, syn. nov. - TIPO: República Dominicana. Santo Volume 97, Number 3 2010 O'Leary et al. Revisión Taxonómica de Verbena B. Flor con bráctea. C. D. Verbena macdougalli. D de Holmgren 4691 (US). EG A, B de Mearns 525 (U pe A, B. Verbena stricta. —A. Aspecto general de la planta. pecto general de la planta. —D. Flor con bráctea. Figura 8. —. 394 Annals of the Missouri Botanical Garden Figura 9. Verbena menthifolia. —A 5 s - —A. Aspec bráctea. A-C de Sharp 44326 (NY) specto general de la planta. —B. Detalle de pubescencia del tallo. —C. Flor con Volume 97, Number 3 2010 O'Leary et al. 395 Revisión Taxonómica de Verbena Domingo, ad Angostura del Río Yaque, 8 May 1887, E F. A. Eggers 1828 (lectotipo, - designado, NY visto, NY foto SI!; isotipos, M no visto, US 00940047 no visto, US 00940047 foto SI!, WU n no visto, WU foto SI!). pos, GH no visto, MICH no visto, MICH foto Sm. s no visto, TEX foto SI!, US no visto, US foto SI!). Verbena comonduensis Moldenke, Phytologia 18: 343. 1969, syn. nov. Verbena menthifolia var. comonduensis (Moldenke) Moldenke, Phytologia 46: 155. 1980. TIPO: México. Baja California: Comondu, 19 Mar. 1969, A. R. Moldenke & A. B. Moldenke 2922 (holotipo, TEX no visto, TEX foto SII). erbena domingensis f. foliosa Moldenke, Phytologia 34: 19. 1976, syn. nov. TIPO: Repüblica Dominicana. Peder- nales, near Canote, ca. 5 mi. W of Aceitillar, Baoruco Be . 1969, A. H. Liogier 16846 , NY no visto. NY foto SI!; ep US no visto, o. US foto SI!). Verbena domingensis var. cubensis stg kien 50: 1982, syn. nov. TIPO: orido, 13 e 1905, A. H Curtiss 677 dia ipo, NY. no dss NY foto SI!; isotipos, F no visto, M no visto, SI!, US no visto, US foto SI!). Hierba erecta de 60—140 cm, p d la base; pubescencia variable, subglabra estrigosa hacia el ápice. Hojas de ape awaq tripartida, trisecta o pinnatipartida, de 3-8 X 0 3 cm, margen irregularmente inciso-dentado, ans agudos, base cuneada, pelos estrigosos breves y poco densos sobre la cara adaxial, más densos y adpresos Sobre las venas de la cara abaxial. Sinflorescencia bracteosa, formada por paracladios laxos, mayor a un orden de ramificación, florescencias laterales no superan a la terminal, filiformes, de 7-20(-30) x ca. infundibuliforme, mbo corolino 0.3-0.45 cm, an- 80sto, externamente subpubérulo, internamente pu- e, garganta con pelos moniliformes, limbo Poco desarrollado; estambres insertos hacia la zona apical del tubo corolino. Clusas de 1.8-2 mm, dorso longitudinalmente estriado, cara comisural papilosa. Anatomia caulinar con parénquima ibi de disposición continua, presencia de numerosos cor- dones de esclerénquima. Distribución y ecología. Verbena menthifolia se “acusa en Estados Unidos de América, México, Mace Haití, República Dominicana y Cuba. ; as ve maleza a orilla de rutas e y campos de cultivo, creciendo entre la vegetación ruderal o matorral, en pastizales y suelos arenosos o arcillosos. Observaciones. Verbena menthifolia se diferencia de V. officinalis porque ésta última posee abundante pubescencia glandular en las piezas florales; por otro lado se diferencia de V. neomexicana porque é última presenta flores de mayor tamaño (0.4-1 cm long. en V. neomexicana vs. 0.3-0.45 cm en V. son morfológicamente heterogéneas y sus flores más grandes y conspicuas con tubo corolino de mayor longitud (0.4—0.65 cm vs. 0.3-045 cm en V. menthifolia). Schauer (1847) y Sanzin (1919: 124) consideraban Verbena setosa sinónimo de V. . Autores bác di análisis del ejemplar tipo. Perry (1933) trata Verbena domingensis como alicinala El material tipo de la im hoias y sinónimo de Y. pe o posee pelos adian, siendo la presencia de . officinalis. Moldenke en 1976 funda V. domingensis ` foliosa para referirse taxón pero con hojas, no empobrecido (Moldenke, 1976). eS ' ioldeake (1982a) encuentra un ejemplar muy similar coleccionado en Cuba, por lo cual lo llama variedad cubensis. Perry (1933) cree que este último taxón sería V. officinalis. En el presente tres taxones se consideran sinónimos de V. menthifolia, porque no poseen la pubescencia glandular característica de V. officinalis y are el ejemplar tipo de las mismas se corresponde morí n V. menthifolia. A partir del análisis del ejemplar tipo, junto con la descripción en el protólogo, se A i erbena comonduensis es un sinónimo de V. menthifolia no pudiendo encontrarse ninguna Mage con ésta última especie Este taxón se c incluye en el grupo informal men anteriormente por presentar los caracteres aracteres definidos para el mismo. Urban (1908) citó — e ds Verbena domingensis: 1828 y Bertero 735. La mayoría de los KSE lares de Urban estaban depositados en B y fueron destruidos. En NY y US se encontraron isotipos de Eggers 1828; dl e oe 6 lectotipo porque 5e en mejor myn gt a A A s 0 o a ao d XH vc may" cared ate PAI AA X NOR eia OS a A a RA EIN a AS RAINE BBL WIR ER LE RDN AAS a NR RR laa e ideo: A EUNDI II M A ach bm AER TA io reia ee AR ha qa ae A Annals of the Missouri Botanical Garden Figura 10. A-C. Verbena neomexicana var. neo del tallo. —C. Flor con bráctea. D, E. Verbena neo. bráctea. A-C de Holzinger s.n. (US); D, E de Sperry 478 (US). conservación que el ejemplar de US. El sintipo lado. Bertero 735 no fue hall Material adicional examinado. E.E. UU. Arizona: Pima Co.. e _Range, Jose Juan Tank, Elias et al. 10254 (NY). San Diego Co., Mission hills, San Diego, A 3406 (MO, NY, US). Florida: s. loc., Jan. Ape Biel 121 7, fuge, (US); Mome des ommisaries, s.d., Curtis s.n. (US 11881388). MÉXICO. s. loc., 30 Apr. 1849, 823 (MO). Baja California: Distr. del Sur, Llano de Domingo, Carter et al. 2135 (MO. US). Chiapas: Frontera Comalpa, Breedlove 27018 mexicana. — mexicana var. hirtella. A. Aspecto general de la planta. —B. Detalle de a —D. Aspecto general de la planta. —E. Flor NY) Coahuila: Saltillo, Palmer 191 (MO). Federal: Miranda & Barkley 16998 (MO, NY, 3 Durango: 9 mi. NE 8576 (NY, US). Guanajuato: 20 km hwy. to El Real, Hernandez Xolocotzi ? t O a N Ima pes Beliy IMT [DO Jal qa $ 4 kn N Tulancingo, Hi í (MO). Mé Arsëne (B (MO, US). Morelos: Rincón, cerca de Morelia, s.d., Arséne s.n. (US 464302). Oaxaca: de las Sedas a Salomé, Conzatti 4207 (US). Queretaro: s. loc., Jan 10242 (US). San Luis Potosí: Alvarez, Palmer 141 (MO). de E Veracruz: Las Vigas, ca. Las Vigas, Volume 97, Number 3 2010 O'Leary et al. 397 Revisión Taxonómica de Verbena REPÚBLICA DOMINICANA. d Falls, ld 14838 (US. La Vega: cerca Rio onstanza, Jiménez E. (US). d agen del Rubias, gree 1067 (US). San Juan: Lagiiita y Pico Duarte, 2300- 2500 m, tum et al. 363 (US). 16. Verbena neomexicana (A. Gray) Small, Fl. S.E. US. (A. Gray), ed. 1 [Small]: 1010. 1903. Basónimo: Ver canescens var. neo A. Gray, Syn. Fl. N. Amer. (A. Gray) 2 d "337. TUE) (holotipo, GH no visto, GH foto SI!; isotipo, UC no visto, UC foto SI!). Figura 10. Hierbas erectas hasta de 80 cm de altura, a veces algo lefiosas en la base, pubescencia hirsuta, hispida 9 escabrosa a lo largo de toda la planta, con algunos pelos glandulares. Hojas de 1-6 X 1-3 cm, de lámina entera elíptica o generalmente dividida, pinnatilobada a pinnatipartida, base subamplexi- caule cuneada hacia un pecíolo ancho hasta de l cm, ápice agudo, margen irregularmente inciso- dentado, textura rugosa, con pelos hirsutos sobre las venas y en los márgenes, híspido-escabrosos sobre la cara adaxial, con algunos pelos glandulares. Sin- frondosa, formada por paracladios trí- meros, florescencias densas en la antesis, ca. 0.6 cm lat, hasta de 30 cm en la fructificación, con frutos distanciados, subtendidas por brácteas foliáceas en la base. Brácteas florales ovado-anchas, de ápice agudo, de 0.2-0.4 cm, margen ciliado; cáliz de (0.25-0.35(-0.5) em, con 5 dientes triangulares o gudos, subconniventes en la fructificación; ambas piezas hirsut entes con pelos glandulares, abundantes o no; corola de color azul, purpúreo, lila o blanco, infundibuliforme, tubo corolino breve o largo, de 0.41 cm, externamente subglabro, garganta con pelos moniliformes, limbo extenso o no, entre 04 y 1 em lat; estambres insertos hacia la zona apical del tubo o, Clusas mayores a 2 mm, dorso longitudinalmente estriado, cara comisural verrucosa. Anatomía caulinar con parénquima clo- rofiliano de de disposición discontinua, presencia de numerosos cordones de esclerénquima. Número cromosómico. n = 7 (Dermen, 1936). E Distribución y ecología. Verbena neomexicana se asa POr el sudoeste de Estados Unidos de érica hasta el norte de México. Observaciones. Se reconocen dos variedades para sste taxón diferenciándose principalmente en la ern la morfología foliar y en el tamaño de Este taxón se incluye en el grupo informal Hastatae por presentar los caracteres definidos anteriormente para el mismo. CLAVE PARA LAS VARIEDADES DE VERBENA NEOMEXICANA SUDOESTE DE ESTADOS UNIDOS DE AMÉRICA Y NORTE DE MÉxiIco L A RU M eee e var. neomexicana 16a. Verbena neomexicana var. neomexicana. TIPO: E.E. U.U. Arizona: Sta. Catalina Mtns., Sabino Canyon, 21 Apr. 1922, H. C. Hanson A1130 (holotipo, MO no visto, s = SID. Verbena runyonii ke, Phytologia 2: 25. 1941, syn. nov. TIPO: E.E. U.U. e Cameron Co., El Jardin tract, 2 Apr. 1941, R. Runyon 2 485 (holotipo, NY no visto, NY foto SII). Verbena russellii Moldenke, Phytologia 2: 55. 1941, syn. nov. TIPO: México. Sinaloa: Culiacán, 21 tie 1910, J. N. Rose et al. 1 NY no visto, NY foto SI!; isotipo, US no visto, US foto SI!). La variedad tipo presenta hojas de lamina pinnatilobada a pinnatipartida, de 2-6 X 2-3 em; aE híspida o escabrosa, cara abaxial de hojas con venas terminales de cada diente no protruyentes. Cáliz con 5 costillas no evidentes, triangulares; limbo corolino de 0.4-0.6 cm Distribución y ecología. Sudoeste de Estados CA es Mia a a ch Minen Seda encuentra en terrenos rocosos, Secos, arenosos o en — Verbena neomexicana var. neomex- se asemeja a V. canescens pero esta última se Sena por la pubescencia hi nte, las hojas de base subamplexicaule, el peste ligeramente y brácteas florales más largas que el é ú ó fácilmente V. plicata, pero este último taxón es oe por sus largas brácteas florales ” vena media evid y por la forma espatulada de las o (ver ne bajo tha Lehm., pero éste último no posee cats la variedad xylopoda por la Peny (1983) defn da y glandular y el tubo A am eat ie a GRU Cel e Dieter nee ate tad oa ae came AE w A Annals of the Missouri Botanical Garden corolino de mayor longitud. Siendo estos caracteres muy variables en Verbena neomexicana en este trabajo la variedad xylopoda se trata bajo la sinonimia de V. neomexicana. Ejemplares como Blumer 1804, MO; Tidestrom 872, US; y Peebles 3790, US determinados por Perry como variedad xylopoda no difieren de V. variedad tipo. Moldenke (1941a: 27) funda Verbena pinetorum, sin embargo el ejemplar tipo de este taxón no se ha podido localizar, habiéndose consultado a los herba- rios donde Lon dep "s. 1 3 : de F. Shreve. Por lo tanto, este taxón se trata como dudoso, siendo a partir de la descripción en el protólogo i nte un sinónimo de V. neomexicana. Moldenke (1941a) describe Verbena runyonii como nta 2al ejer tpo de E L anash... mas de V. V. taxón s EL ania de Ie dsp onl prog de peri verificar que tet Á un emanim > El ejemplar tipo de Verbena pinetorum Moldenke no fue localizado, sin embargo en ARIZ se encontraron ejemplares determinados como V. pinetorum por Moldenke en 1941 y 1947. El análisis de los mismos evidenciar que se trata de un sinónimo de V. neomexicana. Perry (1933) cita Verbena officinalis var. hirsuta Torr. como sinónimo de V. ana, no se ha neomexic localizado el ejemplar tipo del taxón de Torrey. Tipificaciones y nomenclatura. Los tipos de Torrey sedit Media de Verbena officinalis var. Mec la colección de tipos y tampoco en el herbario general; el Dr. Moldenke aparentemente no encontró el tipo en NY (Michael Nee, comun. pers.). Moldenke (1964c: 176) dice que mu muy probablemente la variedad hirsuta se base en la misma colección que la de V. neomexicana, por lo cual se trataría de un sinónimo nomenclatural de la misma. Material adicional examinado. E. Arizona: Bizbu, Mearns 1013 (US); Huachuca w. (US); slopes along Calabasas, Ti Tidestrom 873 (US), Baba vari Mtns., Peebles et al. 3790 (US); Chiricahua Blumer 1804 (MO), Pinal Co. _5 mi N Orale, along San en Pedro Ri River, Maguire 10884 (MO). California: El Marmol B.C. Norte, Apr. 1967, Stephenson s.n. (MO 2686031) Louisianas Cameron Co., Wery Ranch, Col o Mexico: Grant Co., East 27 T sn. (US 660559): Pinos eens om co ae Cas De Fen ae 6 mi. n Hwy. 45, Wallace et al. 197 Hermosa, 35 mi. S Monterrey, White 1577 (ARIZ, US). Oaxaca: Wochixtlán, cerro Wochixtlán, 2250 4288 (US) San Luis Potosí: open hillside of chacras, Lundell 5047 (ARIZ). Sonora: 6 mi. E agua Prieta, rd. to Colonia Morelos, White 3836 (NY, US). Tamaulipas: Sierra de San Carlos, Bartlett 10021 (US). 16b. Verbena neomexicana var. hirtella L. M. Perry, Ann. Missouri Bot. Gard. 20: 298. 1933. TIPO: E.E. U.U. Texas: Chisos Mtns., 22 May 1928, E. J. Palmer 34065 (holotipo, MO no visto; isotipos, GH no visto, NY no visto, NY foto SI!). Figura 10D, E eee abramsii Moldenke, Amer. Midl. Naturalist 24: 750. syn. nov. Verbena lasiostachys var. abramsii olen) sen .. Fl. Calif. (Jepson) 3: 381. 1943. : . California: S San Diego Co. Hot E NN 875, E. Palmer 309 (holotipo, NY no visto, NY foto SI!; isotipo, UC no visto). Hojas de lámina entera, elípticas, de margen dentado, de 2-5 X 1-2 cm, pubescencia hirsuta breve y densa. Cáliz con 5 costillas evidentes y dientes agudos marcados; limbo corolino extenso de 0.6-1 cm lat. Clusas ca. 2-2.8 mm. Iconografía. Gleason (1952: 132). Distribución y ecología. Se distribuye por el sur- sudoeste de Estados Unidos de América y norte de México en el estado de Chihuahua, habita terrenos arenoso-arcillosos, O zonas rocosas. Observaciones. Diggs et al. (1999: 1056) en el tratamiento de Verbena para un bes florístico de Texas reconoce dos varied neomexicana la variedad tipo y la variedad hirtella. Perry (1933) diferencia la variedad hirtella por la pubescencia más fina y breve, las hojas de lámina entera, elongadas y la presencia de limbos corolinos mayores a 0.6 cm lat. Generalmente se trata de plantas de base semileñosa, ej., Lewis 5457 (MO), de poca altura, con las hojas reflejas de modo que la lámina adquiere una forma convexa en su cara adaxial y cóncava en la cara Verbena plicata se diferencia de la variedad hirtella porque presenta brácteas florales generalmente de T ESES llegando a 0.6(—0.9) cm vs. 0.2-0.4 cm V. neomexicana, y tubo corolino más breve, nunca I a 0.65 cm; pudiendo en V. neomexicana llegar a lc QUEEN hirsuta también se puede confundir con Verbena cloverae, pero éste último taxón posee hojas de lámina entera a trilobada y ápice obtuso, no volume 97, Number 3 2010 Jepson (1943) trata Verbena abramsii de Moldenke (1940b) como variedad de V. lasiostachys, diferenciándola porque el cáliz posee dientes breves ligeramente erosionados. El análisis del ejemplar tipo de V. abramsii evidencia que este taxón no comparte con V. lasiostachys caracteres propios de la especie como las hojas de lámina trilobada y las florescencias densas, ya que posee hojas de lámina entera y florescencias poco densas. En el presente tratamiento se verifica que el ejemplar tipo de V. abramsii es un sinónimo de V. neomexicana var. oe. adicional examinado. ari, Harrison 4778 (US). Nex Moda orro Mins., Herrick 715 (US). Texas: Brewster Co., Big Bend Park, Lewis et al. 5457 (MO); Brewster Co., Chisos Mins., Sperry 478 (US). MEXICO. Baja California: Laguna Seca, 5 (US). Chihuahua: San Pedro Conchos, Shreve 9089 (US). Coahuila: Villa Acuña, cma de Sentenela en json Piedra Blanca, Wynd 525 (MO). Nuevo León: Galeana, Hac. Cieneguillas on Co. P 11 Aug. 1938, Sodai € Univ. ILL 992 (MO). Arizona: 17. Verbena officinalis L., Sp. Pl. 1: 20. 1753. TIPO: Herb. Clifford: 11, Verbena 6, fol. 6 (lectotipo, designado por Verdcourt [1993: 98], BM no visto, BM foto SI!) Hierba grácil, erecta, de 20-100 cm de altura, ramificada desde la base, con pubescencia estrigosa- escabrosa cuando joven, con pelos glandulares, subglabra hacia la madurez. Hojas de lámina variable, trilobada, tripartida, pinnatipartida o entera, de 2-12 X 1-45 cm, ovadas, base subsésil, angostándose ia un pecíolo breve hasta de 1 cm, margen variable, nunca entero, inciso dentado-serrado con dientes ambas caras con pubescencia adpreso-estrigosa. Sinflorescencia bracteosa, formada por paracladios trímeros laxos, mayor a primer orden de ramificación, florescencias laterales no superan a la principal, filiformes, de 10-35 X 0.3-0.5 em, alargándose en la Seni. pedunculadas, raquis de pubescencia ar. Brácteas florales ovadas de n eL em, de ápice agudo, con pubescencia escabrosa y margen piloso; cáliz de 0.15-0.35 cm, con 5 dientes triangulares, subconniventes en la fructifi- ulares; corola de color rosa, rojizo, violeta o blanco, infundibuliforme, tubo corolino de 0.3-0.6 cm, an- 80Sto, externamente viloso, internamente pubescente “on pelos moniliformes, limbo poco desarrollado; a insertos hacia la zona apical del tubo MM Clusas de 1.8-2 mm, dorso oe . Mente estriado, cara comisural papilosa. Anatomi T caulinar con nte clorofiliano de apasi O'Leary et al. 399 Revisión Taxonómica de Verbena co resencia de numerosos cordones de esclerénquima. Distribución y ecología. Verbena n—— es una de las especies de Verbena distribuida. eu (1993), Munir nto y Méndez Santos (2003) la consideran nativa del continente europeo, en la región mediterránea, África y Asia, y naturalizada en casi todo el resto del mundo, como América y Australia. Sin embargo, Barber (1982) sugiere que. ea mb. phala qua n ¿sigan sa wr An al rain resto del avido deki deb d ao A s A sima americano here, & Oliver, 1961). Masha v veces a de dm arcillosa. Observaciones. Los nombres Verbena officinalis var. vulgaris Schauer (en Martius, Fl. Bras. 9: 191. 1851, nom. illeg. superfl.) y Verbena officinalis var genuina Briq. (Ann. Conser. Jard. Bot. Geneve 10: 105. 1907, nom. illeg. superfl.) se basan en el ejemplar tipo de V. officinalis por lo cual son son nombres superfluos (McNeill et al., 2006: Art. 52). Este taxón se incluye en el grupo informal Verbena por presentar los caracteres definidos anteriormente CLAVE PARA LAS VARIEDADES DE VERBENA OFFICINALIS: Arnica, Asia, AUSTRALIA, EUROPA, ESTE DE be Estapos UNIDOS DE AMÉRICA, ANTILLAS, AMÉRICA DEL SUR E ISLAS DEL PACÍFICO Y DEL ATLÁNTICO ...... E Hojas enteras o no, con segmentos breves, anchos y obtusos, margen crenado a serrado-obtuso eee e e e eee eee eae 4» "^ v K row» e kk. eA l7a. Verbena officinalis var. officinalis. : Pl. 1: 20. 1753. Verbena officinalis var. RR Comp. Bot. Mag. 1: 176. 1836. TIPO: Meni 8 ati, say pe hee ond ia SIR edel ei. Fragm. (Mueller) 1: im x ar. macrostachya (F. Mul) “= ease aps pesa — op. Gl w vite Eden n M E E P e A DAR RM LP RUE EQ CU i P NN Annals of the Missouri Botanical Garden Lk. SE Ji. wu. L , Mitth Thüring. Bot. take oe ee 1897, syn. nov. TIPO: Grecia. “In reg. infer. m. Pindi ca. monaster- ”, 3500-3700 m, ium Korona, in nemorosis 20-28 June 1885, H. C Beanie ua. (holotipo, JE no visto, JE foto SI!). Verbena officinalis var. ramosa H. Lév., Repert. Spec. Nov. a Veg. 10 50-262 40 440. 1912, syn. nov. TIPO: China. Prov. du Kouy-Techéou [ ]: re Lan-Men-Ouay, 16 p 1898, Em. Bodinier 2: (holotipo, E no visto, E foto SI!). Verbena officinalis f. anomala M Phytologia gcn 163. 1982, syn. nov. wangtung [Guangdong]: Hainan HAE 1934, H. Y Liang 64870 (holotipo, MICH no visto, MICH foto SI!; isotipo, NY no visto, NY foto SI!). Verbena officinalis var. eremicola Munir, J. Adelaide Bot. Gard. 20: 88. 2002, syn. nov. TIPO: Australia. Far NE of South Australia, 5 km ENE Karawinni waterhole, 17 Aug. 1975, J. Z. Weber 4543 (holotipo, AD no visto). Hojas de lámina entera o trilobada, tripartida, pinnatilobada, segmentos breves, obtusos, margen crenado a serrado-obtuso, las hojas basales muchas veces de lámina entera y las apicales divididas y de menor tamaño. Flores con brácteas de 0.15-0.3 cm; cáliz de 0.15-0.3 cm; tubo corolino de 0.3-0.5 em. Número cromosómico. n = 7 (Noack, 1937; Schnack & Covas, 1944; Vasudevan, 1975; Koul et al., 1976; Aryavand, 1980; García Martin & LM 1985; Ghaffari, 1987); n — 28 (Bir & Saggoo, 1979 2n = 14 (Dermen, 1936; Noack, 1937; os 1976; Vachova, 1976; Van Loon & Kieft, 1980; Lóve, 1982b: 587; Van Loon, 1982; Díez et al, 1984; Semerenko, 1985; Montgomery et al., 1997); 2n = 42 (Huang et al., 1986, 1989). lconografía. Britton y Brown (1913: 95); Gleason (1952: 128); 1966: pl. 38); Michael (1997: 294, fig. 1); Munir (2002: 79, fig. 7). Distribución y ecología. Verbena officinalis var. officinalis es originaria de Europa y Asia (Britton & Brown, 1913; Moldenke, 1964c; Munir, 2002) donde es frecuente, y actualmente se encuentra naturalizada en el resto del mundo, como en islas del Pacífico y del Atlántico, este de Estados Unidos de América, Antillas y América del Sur. Observaciones. La morfología de las florescencias muy variables en V iini. Se han encontrado ej de lámina entera (ej., Hind 727737, NY; Moore 393, US; Tyacke 1838, NY) y ejemplares con hojas pinnatipartidas (ej., Duthie 4282, US). Por otro lado hay ejemplares que poseen florescencias filiformes y frutos dies ca. 1.5 cm (ej., Davis 8493, US; Small 4762, US; Reclaire s.n., US 1750319); y otros donde las Se ee Dorsett & Mueller (1858) describe Verbena macrostachya como una especie con hojas ovadas de cuneada hacia un pecíolo decurrente y hojas superiores subsésiles, florescencias elongadas y robustas, y la asemeja a V. stricta, diferenciándose ésta última por poseer hojas elíptico-orbiculares y ausencia de pelos glandulares. Bentham y Mueller (1870) consideran V. macrostachya como una variedad de V. officinalis con flores mayores y florescencias densamente glandulares e hirsutas. Michael (1997) la vuelve a considerar una especie, basándose en sus - flores de mayor tamaño bescencia híspido-glandular. El análisis del ides stachya se superponen morfológicamente con los presentes en V. officinalis. Hay ejemplares como Fosberg 37559 (US) y Jermyn 824 (US) con las florescencias robustas como las definidas para V. macrostachya y las hojas similares a V. officinalis. Por lo tanto es imposible ca ambos taxones y aquí se tratan como sinónim Varios autores pei, Perry, isi Moldenke, 1964g: 100; Sanders, 2001) han considerado Verbena riparia como especie , válida. Sin embargo el análisis de varios ejemplares coleccionados por Small y A. Heller, determinados por los mismos como V. riparia permite comprobar que no puede diferenciarse de V. officina- lis, por lo cual en el presente tratamiento ambos taxones se tratan como sinónimos. Verbena officinalis var. grandiflora se diferenciaría de la variedad tipo porque las flores son el doble de tamafio y se disponen remotas, en florescencias elongadas. Sin embargo, las dimensiones descritas del rango El análisis de los tipos de la variedad ramosa y de la forma anomala, ambos de China, evidencian que son sinónimos de Verbena officinalis. La proliferación anormal de florescencias que los dos ejemplares tipo presentan se considera un carácter taxonómicamente irrelevante. Moldenke (1982b: 163) sugiere que la forma anomala podría ser una planta atacada por un virus. Munir (2002) caracteriza la variedad eremicola por poseer las flores densamente imbricadas, en flores- cencias delgadas. El análisis de la descripción original junto con el estudio de material de herbario permitió determinar que este taxón es un sinónimo de Verbena officinalis. Moldenke (1964c: 198) cita Verbena rumelica Velen. (Velenovsky, 1891) y V. vulgaris Bubani (Bubani, 1897) como sinónimos de V. officinalis, los ejemplares tipo de estos dos taxones no se Volume 97, Number 3 2010 O'Leary et al. Revisión Taxonómica de Verbena localizado. Munir (2002) menciona V. spicata Gilib. (Gilibert, 1782) como sinónimo de V. officinalis. Según Moldenke (1964d: 277) Verbena officinalis var. albiflora Strobl (Strobl, 1883) difiere únicamente por las corolas blancas, un carácter taxonómicamente irrelevante para sustentar un taxón. El ejemplar tipo es de Italia, Sicilia, pero no se ha localizado. Tipificaciones y nomenclatura. En el protólogo de Verbena spuria se menciona: “Habitat in Canadá, Virginia” (Linnaeus, 1753: 20), por lo cual el tipo puede ser de Estados Unidos de América o Canadá. En BM no se encontró ni emplar original. El ejemplar del Herbario Clifford (BM 0005. officinalis no corresponde a Linnaeus. Ad Linnaeus no menciona V. spuria en el Cliffortianus (Linnaeus, 1738), y después de partir de Holanda en 1738 no volvió a visitar y Herbario Clifford. No hay evidencia de la exist original de V. spuria por lo cual se debe Bishi is Preferentemente, el neotipo debe ser elegido en concordancia con el protólogo (McNeill et al., 2006: Art. 9). Se realizó una búsqueda de material de Linnaeus en herbarios de Norteamérica (C, H, L, LD, LIV, OXF, P, S, SBT, UPS) y no se encontró ningún ejemplar, por lo cual se buscaron ejemplares mencionados por autores de floras antiguas de la región: Nuttall (1818), Muhlenberg (1818), Chapman (1860), Gray (1 856). La primer mención a V. spuria en regió n Nis maternal . En PH se encontró un ejemplar de rg con una etiqueta V. spuria nro. 68. Este ejemplar fue elegido neotipo e es un buen material y concuerda enteramente con la descripción en el protólogo. Como existen dos hojas del mismo se eligió una de ellas como neotipo (PH 3073), siendo la restante un isotipo (PH 3074). Charlie Jarvis, Linnaean Plant Name Typification Project (comun. Pers.) coincide que el taxón debe ser neotipificado y aprueba la elección del neotipo aquí propuesto. Small y Heller (1892) al publicar Verbena riparia Auibuyen este taxón a Rafinesque y no indican tipo. El as Durand en 1800 destruyó todo el de Rengar (Michael Nee, NY, comun. pers.; Harold Robinson, US, comun. pers.) por lo cual nte el ejemplar tipo de este taxón no existe. Consecuentemente, se debió elegir un lectotipo ante la inexistencia de material visto por Rafinesque asociado al nombre V. riparia. En NY se encontraron varios » ejemplares coleccionados en Virginia y North ae por Small y Heller previos a la publicación — e V. riparia. Se designó lectotipo un ejemplar North Carolina que posee una etiqueta de Moldenke de 1963 que dice *LOGOTYPE! Verbena riparia Raf." y otra de Roger Sanders del año 2000 donde dice que el ejemplar es un buen candidato para lectotipo en caso de que el holotipo no sea En el protólogo de la variedad bla. Muni (2002) menciona que hay un isotipo de la misma en HBG y otro en BR. Sin embargo, Hans-Helmut Poppendieck, curador de HBG (comun. pers.) cree que el Dr. Munir tenía intenciones de dejar un isotipo allí pero que aún no lo ha hecho. Por otro lado, Piet Stoffelen de BR (comun. pers.) tampoco encontró el isotipo de este taxón en el he Material | adicional examinado. DEL NORTE. E.E. U.U. Florida: Escambia Co., Pensacola, : Greencastle, s.d., Lemam s.n. s.d., Curtiss s.n. (NY). Indiana: 150043). : Sommerset Co., Grisfield, H 76 (US). New York: Hudson Co., Jersey Dm 9 qi 1879, Carolina: Bladen Co., Clarkton Schrenk s.n. (NY). North Small 4762 (NY). South Carolina: Anderson i Ander- (US) Virginia: Smyth Co., Middle Fork Hoston tm at Marion, 2100 ft., 6 July 1892, Small s.n. (MO, NY, U. AMÉRICA My Petropolis, Barth 916 (US). Santa Feb. 1950, Rei 3287 (SI). CHILE. X Lagos: Panguipulli, Joseph 5408 (US); Valdivia, Ins. Teja, Holler- — 191 6 (MO, US). AFGANISTÁN. NES Koelz 11785 (US). ARA- BIA. HD of stream, 12 mi. NW Saná, Yemén, 11 Feb. 1951, Kuntz s.n. (US 1 994907. CHINA. _— Xiamen, Jan 1981, Xiam. Exp. 20 (US). Heilongjiang: Szec n Koagtin Hsien, Tachienlu, Fang 3661 vee Ssh, Jianesi, Liu 890121 (MO). ew Kong: Hong Kong, s.d., Shiu Ying Hu 10350 (US). INDIA. Kashmir, Stri 1856, s. coll. (US pos Kulu, n x. Punjab, Koelz 4769 (US); Kumaun, near N (US). IRÁN. rbaijan: Hasanlu, m one x (MO). Gorgan os cs July e Koelz 16144 (US). Beach 5407 (US). JAPÓN. Baturn RYUKYU ISLANDS. Okinawa Islands: a, Taketomi Shima, SE Hazama, Fosberg 37559 (US); CS woa Sima 4km 4 km H N Zumori, Fosberg . Yaeyama MOM TM Kabira, Smith 50 2 9 Kabira, Smith 211 (US). TURQUÍA. s. loc., s.d., Frivoldsky s.n. (US 2646 mnia ALEMANIA. s. loc., 17 July 1906, s. coll. (SI 3410). Baden-Wiirttemberg: Kunze lan, Jan. 1884, Holzin- ger i (US 245962). Bohemia: From Goslar to Reich- 1947, Weberling s.n. (MO 5408726). oun irat Eisen, Enlebom, Kapp! 3412 G) > "= m STRIA. Wien, Stearn 9. y 979. e Silikatschiefer, 27 July 1984, Polatschek s.n. (SI). BELGICA. Bruselas, Sep. 195 7 ESPANA. Castilla-La Leadlay & Petty 108 MO). Casaus Bake 4845 I). FRANC IA. e Duval Louve, " Hicken 3411 (SD. Midi-Pyréneés: Zetterstedt 1050. (NY). desde Normandy: Romilly-sur-Andelle, Tidestrom 13282 Annals of the Missouri Botanical Garden mo ORGIA. Kareli District: W of town Agara, Atha et al. 3653 ee HOLANDA. Limburg: Strucht, 14 A Sep. P & Kramer s.n. (NY 49726). Zuid-Holland: Rotte dam, July 1898, Reclaire s.n. (US 1750319). INGLATERRA. s. loc., Apr. 1921, Greenway 340 (NY). East: Essex, Jermyn 824 (US); Coulsdon, 13 July 1902, Denton s.n. (NY); Ballast, Martle ermyn 822 (US); Cornwall . Bernet s. Wallis, abore St. Leonard, side of Rhone Valley, ad Bio Rheno-Trai 230 (NY). ISLAS DEL PACIFICO. NIUE ISLAND. E Alofi, Yuncker 10145 (US); s. loc., 25 Nov. 1899, Moore 393 (US). ISLAS n ARE ISLAS AZORES. Sta. María, Trelease 685 (MO); s. loc Brown 213 (US). ISLAS BERMUDA. s. loc., Stewardson 28 (US); s. loc., 3 Aug 1913, Collins 267 (US); Bailey's Bay, seda 492 20. ISLAS CABO VERDE. Isla de Santiago, c. Ribeira Principal, Granvaux Barbosa 6013 (MO). Ms CANARIAS. Gran Canaria, Tafira, e Cook 569 (MO); Gran Canaria, Caves, Carter Cook 35 17b. ra officinalis var. natalensis Hochst. C. Krauss, Flora 28: 68. 1845. TIPO: senti KwaZulu-Natal: pro, Umlaas, Dec., C. F. Krauss 151 (holotipo, g no visto, M foto SI!; isotipos, MO!, SI!). cs e Don, — Fl. Nepal. 104. 1825. TIPO: pal. Bassaria, 7 Mar. 1802, F. Buchanan omiin s.n. "iD. BM no erg BM foto SIN). Verbena officinalis subsp. "ipei R. Fern. re es Bol. Soe. Brot., ser. 2(62): 305. 1989, s. Volens R. Fern. & Vero.) P. W. Michael. = 7(3): 296. 1997. Verbena inalis var. € Fem. & m Munir, J. Adelaide Bot. ‘Gard. 20: 2002. TIPO: Zimbabwe. Salisbury, betw. E West & Mabelreign, 1480 m, 21 Aug. 1955, R. B. Drummond 48. (holotipo, K no visto, K foto SI!; isotipos, B no visto, BR no al S no visto). Verbena officinalis var. — ein. J. Adelaide Bot. Gard. 20: 86. 2002, syn ustralia. Victoria: Mt. Buffalo, vic. chala Ves 19 Feb. 1986, D. E. Albrecht 2474 (holotipo, 260636 no visto, MEL 1560636 foto SI!; isotipo, poa 1560637 no visto, MEL 1560637 foto SI!). La variedad natalensis difiere de la variedad ti tripartidas o pinnatipartidas, con los segmentos angostos de ápice agudo, margen dentado serrado- acuminado, las las hojas basales y las apieales similares. Posee flores algo mayores res que la variedad tipo, con mente are corolino de 0.3-0.6 cm. cm. Iconografia. Henderson y Anderson (1966: fi 128); posi y Verdcourt (1989: tab. 1); Michael (1997: 296, fig. 3); Munir (2002: 83, fig. 8) Distribución y ecología. Verbena officinalis var. natalensis crece en Africa, Asia, Europa y Australia. noe s y Verdcourt (1989) fundaron Verbena officinalis subsp. africana; poste- riormente aba (1997) a ree a especie; en 2002, unir la volvió a tratar dentro de V. officinalis pero como variedad. A partir del análisis del ejemplar tipo de este taxón se evidencia que no existen diferencias morfológicas con V. officinalis var. natalensis, por lo cual en el presente tratamiento ambos taxones son tratados como sinónimos. Munir (2002) funda la variedad monticola sobre la base de la: pubescencia glandular del raquis y la presencia de un breve pedicelo; estos caracteres son muy variables en Verbena officinalis. Munir (2002) menciona este taxón como puede de Victoria (Australia), sin embargo se han encontrado uae fuera de Australia, como Jessep 467639 (MO) de Nueva Zelanda, que presentan los caracteres diag- nósticos de la variedad monticola, como por ejemplo frutos pedicelados. El análisis de la descripción original realizada por Munir (2002), del material tipo y de otros ejemplares permitió verificar que esta variedad es en realidad un sinónimo de la variedad nsis. El ejemplar tipo de Verbena sororia posee hojas pinnatipartidas, con los segmentos de ápice agudo, margen inciso serrado, las hojas basales y las apicales similares. El análisis del mismo permite determinar que se trata de un sinónimo de la variedad natalensis. Este taxón se incluye en el grupo informal Verbena por presentar los caracteres definidos anteriormente para el mismo. Material adicional exa a: AFRICA. P Nairobi & Athi rivers, cerca Juja farm, Mea rns 82 (US); fro Nyeri to Wambugu, Mearns 1 L5 US) ETIOPÍA. NE lake Alemaya, 35 km rd. from Dire Dawa to Harar, De Wilde 4845 (MO). MOROCCO. High Atlas, Amigdal, betw. ljoukak & Asni, 13 June 1974, BM expedition, s. coll. — agone TANZANIA. Arusha: Ngorongoro, rd. to Lodoare St., Norten Highland forest, Margwe 29 (MO). ASIA. CHINA. Anhwei [Anhui] Province: Chiu Hua Shan, Chin 8514 (US); 31 = _ sal n. (US 456231). Yunnan: Chuxiong lomew et al. 1253 (US); Na Nanking Tu ges (US). “JAPON. Kuma tsuzura, Shimura, Musachi, 19 June 1893, s. Pe (US 206019); Kuma tsuzura, Chikuzen, atara, Takenonchi 1 724 (US); Okinawa, Buckner Bay, Beauchamp 1178 (US; Isla t. Omoto, Iwatsuki et al. 102 (MO). TAIANA Chiang Mai: Doi Inthanon, 39 km "P. mtn. to gate, A 3977 (MO). TAIWAN. Annan, July 1943, Scholes s.n. (Us 2630558); , Taihoku-shi, Tanaka 11032 (MO. - Volume 97, Number 3 2010 O'Leary et 403 al. Revisión Taxonómica de Verbena Figura 11. A-D. Ve Verbena a perennis v Detalle de pubescencia de hoja, cara abaxial. encia del tallo. —F. (M0); E, F de Stanford et al. 486 (MO). f; rk 3087 (US), Aveyron: Tournemire-Roquefort, Mar PACÍFICO. P E. Okinawa E Kade: . Moran 5066 (US); "c Miyako 1 Jima, 1 km E Takebaru, Fosberg 38613 urema Ji & Sunagawa 22 (US); var. perennis. —A. Aspecto — D. Flor con bráctea. E, F. Verbena perennis var. e de pubescencia de hoja, cara abaxial. A f 1 a A EP WERT NY TRA E y Po e d th La 1 i o general de la planta. —B. Detalle de pieno del tallo. E. Detalle var. johnstonii de Nelson 11406 (MO); Mid quo Okinawa, Naha, Univ. Ryukyus campus, Walker 8101 (US); cee a, Phillips 46 (US). ockanta. AU aee New South Wales: Fauaba- long, May 1906 n. (BAF); Cobar, Bundy-Coola, Constable 11633 (US). NUEVA ZELANDA. Canterbury: Ashburton River, Jessep 467639 (MO). aa M DN dad sus a al ÓN REL aM ELE Annals of the Missouri Botanical Garden 18. Verbena perennis Wooton, Bull. Torrey Bot. Club 25: 262. 1898. TIPO: E.E. U.U. New Mexico: Lincoln Co., White Mtns., 1800 m, 21 July 1897, E. 0. Wooton 187 (holotipo, NY no visto, NY foto SI!; isotipos, BKL no visto, GH no visto, GH foto SI!, MO no visto, P 00371002 no visto, P 00371002 foto SI!, P 00371003 no visto, P 00371003 foto SI!, SI!, TEX no visto, US no visto, US foto SI!). Figura 11. Sufrütice erecto, de base lefiosa, generalmente con raíz gruesa, con numerosos tallos ascendentes, hasta de 40 cm de altura, pubescencia variable desde a Jfogecas — generalmente l es. Hojas de 1-5 X 0.1-0. 5 cm, de jwis entera T lineares, las cladios trímeros laxos, de un orden de ramificación, las florescencias laterales no superan a la E florescencias cilíndricas, laxas, de 3-20 X 0.3 0.6 cm, frutos distanciados ca. 1 cm, raquis co pubescencia glandular. Brácteas florales ovadas le 0.2-0.4 cm, de ápice agudo y margen ciliado, con bescencia estrigosa o hirsuta y pelos glandulares breves; cáliz de longitud mayor o igual que la bráctea, de 0.32-0.45 cm, pubescencia estrigosa o hirsuta con pelos glandulares breves, con 5 dientes triangulares, subconniventes en la fructificación; corola de color azul, violeta a lila, infundibuliforme, tubo corolino de 0.55-0.85 cm, limbo extenso o no, de 0.3-1 em, extemamente pubescente y pelos moniliformes en la garganta; estambres insertos hacia la zona media del tubo corolino. Clusas de 2-2.5 mm, dorso long- itudinalmente estriado, cara comisural muricada. Anatomía inar con parénquima clorofiliano de disposición continua, presencia de numerosos cor- dones de escleré Nümero cromosómico. n — 1 (Lewis & Oliver, 1961; Ward, 1984) Distribución y ecología. Verbena perennis se dis- tribuye por el sur de Estados Unidos de América y norte de México. neomexicana en cuanto a la pubescencia y el tamaño de las flores, sin embargo se distingue fácilmente porque las hojas de V. perennis son lineares Este taxón se bs en el grupo informal Hastatae por M los caracteres definidos anteriormente CLAVE PARA LAS VARIEDADES DE VERBENA PERENNIS: SUR DE ESTADOS UNIDOS DE AMÉRICA Y NORTE DE MÉXICO 1. a con tallos subglabros a ligeramente estrigo- 18a. var. perennis 18a. Verbena perennis perennis. Fig- ura 11A-D. var. Esta variedad se diferencia por poseer tallos abros con algunos pelos estrigosos breves, adpresos y hojas con pubescencia estrigosa poco densa. Distribución y ecología. Sur de Estados Unidos de América en los estados de Nuevo México y Texas. Se la encuentra en suelo calcáreo, rocoso, árido. Material adicional examinado. E.E. U.U. New Mexico Eddy Co., Carlsbad Caverns, Nelson 1 tee E Sierra Co. 5 Berendo Creek, f 1568 (MO, US). Texas: Guadalupe Mtns., Clark 4250 Ingram 2736 (US). (MO); Brewster Co., 10 mi. E Alpine, 18b. Verbena f var. impetus Moldenke, Phytologi na perennis f. insi c) Moldenke, Phytologia 44: 1 . Retherford & R. D. Northcraft 915 (holotipo, NY no visto, NY foto SI!; isotipo, MO no visto). Figura 11E, F. Esta variedad se diferencia por poseer tallos y hojas con pubescencia hirsuta densa. Distribución y ecología. Esta variedad habita terrenos secos y áridos del norte de México. Observaciones. Moldenke (1946: 150) define la variedad johnstoni; sobre la base de la pubescencia densa y las hojas hasta de 5 lóbulo lineares. Nesom (1992: 321) la eleva a — basándose fundamentalmente en su di pu- bescencia, siendo en Verbena perennis los nie y hojas subglabras y ; lares. Se acepta el criterio de Moldenke (1946) dado que ambos taxones comparten las hojas con lámina reducida, lineares a sublineares, lo cual es un carácter poco frecuente en el género, siendo la pubescencia lo único que las diferencia, lo cual no es lo suficiente confundirse con V. canescens, sin ae las hojas de V. canescens son oblongo Volume 97, Number 3 2010 O'Leary et al. Revisión Taxonómica de Verbena ^ MW Y Sh á 12. Verbena plicata. —A. Aspecto general de la planta. —B. Cara F T — D. Fruto recubierto con cáliz y bráctea. A-D de Tracy ágostas, de base atenuada hacia un pecíolo ancho y Ñ las brácteas son de mayor longitud que el liz siendo hojas lineares subsésiles y brácteas de _ ‘Menor o igual longitud que el cáliz en V. perennis. ial de hoja, detalle de venación. —C. Flor abaxial & Earle 30 (isotipo, MO). Material adicional examinado. MEXICO. Coahuila: Coahuila—Zacatecas border, 15 km W Conc. del Oro, 19 July 1941, Stanford et al. 486 (MO). Nuevo León: Galeana, Sta. Rita, 14 May 1981, Hinton et al. 18244 (MO). A EE TEE AS Annals of the Missouri Botanical Garden 19. Verbena plicata Greene, Pittonia 5: 135. 1903. TIPO: E.E. U.U. Texas: Ward Co., Barstow, 14 Apr. 1902, S. M. Tracy & F. S. Earle 30 (holotipo, NDG 43325 no visto, NDG foto SI!; isotipos, MO!, NY no visto, NY foto SI!, SI!, TEX no visto, TEX foto SI!, US no visto, US foto SI!). Figura 12 co e lene ke) Degener 5148 (holotipo, NY no visto, NY foto SI). — o pipes erecto, hasta de 25 cm i altura, de l base raiz fibrosa, hirsuta con algunos pelos glandulares. Hojas de 1-6 X 1-4 cm, de lámina elíptico-redondeada, espatuliforme, trilobada, ápice obtuso, base subamplexicaule angos- tada hacia un pecíolo ancho de longitud variable llegando en ocasiones a tener casi la misma longitud que la lámina, margen inciso-dentado, cada diente con ápice mucronado, rugosas, ambas caras con pubescen- cia hirsuto-canescente, a veces glandular, cara abaxial con venación notoria, venas terminales de cada diente gruesas y protruyentes, de coloración blanquecina. ndosa, formada por paracladios trímeros laxos, mayores a un orden de ramificación, las florescencias laterales no superan a la principal, florescencias cilíndricas de 8-15(-25) x 0.5-0.6 cm, flores densamente imbricadas en antesis, frutos remotos. Brácteas florales je ovadas, más largas que el cáliz, de 0.3-0.6(0. m, anchas, de 0.15—0.4 cm lat., acrescentes en la RE. con notoria vena media, de aspecto folioso, hirsuto- glandular, saa ciliado; cáliz 0.3-0.4 cm, con 5 dientes tri subconniventes en la fructifica- ción, mih] ar ¿lindas corola de color rosa, lila o rojizo, infundibuliforme, tubo corolino 0.4— 0.65 cm, glabro externamente, algunos pelos en la zona media del tubo, limbo poco desarrollado; estambres insertos hacia la zona ird. del tubo poian, Clusas de 2-2.5 mm, dorso liso o longitudinalmente estriado, cara comisural papil Anatomía caulinar con parénquima clorofiliano de disposición discontinua, presencia de numerosos cordones de esclerénquima. Número cromosómico. n = 7 (Lewis & Oliver, 1961). lconografía. Diggs et al. (1999: 1059, fig. 108). Distribución y ecología. Verbena plicata se en- cuentra en el sudoeste de Estados Unidos de América en Arizona, Nuevo México y Texas, hasta el norte de México. Crece en terrenos abiertos, húmedos o anegados, también arenosos o algo calcáreos y en praderas rocosas. Observaciones. Este taxón se encuentra cercana- mente relacionado con Verbena canesc (véase observaciones bajo V. canescens) y con V cloverae (véase observaciones bajo V. cloverae). Moldenke (1941a) funda Verbena plicata var. degeneri; diferenciándola por poseer las brácteas florales rígidas, de 0.9 X 0.6 cm, abruptamente acuminadas hacia el ápice. Posteriormente, Moldenke (1964f: 18) dice que esta variedad sería endémica de dos condados de Texas, y agrega que posiblemente se trate de una forma dada en el riguroso ambiente en el cual se la encuentra. Sobre la base de estos comentarios y a partir del análisis del ejemplar tipo se considera que esta variedad no merece valor taxonómico y se trata bajo la sinonimia de V. plicata. Este taxón se incluye en el grupo informal Hastatae por presentar los caracteres definidos anteriormente para el mismo Material adicional examinado. .U. Arizona: Pima re me Toumey E (US). en Mexico: Chaves Co., mi. E jet. 285-70, n Hwy. 7 0, Higgins 7023 (NY). n T Co. 6 mi. E Eldorado, Waterfall 11980 (US). Texas: Ward Co., 3 1/2 mi. NW Monahans, Cory 51970 (NY). MEXICO. Sonora: 7.9 mi. N Esqueda, Wiggins 11783 (US). Tamaulipas: 6 mi. NE San Antonio, Lewis & Oliver 5412 (MO). 20. Verbena recta Kunth, Nov. Gen. Sp. (quarto ed.) 2: 277. 1818. Verbena carolina Í. recta (Kunth) Loes., Repert. Spec. Nov. Regni Veg. 9: 362. 1911, sphalm. “caroliniana” Verbena carolina var. recta (Kunth) Loes., Repert. Spec. Nov hg Veg. 9: 362. 1911, sphalm. “car- oliniana”. TIPO: México, Hidalgo: entre Pachuca y Co. Mien s.d., W. Humboldt & A Bonpland 4066 iioi dtes P no visto, P foto SI; isotipos, P no visto, P foto SI!, SI!). Figura 13A. Hierba perenne, erecta, hasta de 80 cm de altura, ramificada en la parte apical, pubescencia hispida. Hojas de lámina entera, de 3-10 X 1—4 cm, ovadas, ápice agudo a subobtuso, base cuneada, pecíolo de l em, margen irregularmente serrado a biserrado, dientes de ápice acuminado, cara superior adpreso- a Ti de Didi: ovadas, de ápice a de 0.15-0.2 cm, de menor longitud que el cáliz, margen piloso, dorso subglabro; cáliz de 0.2 cm, con pubescencia adpresa breve y escasa, con 5 dientes triangulares, subconniventes en la fructificación; Volume 97, Number 3 O'Leary et al 2010 i Revisión Taxonómica de Verbena "€ ——— OO dd Fi L na F o eed aps id en gi =n x la planta. B, C. Verbena simplex var. Mp — B. Aspecto general de ar. orcuttiana. —D. Flor con boites. E Detalle de ind del tallo, A de Pringle 13997 € Gn. A v d yolk s.n. (US) D, E de Moran 13604 (US). co : —— x. violeta o lila, infundibuliforme, tubo montañas, a altitudes superiores a 2800 m, por lo cual | is em, glabro externamente, pubescencia ha sido poco coleccionada. | pe ee en la garganta, limbo poco haen mantan karia la xoa a _ Observaciones. Verbena recta es morfológicamente del tubo lor Cluses L5 pical ^: ilar a V. hastata, de la cual se diferencia porque ara comisural lisa. co q, de decia A la primera presenta florescencias más breves, agru- ía caulinar con parén- : : quima clorofiliano de disposición conti padas en paracladios congestos, debido a los de numerosos cordones pes n continua, presencia hipotagmas reducidos, siendo los paracladios laxos Distrib npe ec en V. hastata. El grado de desarrollo de los nica o y ecología. Verbena recta es endé- — muchas veces determina los diferentes X Centro y sur de México, donde es poco pos de inflorescencias en Verbena (Martínez et al, U iin, siendo que se halla restringida a las altas 1990. — . Annals of the Missouri Botanical Garden hastata únicamente se ha encontrado en Estados Unidos de América y Perry (1933) la odiis is taxón válido y Rzedowski y Rzedowski (2002) dice que ha sido citada por otros autores, sin mencionar quienes, para los estados Morelos, Puebla, Tlaxcala y Van. pero no se han visto ejemplares de esos estados. Este taxón se incluye en el grupo informal Hastatae por presentar los caracteres definidos anteriormente para el mismo. Material adicional examinado. s. loc., pond 1826, $. coll. (US 264565). MÉXICO. Distrito F Estación Chincua, Reserva ornejo Tenorio 73 (IEB); 3972 s M 03 (IEB); del Burro, Díaz Berria 1042 iue Oaxaci: Miahuatlán, 1 Llana. Hinton et al. 26191 (IEB). 21. Verbena scabra Vahl, Eclog. Amer. 2: 2. 1798. PO: Jamaica. s. loc., s.d., J. Von Rohr 35 (holotipo, C no visto, C foto SI!). Figura 14E, F. Verbena sc ped T Phytologia 14: 296. E. i nov. TIPO: E x U. Texas: Beaver Creek, Burnet Co., 21 July 1966, J. R. Crutchfield 1837 (holotipo, TEX no visto, TEX foto SI!). na scabra f. ternifolia meu Phytologia 29: 503. 1975, syn. nov. TIPO: E.E. U.U. Texas: Tom Green Co., Dove Creek, elo 19 July e a Eckhardt 1739 (holotipo, TEX no visto, TEX foto Hierba erecta hasta de 2 m de altura, subleñosa en la base, toda la planta con pubescencia escabrosa de pelos breves y rígidos. Hojas 2(3) por nudo, de lámina Pam m de 4—8(-13) X 3-4(-6) cm, ce agudo a subobtuso, margen serrado o subcre- dn base ia vum pud de 1-4 cm; ambas caras mayor a primer orden de ramificación, las florescen- cias laterales no superan a la principal, filiformes, en la fructificación hasta de 30 X 0.3-0.4 cm. Brácteas princi mente a lo largo de las venas; corola de color violeta o infundibuliforme, tubo corolino de 0.28-0.3 cm, limbo poco desuriollado, externamente glabro, pelos moniliformes en el interior; estigma bilobado sub- tendido por dos prolongaciones estériles del estilo a modo de lóbulos obtusos; insertos hacia la zona apical del tubo corolino. Clusas ca. 1.3-1.5 mm, dorso reticulado longitudinalmente estriado, cara comisural verrucosa. Anatomía caulinar con parén- quima clorofiliano de disposición continua, presencia de numerosos cordones de esclerénquima. Iconografia. Gleason (1952: 128); Correll y Pul (1982: 1249, fig. 538); Diggs et al. (1999 1059, fig. 108). Distribución y ecología. Verbena scabra se dis- tribuye por las Antillas, el Caribe y el sudeste de Estados Unidos de América, donde se la encuentra generalmente en suelos húmedos o terrenos bajos, dos. Méndez Santos (2003: 8) la cita para Cuba como subespontánea naturalizada Observaciones. Schauer (1847) sinonimiza Verbe- na scabra bajo V. urticifolia. Perry (1933) las trata como especies distintas, diferenciándolas porque la última posee los dientes del cáliz fructífero no conniventes en la madurez, clusas de dorso liso apenas estriado y superficie estigmática subtendida por una ba. estéril; mientras que en V. scabra el cáliz posee dientes conniventes en la madurez, clusas de dorso reticulado y superficie estigmática ubicada entre dos prolongaciones estériles del estilo a modo de lóbulos obtusos. Este último carácter se observa únicamente en V. scabra. Verbena scabra se asemeja a V. carolina diferen- ciándose porque esta última es una planta subglabra a híspida con hojas generalmente sésiles a subsésiles, a veces con breve pecíolo, siendo V. scabra plantas de encia escabrosa ioladas. Moldenke (1967) diferencia la forma angustifolia por las hojas angostas r del estudio de numerosos ejemplares de dla. se pudo observar que el ancho de las hojas es un carácter muy variable en Verbena scabra por lo cual es imposible sustentar una forma basada en esos caracteres. En 1975 Moldenke describe la forma ternifolia por poseer tres hojas por nudo, en lugar de dos, y el resto de los caracteres similares a Verbena scabra. Méndez Santos (2003: 8) también menciona que hay ejemplares de V. scabra con tres hojas por nudo. Habiendo analizado abundante material se han encontrado numerosos ejemplos donde se observa en el mismo ejemplar nudos con dos y otros con tres hojas por lo cual esta morfología no merece valor taxonómico. Este taxón se incluye en el grupo informal Verbena por presentar los caracteres definidos anteriormente para el mismo. Tipificaciones y nomenclatura. Sprengel ( 1825) cita Verbena scabra de Muhlenberg como sinónimo de Lippia queretarensis Kunth; pero el nombre V. scabra Volume 97, Number 3 Olen ae 2010 Revision Tax ith de M 409 D F Fi I Can 14. A-D. Verbena urticifolia. —A. Aspecto Ty de la planta. —B. Flor con bráctea. A de gi pes _Sáliz fructífero con dientes no subconniventes. E, Verbena k pu T D ero con dientes anive —F. Detail a sésiles gcn e n. (US; E, F ntes, > bd Annals of the Missouri Botanical Garden Muhl. ex Sprengel es un nombre ilegítimo (McNeill et al, 2006: Art. 53). Verbena scabra Marnock también es un nombre ilegítimo (McNeill et al., 2006: Art. 53); y en este caso el taxón de Marnock es sinónimo de V. rigida Spreng. (véase O'Leary et al., 2007) AMERICA DEL NORTE. Co., California: San Bemardino Co. , Ross E ee o, 76 km N SR 6 in downtown Starke. own, Godfrey (MO). Texas: Jefferson Co., Bienen. fe 10692 As Virginia: Surry Co., Gray’s Creek, near Cross creek, Fernald 6863 (MO, NY). MEXICO. Baja California: 5 mi W of Rane ca. Mouth Sto. Domingo River, Wiggins & Demaree 4766 (NY) Coahuila: La Soledad, SW Monclova, Palmer 1040 (NY). ISLAS DEL CARIBE. BAHAMAS. Eleuthera, NE edge of North Palmetto, Correll & Correll 48999 (US). New Providence: West Bay St., Correll 51393 (MO). BERMU- DAS. N of Hamilton, niger: 373 (US). CUBA. St. Johns, Grisebach 639 (US). HAITI. Nippes: Mi a ae S. Estero, Eyerdam 432 (US). sae l. Creve f Westmoreland, 1/2 mi. E of Negril, Adams 10967 MO PUERTO RICO. Cabo viejo, Krug & Urban 767 (CORD). io Abajo State Tm Acevedo-Rodriguez 10747 1 Damas (MO). Peravia: San José Ocoa, river Ocoa, Jiménez 4738 (US). Santo Domingo: de la Vega, Constanza, Ekman 13985 (US). 22. Verbena simplex Lehm., Index Seminum (Hamburg) 17. 1825. TIPO: E.E. U.U. Tennes- see: Perry Co., 6.3 mi. S of Buffalo, 24 May 1972, R. Kral 46566 (neotipo, aquí designado, MO). Figura 13B—E. Hierba erecta, de 10—65 cm de altura, tallos ascendentes, ramificados de forma fastigiada desde la base, ésta a veces algo leñosa, plantas subglabras con pubescencia adpreso-estrigosa. Hojas de lámina entera, elíptico-linear, de Toa x 0.4-2 cm, subsésil, ápice agudo y base margen entero a irregularmente dentado hacia el ápice, dientes breves. Sinflorescencia frondosa, formada cladios solitarios o trímeros laxos, las florescencias es no superan a la principal, florescencias cilíndricas de 10-25 X 0.4-0.6 cm, en la fruetificación, flores y frutos dei imbrica- dn. Brácteas florales ovadas de o agado. de 0.32-0.5 em, margen piloso; cáliz de 0.4—0.5 cm con 5 dientes agudos de 1 mm, subconniventes en la fructificación, pubescencia estrigosa; corola de color lila o blanco, infundibuliforme, tubo corolino de 0.55-0.8 cm, viloso o gl pubescencia de pelos moniliformes en la garganta, limbo corolino desarrollado, de 0.6 em lat.; bres insertos hacia la zona apical del tubo corolino. Clusas ca. 2-2.8 mm, dorso longitudinalmente estriado, cara comisural lisa rru natomía caulinar con parénquima diii de dispiticióe erosos cordones de ro externamente, con estam- continua, presencia de esclerénquima no Distribución y ecología. Verbena simplex crece en el sur de Canadá, centroeste de Estados Unidos de América y en el estado de Baja California en México. Observaciones. Este taxón se incluye en el grupo informal tatae por presentar los caracteres definidos anteriormente para el mismo CLAVE PARA LAS VARIEDADES DE VERBENA SIMPLEX: CANADA, CENTROESTE DE ESTADOS UNIDOS DE AMÉRICA Y ESTADO DE BAJA CALIFORNIA EN MÉxICO 1. Hojas con pubescencia adpresa, estrigosa; piezas florales sin pelos glandulares 22a. var. simplex 1”. Hojas con pubescencia híspida o estrigosa; piezas florales con pelos glandulares breves E AAA m me es ee ee eee ee le we oo 22a. Verbena simplex var. simplex. Figura 13B, C. Verbena angustifolia Michx., Fl. Bor.-Amer. (Michaux) 2: 14. 1803, nom. illeg., non Verbena angustifolia Mill., Gard. Di ed. a 15. 1768. TIPO: E.E. U.U. “Hab. in P. kl ia, nro. 9" loli P no visto, P foto SI!; isotipo, SI!). ramp Moldenke, Phytologia 40: 468. 1978. TIPO Missouri: Franklin Co., Pacific, 4 i 1896, . Eggert s.n. (holotipo, NY no visto, NY foto SI!; isotipo, UC no visto). buses — albiflora Moldenke, e 10: 172. 964. TIPO: E. . Kan , Elsmore, 22 M 1957, R. L. McGregor 13217 M ex KANU no visto, KANU foto Hojas escasamente pubescentes con pelos poco densos, adpresos, estrigosos sobre las venas. Bráctea floral subglabra con el margen apenas piloso, cáliz con algunos pelos adpresos, estrigosos; raquis Su glabro. Número cromosómico. n = 14 (Dermen, 1936). Iconografía. Britton y Brown (1913: 96) (sub. nom. Verbena angustifolia); Gleason (1952: 132). Volume 97, Number 3 2010 O'Leary et al. 411 Revisión Taxonómica de Verbena Distribución y ecología. Esta variedad se la encuentra en terrenos rocosos y arcillosos del este de Canadá y centroeste de Estados Unidos de P a Observaciones. Perry (1933) dice que Verbena se asemeja morfológicamente a V. hastata, diferenciándose porque V. hastata posee florescencias más breves y angostas y las hojas son ovadas y ioladas, siendo elípticos y subsésiles en V. simplex. Moldenke (1940b) funda la variedad eggertii diferenciándola de la variedad tipo por poseer numerosas ramas surgidas desde la base, el análisis del ejemplar tipo no permite distinguir este taxón de Verbena simplex var. simplex, existiendo Simeon multiramosos (Fox 4910, NY) hasta al 32854, MO), por lo cual en la variedad eager se trata bajo la sinonimia de V. simplex var. La forma albiflora de Moldenke a se diferencia por las corolas blancas, carácter taxonómi- camente irrelevante por lo cual en el presente tratamiento se trata esta forma como sinónimo de la forma tipo. Tipificaciones y nomenclatura. La mayoría de los ejemplares tipo de Lehmann se encuentran depo- sitados en S, sin embargo, Mia Ehn (comun. pers.), curadora de ese herbario, no ha podido localizar ningún material original de Verbena simplex. Tampoco se ha localizado material original en otros herbarios y por lo tanto se debió neotipificar este taxón. Se eligió un ejemplar que coincide con la descripción del protólogo. oom examinado. CANADA. Ontario: Ms Mas NY). Quebee: Ile Ste-Helene, ca. Montreal, Roy 3681 (SI, US). E.E. U.U. Alabama: Dekalb ^ 3.5 mi. S jet. Ala. 35, Ft. Payne exit, kl. 52854 (MO). : Clark Co., Okolona, Demaree 17808 (NY). T ker Co., aoc Mtn., betw. 5 Fayette & renton, Cronquist 5280 (MO). Ilinois: Cook Co., Chicago, — Island, 22 July t Braun s.n. (US 2712369); Will > Nes , 18 June 1898, Umbach s.n. (US ua p e .. 3 mi. E of Crawford Co. Line, Era Iowa: Cumberland Co., Backen Somes 3301 (US. K : Johnson Co, 1.5 NE Edgerton, Youngjune Chang 745 (NY). Kentucky: ‘ee Cumberland River, Eggleston 4458 (NY). Washington Co., SW Dargon, round t ; : Berkshire Co., Sheffield, Louis Co., (MO). . Bush 7647 (NY, US). North Carolina: 7 mi. W Stone Co., 22b. Verbena simplex var. orcuttiana (L. M. Bot. Gard. 20: 284. 1933. TIPO: México. Baja California: Hanson's Ranch, 30 July 1883, C. R. Orcutt 909 (holotipo, GH no visto, GH foto SI!; isotipo, NY no visto, NY foto SI!). Figura 13D, E. Hojas con pubescencia hispida o estrigosa sobre ambas caras, más densa en la cara abaxial. Bracteas cáliz con igual pubescencia; raquis con pelos andulares breves. Distribución y ecología. Esta variedad es endé- mica de México, del estado de Baja California, donde es común en tierras secas y arenosas. Observaciones. En 1933 Perry funda Verbena orcuttiana distinguiéndola de V. simplex á pubescente y por poseer pelos la breves en las piezas florales. Si bien las diferencias sostenidas por la autora son reales se considera que estos caracteres no son lo suficientemente importantes como para sostener una especie. Perry (1933) cita cuatro ejemplares, del estado de Baja California, en México. Como no se ha encontrado material con tales características en otras regiones, es probable que se trate de una variedad morfológica de Y. simplex y en el presente tratamiento se la considera como La variedad orcuitiana y la variedad tipo poseen distribuciones separadas, siendo la primera endémica del estado de Baja California, mientras la variedad se encuentra en el centroeste de Estados Unidos hasta Canadá. O. Baja Calif CA Jay ims C Orci c gi ie 56116) Sema 1/2 mi. from Botella, Moran 13604 (MO, Lt iss Las Filippi, sierra Juarez, Wiggins 9157 (US); San Domingo & Queretaro, Wiggins 5508 (U 23. Verbena stricta Vent., Descr. Pl. Nouv. 53. 1800. TIPO: E.E. U.U. “Regione Illioensi”, s.d., s. coll. (holotipo, P no visto, P foto SI!; isotipo, SI!). Figura 8A, B. Verbena rigens Michx., Fl. Bor- es MAE 14. 1803. TIPO: E.E. U.U. *Hab. in D Mk coll. (holotipo, P no visto, P foto o SI! isotipo, SI!). Verbena stricta f. roseiflora Benke, TIPO: E.E. U.U. Kansas: Cloud y 1929, R. C. Benke 5164 (holotipo, F no visto, F foto SI! : isotipos, GH no no visto, NY no visto, NY foto SI!, US no visto, US foto SI. Hierba erecta, de 0.3-1(-2) m de altura, tallos itarios o varios desde la base, a cds set d e RE Ea iae Lee pa EENI 412 Annals of the Missouri Botanical Garden pubescencia densa, hirsuto canescente, pelos de más de 1 mm. Hojas de lámina entera, elíptico-orbicular, de 3.5-10 X 3-5 cm, sésil a subsésil, base cunead ápice agudo u obtuso, margen inciso serrado, rugosas, gruesas, pubescencia híspido-estrigosa en la cara adaxial y muy densamente pilosa en la cara abaxial, con pelos de 1 mm, prominentemente reticulado eros, mayor a un orden de ramificación, las florescencias laterales no superan a la principal, florescencias cilíndricas de 25—30(—40) X 0.6-0.8 cm, pedunculadas, flores y frutos densamente imbricados. Bráctea floral elíptico angosta de ápice agudo, de 0.33—0.6 cm, de similar longitud que el cáliz, margen ET cáliz de 0.35- 0.6 cm, con 5 dientes agudos de ca.1 mm, sub- conniventes en fructificación, eli híspido- en piezas, a veces con escasos pelos glandulares breves; corola de color violeta, azul, rojizo, lila o blanco, infundibuliforme, tubo corolino de 0.6—0.8 cm, angosto, externa e internamente viloso, pubescencia de pelos moniliformes en la ta, limbo desarrollado de 0.5-1 cm lat.; estambres insertos hacia la zona apical del tubo corolino. Clusas de 2.5-3 mm, dorso longitudinalmente estriado, cara comisural lisa. Anatomía caulinar con parénquima clorofiliano de disposición continua, presencia de numerosos cordones de esclerénquima. Número cromosómico. 2n = Noack, 1937). 14 (Dermen, 1936; grafía. Britton y Brown (1913: 96); Gleason M 132); Sanders (2001: 342, fig. 2, o). Distribución y ecología. Verbena stricta habita el este y centro de Estados Unidos de América, creciendo en suelos limosos y arenosos. Observaciones. Verbena stricta se caracteriza por las florescencias densas compactas y anchas, con flores conspicuas, por la abundante pubescencia hirsuta, y por las hojas elíptico-orbiculares. erry (1933) dice que se trata de un taxón difícil de delimitar ya que tiene tendencia a hibridizar con especies vecinas. Perkins et al. (1975) en un estudio de ap interespecífica con m de Verbena stricta, V. halei, V. urticifolia y V. bracteata, simpátricas k un condado de Oklahoma. concluyen que V. stricta es una especie fuertemente alógama taxones cercanamente aa. ded la hibrida- ción entre miembros del complejo es factible, y de hecho muchos posibles híbridos han sido descriptos por Moldenke (1962: 272, 1964h: 195). Verbena stricta es morfológicamente semejante a V. macdougalii (véase diferencias bajo ésta última especie). Moldenke (1964h: 190) cita Verbena rugosa Michx. y V. scoparia Tausch. como sinónimos de V. stricta, sin embargo los ejemplares tipo de todos estos taxones no se han localizado. Perry (1933) cita Verbena stricta var. mollis Torr., V. mollis Raf., V. cuneifolia Raf. y V. stricta f. albi Wadmond como sinónimos de V. stricta, sin embargo los 1e tipo de todos estos taxones no se han localiza Este taxón se incluye en el grupo informal Hastatae por presentar los caracteres definidos anteriormente para el mismo Tipificaciones y nomenclatura. El tipo de Verbena stricta se basa en un ejemplar cultivado en Jacques Martin Cels Nursery de Paris en 1800, y depositado n P. nk (1847) y Perry (1933) mencionan Verbena alopecurus Cav. (Cavanilles, 1802: 68) como sinónimo de V. stricta. El ejemplar tipo de V. alopecurus se trata de una ven cultivada en el Hort. Botánico de Ma se menciona en el protólogo, y ine cs en "MA. Sin embargo no se ha localizado este ejemplar; Perry (1933) dice que existe un fototipo del mismo en MO, pero tampoco se ha hallado. También se consultaron los herbarios P, BM y G ya que los ejemplares de Cavanilles se encuentran depositados en esos herbarios, pero no se halló. Rafinesque (1832) en el protólogo de Verbena mollis sólo menciona “V. mollis Raf. var. of V. stricta T. 360”. El ejemplar tipo de V. stricta var. mollis Torr. debería estar en NY ya que la base del herbario NY fue el herbario de Torrey. Allí hay cinco ejemplares de V. stricta, ninguno dice “var. mollis” y además tres de ellos son posteriores a 1827. Por lo tanto el tipo de este taxón no ha sido hallado. Wadmond (1932) diferencia la forma albiflora por la corola blanca. Perry (1933) sinonimiza esta forma bajo la forma tipo. Material adicional examinado. E.E. U.U. Arkansas: Craighead Co., St. Francis River, Demaree 30772 (NY) Colorado: Denver Co., Denver, Eastwood 90 (SI, US) Illinois: Co., near Burton Creek, Evers 197 Indiana: East Chicago, E 2810 T Iowa: Louisa Co., SE B sec. 5, Davidson 858 (US). Kansas: m Co., Syracuse, Thompson 154 im Kentucky: Larie Co., oe Reed esse (MO). Michigan: Delta Co., Burt Bluff, M. . Minnesota: Henneping Co., Ft a 525 (US); Minnesota Co., eT Mash 10478 (NY). Missouri: Reynolds Co., near Suttons Bluff, 3 mi. NW of Centerville, D'Arcy 4644 braska: Nemaha Co., Peru, jp 20 (US); Platte Co., 1/2 mi. S Colu Co., Granton, 21 Sep. SN. Ke dci ss 243275). New York: Essex Co., Ticonderoga, Reed 93572 Volume 97, Number 3 2010 O'Leary et al. 413 Revisión Taxonómica de Verbena (MO). North Dakota: Leibon, 25 July 1944, s. coll. (US 2008469). Ohio: Wood Co., NW Fish Cemetery, 1/2 mi. N New Rochester, Cusick 34007 (NY). Oklahoma: Comanche Co., Medicine Park, Wichita Natl. Forest, Demaree 12996 (MO). Pennsylvania: Lancaster Co., Conewago, New Red eser, 27 Sep. 1901, Heller s. .n. (US 407055). South Wildlife area, Higgins , Iowa, Fink 251 (US). Wyoming: Platte Co., Hansie. Nelson 505 (US). 24. Verbena supina L., Sp. Pl. 1: 21. 1753. TIPO: [España.] s. loc., s.d., Loefling 16, Herb. Linn. 9.1 (lectotipo, designado por Moldenke [1965a: 255], S no visto, S foto SI!). orgs petiolulata H. Lindb., Acta Soc. Sci. Fenn., r. B, Opera Biol. 2(7): 28. T TIPO: [Cyprus]. ca: "in arenosis juxta opp. Larnaca", 27 June 1939, H. Lindberg af uses H no visto; isotipo, K no visto, K foto SIN. Verbena supina f. erecta Moldenke, reres 11: 259. 1965, syn. nov. Verbena supina var. erecta (Molden x Munir, L Adelaide Bot. Gard. 20: 62. España [Spain]. PO. in waste diet n at Algeciras, 24 June 1887, Elisée rchon 81 (holotipo, CB no visto; isotipos, BR no hong o S no visto, S foto SI!). ocumbe egypt.-Arab. 10. 1775. argines agronum Aegypti”, s.d., s. coll. (holotipo, C no visto, C foto SI!). Hierba decumbente a procumbente principalmente en la base de ramas, tallos ascendentes y semierectos hacia el ápice, hasta de 50 cm de altura, a veces erectos desde la base, pubescencia variable, desde híspida, estrigosa a subglabra, en ocasiones con algunos pelos glandulares. Hojas de 0.8-4 X 0. 3 em, de lámina dividida, pinnatilobada a pinnati- partida o bipinnatipartida, ápice obtuso, pecíolo ancho angostado, base cuneada, lóbulos o lacinias oblongas, margen subrevoluto dentado o entero, ambas caras la principal, cilíndricas, breves y densas en antesis, : 2 cm alargándose hasta 6 cm en la fructificación, 50.6 cm lat., pedúnculos estrigosos, ligeramente . Veni subpediceladas, en la fructifica- et el pedicelo floral se alarga levemente hasta 5 mm; Piu floral ovado angosta, de 0.1-0.2 cm, 03 marginalmente ciliada; cáliz de 0.18- TA híspido o 0 estrigoso, a veces con algunos pelos glandulares breves, 5 dientes triangulares poco Tore, subconniventes en fructificación; corola - “e color lila o rosa, infundibuliforme, tubo corolino de 925-045 cm de limbo pee desarrollado, externa- . pente glabra, n la garganta, estambres p insertos hacia la zona soil del tubo corolino. Clusas de 2 mm con cara dorsal lisa y comisural subpapilosa. Anatomía caulinar con parénquima clorofiliano de disposición continua, cordones de esclerénquima en los cuatro ángulos. Número cromosómico. 2n — 14 (Silvestre, 1986; Pastor et al., 1988). Iconografía. Munir (2002: 59, fig. 5). Distribución y ecología. Verbena supina es nativa de la zona mediterránea, creciendo en terrenos arenosos. Še la halla introducida y naturalizada en Europa templada, en el noreste de África, Medio Oriente y Australia. Observaciones. Verbena supina se asemeja a V. gracilis y a V. canescens, pero se diferencia de ambos porque en este taxón las flores son pequeñas con brácteas de menos de 0.2 cm. À su vez, la distribución es diferente, siendo este taxón del Viejo Mundo mientras que los otros dos son americanos. Munir (2002) trata la forma erecta de Moldenke (1965a: 259) como una variedad, y explica que se diferenciaría de la variedad tipo por los tallos erectos o suberectos desde la base, en vez de decumbentes y por ser glabra o lige ramente pubérula, en lugar de estrigosa. El análisis del Mr ¿sma tipo permitió determinar que este taxón es un sinónimo na s Rl (1933) funda Verbena supina var. minor diferenciándola por las hojas menos divididas y las florescencias más breves, hasta de 5 cm. El ejemplar tipo es de Libya, pero no ha sido localizado. Munir (2002) cita V. radicans Moench como sinónimo de V. supina, el ejemplar tipo no se ha localizado. En algunos casos puede haber algunos pelos glandulares breves en cáliz y raquis. Este taxón se incluye en x grupo informal Bracteosae por presentar los caracteres definidos anteriormente para el mismo. Tipificaciones y nomenclatura. En el protólogo de Verbena supina: dice “Habitat in Hispania”. Moldenke e citó Herb. Linn. 35.16 (LINN) como tipo. Sin su tipificación previa: Loefling 16, Herb. Linn. 9. 1 (Moldenke, 1965a: 255) es válida por lo cual pre ser retenida. Munir ( 1949; sin embargo recien en 1965 licación la tipificación. Munir (2002: 57) debate la tipificación. atrial adicional examinado. ÁFRICA. ALGERIA. am we Haloula, Nov. 1827, Munby w E Abi 5M 1911 A. Faure s.n. (NY); Orán: cerca Oran, 9 May e 1909, Gaos (40 À AUR sn. (MO); Assiut UNIES ARDEN ES IS ere 414 Annals of the Missouri Botanical Garden University, Mar. 1962, Nabil El Hadidi s.n. (MO 1908725). Cairo, im ET Ni-Thale, 1880, Schweinfurth n. (US ). ERITREA. Amasen, Asmara, Pappi 4331 €L u sis esas P. Sidi A Mk Nador, SD; s. loc, Nov. 1938, F. hee s.n. d : xb Habibi, 1910, M. Gandoger = pe^ 116765); Kas Faraoum, aes M. Gandoger s.n. (MO 116767); Maroc, Ulad Settut, a, Sennen & Mauricio 8500 (SD); Goulimine, 7 km oe ok Schuhwerk 90/ 219 (NY); Dj. Jahroun, 1910, M. Gandoger s.n. (MO 116766); 6 km N Tiznit, nr. El Mader el toe "al et al. 540 (MO); NE of me Youssef Ben Tachfi Scheme, 3 June 1974, BM Expedition 332 (MO). qeda a Akiouat, Se Adam 13072 (MO). SENEGAL. Dagana, Richard Toll, Adam 12959 wae TUNISIA. Gales, 1907, M. Gandoger s.n. eu IRAQ. B. E B 2a 30 km E Bagdad, on Kut HW, Ba gdad Li iwa, & ihi "ol 4003 (NY); 30 May 1934, H. Field & Y. Lazar 530 (NY) . Sphakia, MR em getty Bács-Bodrog: sup (US); Mezö Túr, 70-90 m, Borbás 934 I PORTUGAL Ribatejo: Golega, rio mE: Rainka 2419 (US). OCEAN STRALI Australia: Gawler Range, Lake Everard, nae 2106 (SI). 25. Verbena urticifolia L., Sp. Pl. 1: 20. 1753. TIPO: Herb. Linn. 35.13 (lectotipo, designado por Méndez Santos & Cafferty [2001: 1140], BM-LINN no visto, BM-LINN foto SI!). Fig- ura 14A-D. Verbena urticifolia var. simplex Farw., Pap. Michigan Acad. Sei. 3: 103. 1924. Verbena urticifolia f - simplex (Farw.) Moldenke, Phytologia 44: 134. 1979. TIPO: E.E. U.U. : Oakland Co., near Lakeville, 11 Oct. 1922, 6443 (lectotipo, aquí dido. BLH no vidit, BLH foto SI!). iM M. Perry & Fernald, l. 450, figs. 5-8. 1936, syn. nov. HPO: EE. U. X UE — Beach, rich woods, 10 Sep. 1935, M. L. Fernald, i Long & J. Fong 5013 (holotipo, GH no visto, GH foto SI!). Hierba erecta, hasta de 1.5 m de altura, tallos solitarios, ramosos hacia el á ápice, glabros a esparcida- mente hispídulos con pelos hasta de 1 mm, distancia- dos. Hojas de lámina entera, ovada a oblonga, de 7-12 X 5-8 em, pecíolo de 2-2.5(-4) em, base cuneado- ápi : ramificación, de aspecto es profu- sión de florescencias, las florescencias laterales no 0.3 cm. Brácteas florales de 0.1-0.15 cm, ovadas de t agudo, subglabras a finamente “ ur as, margen piloso, cáliz ca. 0.2-0.25 e e sobre las costillas a escas con algunos pelos glandulares breves, con 5 triangulares, no conniventes en la difci dejando a la vista los mericarpos en el fruto; corola de color blanco, a veces lila, infundibuliforme, tubo corolino breve apenas exerto del cáliz, de 0.28- e i 5 un > E e £ % z % dit = 5 Èi $ estambres insertos hacia la zona apical del tubo stinn Clusas de 1.8 mm, de dorso liso a ligeramente estriado, cara comi lisa. peo — con pene elorofiliano de de tipinin. Número cromosómico. n = 7, 2n = 14 (Junell, 1934; Dermen, 1936; Noack, 1937; Arora, 1978). Iconografía. Britton y Brown (1913: 95); Perry y Fernald (1936: pl. 450, figs. 1-8); Gleason (1952: 30). pr Distribución y ecología. Verbena urticifolia es común en el centro y noreste de Estados Unidos de América, creciendo en suelos orgánicamente ricos, arenosos o arcillosos, muchas veces en terrenos húmedos Observaciones. Verbena urticifolia es afín a V. scabra (véase diferencias en observaciones bajo este último taxón). También se asemeja morfológicamente a V. carolina y V. ehrenbergiana, distinguiéndose V. carolina por poseer generalmente hojas sésiles a subsésiles, mayor pubescencia, y cáliz fructífero con dientes conniventes. Verbena ehrenbergiana se diferencia por poseer hojas trilobadas y por la ausencia de pubescencia glandulosa en sus piezas es. Verbena diffusa Poir. se basó en un ejemplar cultivado en el herbario de Paris, como se indica en el P y depositado en el herbario Desfontaines. último es el motivo por el cual Sprengel le didus el nombre a Desfontaines: V. diffusa Desf. ex Spreng. (en Linnaeus, Syst. Veg. ed. 16, 2: 748. 1825. nom. illeg.) pero en realidad se refiere a V. diffusa de Poiret. Perry (1933) coloca este taxón bajo la sinonimia de V. urticifolia. Moldenke (1965c: 410) sefiala que probablemente Verbena | incarnata . (Rafinesque, 1832) sea únicamente una variante del color de las flores de V. urticifolia, motivo por el cual la trata como una variedad de este último taxón y posteriormente como una forma. No se ha podido localizar el ejemplar tipo este taxón proveniente de Pennsylvania en Estados Unidos de América. Volume 97, Number 3 2010 O'Leary et al . 415 Revisión Taxonómica de Verbena Farwell (1924) al describir Verbena urticifolia var. simplex la distingue de la variedad urticifolia por el menor tamafio de sus flores, frutos y clusas. Perry (1933) y Moldenke (1965b: 328) tratan esta variedad como sinónimo de V. urticifolia, criterio aquí aceptado a pesar de que Moldenke (1979) 15 años después vuelve a separarla bajo la categoría infraespecífica de diferencian V. ñas y florescencias más laxamente agrupadas. Sin embargo, estos caracteres son muy variables dentro de V. urticifolia por lo cual en este trabajo se trata bajo la sinonimia de este último taxón. Este taxón se incluye en el grupo informal Verbena por presentar los caracteres definidos anteriormente para el mismo. Tipificaciones y nomenclatura. Moldenke (1965b: 334) sugiere que el ejemplar coleccionado por Linnaeus en el Clifford Garden, y preservado como Hoja 5 (BM 557562 no visto, foto SI!) sería el tipo de Verbena urticifolia. Sin embargo no hace una a efectiva según el código (McNeill et al., 2006: Art. 9) y Méndez Santos y Cafferty (2001: 1140) recién lectotipifican este nombre con un ejemplar del LINN. Si bien el ejemplar de BM también constituía material original eligieron el de LINN porque era el ejemplar más completo. Farwell (1924) al describir la variedad simplex mencionó dos sintipos: Farwell 6443 y Farwell 6463. El ejemplar Farwell 6443 fue elegido lectotipo porque es el ejemplar mejor conservado y coincide con la escripción en el protólo Mate uie PE examinado. E.E. U.U. Alabama: Jackson ms of Tennessee River, 2.2 mi. SE ee, Kal 53201 (MO). Ashley Co., Dry a 0.4 mi. N Ark 52 and Miller chapel, Thomas 97761 tieut: Woodbury, Parker 75150 (NY). Mi- ane Madison Co., P.O. Collinsy ille, nr 27288 (NY). diana: Lake Co., Indiana Lake, ake, Lansing 2906 5 (US) lows: Ciy Lake, Barker 1990 ie A Kentucky e Co. W — ceburg on Rd. 8, Buddell 3200 (NY). Louisiana: Parish, Tensas River National Wildlife refuge, monas 140861 (N : Baltimore, Reed 40998 = husetts: Brookline, Lost Pond, Lourteig 1719 me nepin Co., Fort Snelling, 25 Aug. 1891, Hen A tn. (US 670319). Missouri: St. Charl 1077376) P o Some i 1330 (MO). New e Rockland Co., Sloatsburg, Nee et al. * (CTES, SI). North Carolina: Watauga Co., ater Farm, 293 Will Glenn e id, Crosby 17795 5 (MO). Ohio: Co., Cedar sw ae 11704 (MO, is A 294, Ricksecker s.n. (US s 1). urtain ce 9 mi. SW Idabel, 12412 (US). lege ei: Butler Co., N Harmony, Kensy 552 (US). Rhode Island: Bristol Co., Barrington, Seymour 21569 (MO). South Carolina: Aiken Co., Savannah River Hickory Creek, 8 mi. S Denton, Whitehouse 16426 Virginia: Albemarle Co., Shenandoah Natl. Park, Moldenke 19225 (SI). Wisconsin: Chippewa Co., riviere de Manitou, Green Bay, s.d., — s.n. ^ US 2546793); Dane Co., Arbor hills, Braga 7? xutha Lehm., Index S (Berlin) 26. W, L. T: 8. 1834. TIPO: E.E. U.U. Laoi ee Coe Parish, La. 27 & La. 82 betw. La. 1141 & Jetty Rd., 16 July 1988, R. D. Thomas, C. Slaughter & C. McCraney 105919 (neotipo, aqui designado, MO!" NY!). Figura 15. Verbena caerulea Vatke, Index Seminum age LE L . Berol., 20 Oct. 1876 strigosa C. E.E. U.U. “V. strigosa Hook., N. Orl. - Walp.”, s.d., s. coll. Üldlipe, la no visto, K foto SI!). Hierba erecta hasta de 1.8 m de altura, pubescencia adpresa o estrigosa abundante, los de ca. 1 mm, sin pelos glandulares. Hojas de 4-6(-12) X 1535) cm, sésiles, de lámina oblongo-ovada, las basales tri a tripartidas, lóbulo central marcadamente inciso- — dientes agudos prominentes, ápice me base fi NM si = entonces ln venas prominentes en s eies, i abes lage con pubescencia cara cáliz, 0.3-0.45 cm, de ápice agudo, prierons ciliado; cáliz ca. 0.35 cm, con 5 limbo desarrollado; al del tubo corolino. Clusas de 2 mm, dorso I di estriado, cara comisural lisa o papilosa Anatomía caulinar con parénquima clorofi- T z continua, presencia de numerosos la zona Missouri Botanical Garden Annals of the 416 UN à pet SA a SN 5. Verbena xutha. —A. Aspect de Clausen & Tiapido 5371 (NYS © la planta. —B. Detalle de pubescencia del tallo. —C. Flor con Figura 1 bráctea. A-C Volume 97, Number 3 O'Leary et al . 417 Revisión Taxonómica de Verbena Nümero cromosómico. n = 21 (Lewis & Oliver, 1961, sub. Verbena matthesii Turcz.). Distribución y ecología. Verbena xutha se distri- buye por el sur-sudeste de Estados Unidos de América, de enia a Texas, crece en terreno arcilloso y se Observaciones. Verbena xutha es fácilmente reco- nocible por su hábito erecto, hojas grandes, yet ramente trilobadas o tripartidas en la abundante pubescencia estrigosa y sus Mortal largas y laxas. Este taxón se incluye en el grupo informal Hastatae por presentar los caracteres definidos anteriormente para el mismo. Tipificaciones y nomenclatura. Los ejemplares tipo de Lehman están depositados en S; sin embar, Mia Ehn (comun. pers.) no ha podido localizar el tipo de Verbena xutha y no se hallaron posibles isotipos en ife tahaa i had Tho Las hb te tayo necesita ser neotipificado. Se buscó un ejemplar que coincidiera con el protólogo y que fuera de la misma área geográfica, lo que es ambiguo dado que sólo se indica que las i a] del estado de Louisiana en Estados Unis de Moldenke (1965d: 498) cita Verbena matthesii como sinónimo de V. xutha; los tipos de Turczaninow están principalmente depositados en KW y LE, se con- sultaron estos herbarios pero no se halló el ejemplar. Material adicional examinado. . Alabama: Baldwin Co., river . Kral 50477 (MO). Arkansas: Miller Garland City, W bank Red River, E of Ark. 134, Thomas et al. 151144 (NY). ade Wilkinson Co., 2 mi. W Ft. Adams, Rogers et al. 8453 (MO). Louisiana: Plaquemines Pai Pointe 3 a la Hache, as 123 (US). Mississippi: arrison Co., near Pass Christian, May 1931, —— & unii n. (NY nti Texas: . e 2.5 mi. S Gonzales, Clausen & Trapido pes (NY, US): ravis Co., Austin, Sates farm, dd. 11921 (CTES, NY). Taxones Duposos Los siguientes taxones de Verbena no se puede establecer si se pan bajo la serie Verbena o la sene P, — E roid el motivo por el cual se tratan como Verbena na goyazensis Moldenke, Bull. Torrey Bot. Club 77 des e Goiás: Goiás Vas Rio do Pei elxe, 7 Aug. 1 Hashimoto 663 (ho guta He Sp foto ED. on. NY no visto, NY foto ». E material del cual se dispone resulta insuficiente ~ Para resolver este taxón ya que no se ha e ninguna colección y únicamente se cuenta con fotos del ejemplar tipo y un fragmento pequeño a partir de este ejemplar —— L. Rob. & Greenm., Amer. J. Sci. == 42. 1895. TIPO: Ecuador. Galápagos Islands: Du E Aug. 1891, €. Baur 180 (holotipo, GH no visto, GH foto SI!). En la Flora de las Islas Galápagos, Wiggins y Porter (1971) diferencian Verbena grisea del resto de los. taxones de 7 i bipinnatipartidas y por la pubescencia más densa. Vya: der Werff (1977) 7) había reconocido como único taxón válido para las islas a V. townsendii. Se comparó V. grisea con este taxón y se observó que se diferenciaría por la mayor pubescencia y por las florescencias más anchas y densas del ejemplar tipo de V. grisea. Como no se han encontrado más ejemplares de este taxón y sólo se cuenta con el ejemplar tipo, se lo trata como taxón dudoso a la pera de más material. Verbena townsendii Svenson, Amer. J. Bot. 22: 253. 1935. TIPO: Ecuador. Galápagos Islands: ne Island, Academy Bay, 10 Hig 1930, 249 (holotipo, BKL no BKL foto SI: -— CAS no visto, CAS foto sit, GH no visto). Verbena galapagosensis Moldenke, Phytologia 2: 55. 1941 TIPO: Ecuador. Galapagos : Albermarle Island, Cowley Bay, 10 Aug. 1905, A. Stewart 3318 (holotipo, NY no visto, NY foto SI!; isotipos, CAS no visto, CAS foto SI!, SI). Verbena stewartii Moldenke, Phytologia 2: 56. 1941. TIPO: Ecuador. Galápagos Islands: Albemarle , Tagus Cove, 27 Mar. 1906, A. Stewart 3320 (holot ipo, NY no visto, NY foto SI!; isotipos, F no F foto SI, SI!, UC no visto, UC foto SI!, US no X US foto SI!). Moldenke ponen funda Verbena galapagosensis y V. stewartii, siendo el ejemplar tipo de la primera un paratipo de V. townsendii Svenson (Svenson, 1935: 253). Moldenke (en Wiggins & Porter, 1971) diferencia estos taxones principalmente por la morfología foliar, siendo las hojas de sus dos especies enteras lineares, y en V. townsendii trisectas. Sin embargo, van der Werff (1977) explica que las hojas pueden variar desde enteras lineares, hasta profunda- mente divididas, por lo que concluye que los taxones fundados por Moldenke sobre la base de diferencias ón escasamente coleccionados. Se cuenta únicamente con fotografías de algunos ejemplares, principalmente colecciones de Anne y Henning Adsersen del año 1974, depositados en C, pero esto resulta insuficiente para resolver la posición taxonómica de los mismos dentro del género Verbena. 418 Annals of the Missouri Botanical Garden Literatura Citada es R. S. 2000. Verbena. 456-451 en Flora of the Desiert wasa radit tend Mexico. Arora, M. I Chromosomal ee in Verbena University of Arizona Press Taa A CE EE ytologia 43: 525-53 ernándes, R. B. & B. Verdcourt. "1989. A new African Asad, * 1980. ccm number reports LXIX. subspecies m V. officinalis L. Bol. Soc. a x Taxon 29: 130. 305-310. Barber, S. 1982. Taxonomic studies in the Verbena stricta ). — F. Mueller. 1870. Verbena: Pp. 35-3 7 en G. , Flora Australiensis, Vol. 5. Reeve & Co., Bir, S. S. & M. l. S. Saggoo. i Chromosome number reports LXV. f 28: 630-63 Briquet, J. 1895, ; Fp: M Engler & K. Prantl E Die pr Pflanzenfamilien IV, 3a. Wilhelm Engelmann, Leipzi ————. 1907. Decades ross Novarum vel Minus cognitarum. Annuaire Conserv. Jard. Bot. Genéve 10: 99-108. Britton, N. L. € A. Brown. 1913. Verbena. Pp. 94-97 en N. L. Britton & A. Brown (editors), An Illustrated Flora of the Northern United States, ed. 2. Charles Scribners Sons, Bini, R. 1812. Verbena. P. 41 en W. T. Aiton, Hortus Kew ed. 2, Y Longman, Bubani, P. 1897. Flora Presses, Vol. 1: 378. Ulrico Hoepli, Milan. Cavanilles, A. J. 1802. Descripción de las Plantas, 68. id. na. Pp. 306-307 en A. W. Chapman, Flora of the udis United States. lvison, Phin Cockerell, T. D. A. 1911. Verbena. P. 204 en F. P. Daniels, M Flora of Boulder, Colorado, and Vicinity. University of Coleman, N. 1874. M P. 28 en N. Coleman, Cat. Fl. Pl. S. Pe Michi Correll, D. S. & H. B. Correll 1982. Verbena. Pp. 1246-1250 en Flora of the Bahama Archipelago. J. Cramer, Vaduz, Liechtenstein. D'Ambroggio de Argüeso, A. 1986. Manual de Técnicas en am ue Hemisferio Sur, Buenos Aires. vis, E. 1945 . Nat. Leaflet (Lower Rio Grande Valley Ai Club) 2:. 4. De la Peña, M. R. & J. F. Pensiero. 2004. Plantas Argentinas. atál Nombres Comunes. Editorial LOLA. Buenos Aires. Dermen, H. 1936. Cytological study 1 hybridization in tw sections of Verbena. Cytologia T: 160-175. Diez, M. J., J. Pastor & L Fernández. 1984. Números cromosomáticos de plantas occidentales, 297-306. Anal jud. Ba Madrid L 191-194. 9 Diggs, G. M., B. L. Lipscomb & R. J. O'Kennon. 1999. eter pec en Flora of North Texas. Botanical Research Institute of Texas Bot. Misc. 16. NN. — J. 1732. Hortus Elthamensis, Vol. 2: 207-437. Er LEN Ewan. 1981. BEEN ae Utrecht. Farwell, O. A. 1924. Notes on the Michi gan flora, Part VI. Pap. Michigan Acad. Sci. 3: 87-103. € ege J R. Gamarra. 1993. Herbarium m. Fontqueria 36: 67-108. — Manta F. & S. Silvestre. 1985. Números cromosó- cos para la flora española. Números 409—421. Lagasca- lia 13: 313-318. Ghaffari, S. M. 1987. Chromosome counts of some angio- sperms from Iran II. Iran J. Bot. 3: 183-188. Gibson, D. N. 1970. Verbenaceae. En P. C. Standley & L. 0. ro — Flora of Guatemala. Fieldiana Bot. 24(9): 1 Gilibert, J. z inn. Flora Lituanica pe Vol. 1 Gleason, H. A. 1952. Verbena. Pp. 126-133 en The x Britton and Brown Illustrated de of the Northeastern United States and Adjacent Canada, 3rd ed. Macmillan Publishing Co., New York. Gray, A. 1856. Verbena. Pp. 298— A Manual of the Botany of the Northem United ue heii — “Siswa ss € xi of the Mississippi. Georg Putnam & Co., . 1878. s Flora of North America, Vol. 2(1): Greene, E. L. 1888. New Species from Mexico. Pittonia 1: 153-159 Henderson, M. & J. G. Anderson. 1966. Common weeds o th Africa. Mem. Bot. Surv. South Africa 37: 259, a 128. — 2 J. 1974. Clasificación de la arquitectura de las hoj M pa as. Bol. Soc. ore Bot. A 1-26. ua PEs NEL ER 1990. Index Bade: Part I: The is e the te World, 8th ed. New York Botanical Garden, Bronx Hooker, W. J. x On the species of the = aqa ied genera. Bot. Misc. 1: 159— Huang, S., Z. Chen, S. Chen, X. Huang, Q. "Oe X Sh. 1986. Plant chromosome count (3). Subtrop. Forest. "Sei. & Technol. 4 50-56. — Z. Zhao, Z. Chen, S. Chen & X. Huang. 1989. Chromosome counts on one hundred species and infra- specific taxa. Acta Bot. Austro Sin. 5: 161-176. Jepson, W. L. 1943. Verbena. Pp. 3 n A Flora of D Vol. 3(2). Vinireuity of California Press. arie S. 1934. Zur Gynüceummorphologie und Systematik Verbenaceen und Labiaten. Symb. Bot. Upsal. 1(2): 1 129 Koul, A. K. A. K Wakhlu & J. L. Karihaloo. 1976. Chromosome numbers of some sar m of I Infor (Western Himalayas) I. Chromosome Kunth, c S. 1818. Verbenaceae. Pp. 244-285 en F. Humboldt, A. Bonpland & C. S. Kunth, se Genera et Species Plantarum (quarto el) Vol. 2. P. Lawrence, G. H. M. 1951. fe 746-141 en i enin of Vascular Plants. Macm y, New York. Lewis, W. H. & R. L. x. 1961. Cytogeography and v of North American species of Verbena. Amer. J. 48: 638—643. Line J. 1951. Glosología de los Términos Usados en Botánica. Fi Miguel Lillo, Tucumán, Argentina. Hu C. 1738. Hortus Cliffortianus. Amsterdam. Volume 97, Number 3 O'Leary et al . 419 Revisión Taxonómica de Verbena 1753. Verbena. Pp. 18-21 en Species Plantarum, lst ed., FET 1. Stockholm Lóve, A. 1982a. Chsnbdcseq number reports LXXV. Taxon 31: i . 1982b. Chromosome number reports LXXVI. Taxon 98. H. G. Galeotti. 1844. Enumeratio img Bruxelles 11(2): 320—324. Martínez, S., S. Botta & M. E. Mülgura. 1996. Morfología de = ac D en Verbenaceae-Verbenoideae I: Tribu arwiniana 31: 1-17. aa x F. R. Barrrie, H. M. Burdet, V. M E. Hawksworth, K. Marhold, D. H. Nicusus. P: Ded o, P. Silva, J. E. Skog, J. H. Wiersema & N. J. Turland letini. SRS Nomenclature n. Hanove 009, Verbenaceae alas. Fl. Rep. rA P. e 73): & s Cafferty. 2001. E of Linnaean names of taxa of Verbenaceae s.s. described from the Greater Antilles. Taxon 50: 1137-1141 Michael, P. W.1 1997. Notes on Verbena officinalis s.s. and V. closely related taxa. Tasa 7: 293—297. Verbena. P. 14 en Flora bars afner Press, me needful nomenclature dE. Revista Sudamer. m 5: 1 VT Novelties among dci American Verbenaceae. Phytologia 1(14): 453-480. 1940b. Verbenaceous novelties. Naturalist 24: rh — ——. 1941a. Novelties in the Moe and the Verbenaceae. e 2(1): 6-3 lb. Plant novelties. a ogia 2(2): 50-57. —— 1946. Nomenclatural notes II. Phytologia 2(4): na Amer. Midl. on new and noteworthy plants I. Prog 2 Ts 42. nre otes on new and noteworthy plants IV. dat 2(10): 408—428. 55. Notes on new and noteworthy plants XX. na EE 225-230. Dd in Verbenaceace. Amer. Midl. E 59: 3 e kwani a monograph of the genus élue IV. Phytologia 8(5): 230-272. — ——-. 1963a. Materials toward a Verbena VIII, Phytologia 8(9): 460-496 l Materials toward a mnogreph of the genus Verbena IX. Phytologia 9(1 ): 8-54. oe Materials toward a monograph of the genus _ Verbena XL Phytologia 9(3): 113-181. of the genus toward a monograph of the genus 1963d. Materials E XIII. aos 9(5): 267—336. 1964a. Materials is a mo: kes XV. Phytologia 9(7): nuo otes on new = noteworthy plants XLI. > Patel 10(3): 170-172. — ——. 1964c. Materials toward a monograph of the genus nograph of the genus E XX. Phytologia 10(4): 27 964e. Notes on new and noteworthy plants XLII. Pila 10(6): — a monograph of the genus um XXII. Po n hay 1-68. . 1964g. Materials toward a ihe quum Verbena XXIV. Phytologia 11(2): 80-143. —— i Materials toward a the genus Las za. dla e 155-217. genus MONTE XXVI. gia 1 na; 219-287. 965b. M. genus Varina XXVII. naa 116) 290—357. 1965c. Materials toward a monograph of the genus Verbena XXVIII. Phytologia 11(6): 400—422. 1I rials toward a monograph of the genus itional T on the genus Verbena III. Pila d 275-30 1972. Materials el a monograph of the genus Verbena X E Phytologia 24: 216-256. noteworthy plants LXXIV. 5. Notes on IVVVIV Pi 29: m. Yasal qa 1 34(1): 18— . 1977. Notes on new and noteworthy plants XCIX. E en 49-53 Notes new and noteworthy plants ewm. Pl AG): a noteworthy plants CLV. otes on new and Pla 5 506): gts new and noteworthy plants CLVII. Posada ting 162-163. Montgomery, L., M. Khalaf, J. P. Bailey & K. J. Goural. 1 Contributions to a cytological catalogue of British te Irish flora, 5. Watsonia 21: Mueller, F. 1858. Verbena macrostachya. P.60 en Fragmenta Phytographiae Australiae, Vol. 1. Melbourne. Muhlenberg, G. H. E. 1818. cae Plantarum Americae t 2nd ed. William > Hello, Lancaster, Pennsy P iege A "2002. A taxonomic revision of the genus Verbena L. (Verbenaceae) in Australia. J. Adelaide Bot. 21-103. ] L 1 4 ies of Mexican taxonómica de los ceae): Serie Pachystachyae. Ann. Missouri Bot. Gard. 94 1-62 Je z I. Fernández & M. J. Díez. 1988. Números cromosómicos para la flora española. Número Lagascalia 15: 124-129. Perkins, W. ri R. Estes & R. W. Thorp. 1975. Pollination ecology of interspecific hybridization in Verbena. Bull. Torrey Bot. Club 102: 194-198. Perry, L. M. 1933. A revision of the North American species of Verbena. Ann. Missouri Bot. 20: 239-363. — —— & M. L. Fernald. 1936. Plants bon the Coastal Plain irginia. Rhodora 38: 441, pl. 450, figs Post, G. E. 1933. Flora of Syria, Palestine, ud Sinai, 2nd ed., Vol. 2. American Press, Beirut. Annals of the Missouri Botanical Garden Rafinesque, C. S. 1825. Neogenyton, or lidicuien of Sixty- six New Genera of Plants in North America. Lexington, Twenty new genera of plants from the Oregon Mountains. Alani J. 1(4): 144-154. — Flora Telluriana, Vol. 2: 104. em — S. 1966. Drawings of British Plants. P. — N W. 1806. Catalecta Botanica. Fasc 3: 3. Leipzig. Rzedowski, J. & G. C. Rzedowski. 2002. Verbena. Pp. 118- 199 en Flora del Bajío y de regiones adyacentes. Fase es Instituto de Ecología, Centro Regional del Bajío, genera of Verbenaceae in the Sn. enel io. Bot. 5: 303-358. United — R. 1919. Las Verbenáceas. Contribución a la Flora de M : Anales Soe CL - Argent. 87-88: 95-134. Savi, G. 1802. Memoi Mem. Mat. Fis. Soc. Ital. Sci. IX, 349-35 Schauer, J. C. 1847. Verbenaceae. Prodr. e 11: 522- 700. Treuttel et Würtz, Paris. Schnack, B. 1942. ego preliminar sobre una modificación as. 1944. Nota sobre la validez del género Clandalaria (Vereen, Darwiniana 6; 469-471 s Semerenko, L. V. 1985. numbers in some species of flowering ioa of Byelorussian flora. Bot Zhurn. S.S.S.R. 707): 992-994. Silvestre, = 1986. Números cromosómicos flora ümeros 435—455. alia 14: pet E Skalinska, M. 1976. Further M icd sam, of Polish angiosperms XI. Acta Biol. Cracov. Ser Bot. 19: 107-148. Small, J. K. 1933. Verbenaceae. Pp. 1135-1139 en Manual of the Southeasthern Flora. Published by the author, New AA 1892. Flora of W. Carolina and contiguous MC — 3(1): 1-36. Sprengel, C. 1825. Didynamia A (16): em ern Set. Veg, art, J. ` 1911. Expedition of the California Acade my of Galapagos Islands 1905-1 I M RE. ser 4, 1: T-288. oe Strobl, G. 1883 - Oesterr. Bot. Z. 406: ` : 33-34. Svenson, H. K. er Plants of the Astor Expedition 1930 ( and Cocos Islands). Amer. J. Bot. 22 T, Troncoso, = S. 1962. Notas taxonómicas sobre Verbenácca, 2: 527-531. North tiguous territory. Mem. Torrey Bot. Club de sudamérica erbenaceae, V. 231-244 — (edito, Flora e Rios. o Ci. EA Ps E e Symbolae Antillanae, Vol. 5(3): 353-555. Vachova, M. 1976. Index of chromosome bar ur flora, Part = Acta Fac. Rerum Nat. Univ. 1-18. > Bot. 25 vn der Wei, It 197 Vascular plants from the Gal and taxonomic notes. Bot. Not. Vasudevan, K. N. 975. me to the Haase r. Schweiz. Bot. Ges. 85: 210-252. e de J. 1891. Flora Bulgarica. Prague. Verdcourt, B. 1993. Verbena. P. 98 en C. E. Jarvis, F. R. I & D. M. ipm (editors), A qe si tacha Papa Names and Their Types. Regnum V 21: Wadmond, S. 1932. Notes i. rom ciis Wisconsin. Rhodora 34: 18-19. Walter, T. 1788. Phryma. P. 166 en Flora Caroliniana. J. Fraser, DN Ward, D. E. 1984. Chromosome counts from New Mexico and Mexico. ten 56: 5 — —— & R. Spellenberg. 1 osome counts of angiosperms from New Messen and adjacent areas. Phytologia 64: 390—398. Wiggins, I. L. & D. M. Porter. 1971. Verbenaceae. 509 en E : the Galapagos Islands. Stanford University Wilken, en 4 dn Verbena. Pp. 1088-1089, 1093 en D. H. Hickman (editor), The Jepson Manual, Higher Plants of California. University of California Press, Berkeley. APÉNDICE l. Lista de especies y taxones infraespecíficos aceptados de Verbena ser. Verbena, tratados en el presente trabaj 0. te numeración de los taxones en] los Apendi ces sl y? 2 el resto del texto. Verbena bracteata Rodr. Verbena californica Molden Verbena ca anescens Kun Verbena ca. Verbena caroliniana Michx. erbena clouerae Moldenke Verbena px Moldenke Verbena ehrenbergiana Schaue erbena gracilescens var. dicen (Moldenke) N. CRNA PWN P= = = O'Leary . Verbena gracilescens (Cham.) Herter var. gracilescens Desf. Verbena menthifolia Be neomexicana var. kesal L. M. Perry ^ neomexicana P Gray) Small var. neomexicana Verbena natalensis — ex C. Krauss Verbena officinalis E var. officina Verbena perennis var. johnstonii Mio Verbena perennis Wooton var. perennis Verbena plicata Greene Verbena recta Kunth Verbena scabra V. i erbena simplex var. orcuttiana (L. M. Perry) N- O'Leary simplex med jui fed pod und ud jmd Ps jmd jn ET -— N _ PF SSBSRRSSK: e Verbena urticifolia L. Verbena xutha Lehm APÉNDICE 2. Índice de colecciones. Cada espécimen es e por el nombre del primer colector en el caso en dos colectores hayan participado de la colección; si Me Volume 97, Number 3 2010 O'Leary et Revisión Taxonómica de Verbena dos Mito se citan sebes. En el bu de no poseer se encuentra depositado o en su m sólo el herbario. V indica entre paréntesis el námero de orden del taxón al que se and (ver Apéndice 1). Abbiatti & Claps 86 (10); Acevedo-Rodriguez 10747 (25); Acosta 119 (16), Adam 12959 (29), 13072 (29); Adams C. 10967 (25); Aguirre E. 558 (10); Ahles 47840 (25); Ahumada et al. 1232 (10); Allard 14838 (16), 1682 (27); Alvarado s.n. US 1490133 (4); Anderson 10404 (5), 3977 (19); Andreasen et ; À 9; (20); A 2265 (10); Argañarás 86 (10); Arséne 4 à. 17 (16), p (16), 48 (3), 672 Moi 8829 (16), 10242 (16), 10626 (3), 12069 (30), s.n. US (4), s.n. US 464302 (16), s.n. US 464303 (16); Pire s.n. 57 (13); Ashe s.n. (5); Asplund 17801 (T); 20); Atwood 21186 is 28998 (15). Ball 605 (31), 1171 (18), s.n. MO 11723 (20); Balls 4667 de 5266 (3); a 93 (10); : M ADT 1178 (19); Bebb s.n. di Becerra 18141 (15); Bennett et al. 719 (16 Bernet s.n. (20 10); Blakeley 616 (15); Blanchard 1 i (11), 1783 e. 104 08); e nn dd 1349 (10). a (10); m rman s.n. (19); í «He oe 10775. (15); Bourdo e py Be) 119 (4), bis seb Brager 7 (30); Brass 15556 (25); Braun s.n. e 271 ple j n. US 2712379 (27); Braun & Cincinnati « "s 2712374 (30); Breedlove 27018 (16); Brenckle 47533 (28), mn (13), 48067 (12); Brett 308 (4) n. (13); Brooks 1834. ape get pea 3 (20 3200 (30); Buell chem (30); Burk 542 (13); Burkart pene x 5807 (10), 8069 (10), 9083 (10), TS (10), 13192 (10), 13841 (10), et (10), 14028 (9), 14483 (9), 17678 m E 19567 (10), 20272 (10), 22702 (10), 26605 (10), 29656 (1); Burkart & Troncoso 11025 (10), 11365 (10), 26352 (10), 358 (10); et al. 28824 (10), 31067 (10); Bush 28 (12), aoe sth a n Byars s.n. US 330912 (30); Bye 87: lero Marmori G. 1515 (10); Cabrera 7223 (10), o ane Cabrera & Cabrera 2837 (4); pe & Fabris 16032 Qo. 17417 (10); Cabrera & (10); Cabrera 7 082 (12), s.n. MO 1233343 (12); Chandonnet . &n. MO 703969 (13), s.n. MO 859901 (13); Chase 34 (5). 3228 (30), yee oa Chevallier 81bis (29); Chickering s.n. S 30); Ching 8514 (19); Churchill s.n. (27); Clark 7059 (11); Clasen 5371 (31); Clemens s.n. (3), 11 1749 9: .. Clinebell 1141 (5); E Ë Clim ee geras (28), 5053 (12); .. 80); Combs 389 (25 Come 36 13), 4057 ; M en. : : Ste Cams tae 7 4), Es Conzatti 4194 cds pond (16), 4288 ton 4992 (3); 40 (14); Cordini 83 (10); Cornejo Tenorio 73 (24); i 5); iaia ag e Coral Díaz 478 £206. 712 (11); Correll 15205 (6), 21530 (11), 5266 (31), 36820 (18), 40085 (25), 51393 2» se 51469 (25), sme (12), 9239 (25), 9447 (31); Correll & Correll 30882 (22), 38275 (18), — Correll & Thomas 100220 (31); (28), 50298 (13), 50968 (31), 51970 as 53037 Qs Ce Cox et al. 391 Brie. Clark 4250 et al. 1621 (10); an dd 44220 (3); Cronquist ye 17795 LT Crutchfield 2089 (20), s.n. SI 3344 (5), s.n. US qubd 1959 (5), 4386 (5), 4765 s a ge 6159 (5); Cusick on (28), 34007 (28); Cutler 901 (3). Dale Thomas 84970 (30); D'Arcy 1112 (13), 4644 (28); Davidson 858 (28); Davis = vig = (16), 4488 (28), 8493 skp De Wilde 4845 (19); Deam 58210 (30), 61340 (27), 65942 (25); Degener 5038 (22), 2618 (4); Degener & Peiler 16061 hi Dehesa 1551 (4); Del Río 18023 (18); , 8193 (30), 11704 (30), 12996 (28), 16520 (30), ge 17808 (27), 26826 (30), m (27), 29588 (25), 30772 (28); Denton (20); 78 (25); Detling 8411 x Diaél 3419 (4); Diaz Saree p (24), 3962 a Dick & Verda Walter 8111 d ae 91 (16); Domes Mm n Donnell s. rd Dorsett & Morse es e C end 53 (5); Duncan 20214 (12); Duncan 2600 ( Dunn et al. "Rede prod: Inn E (20); sedg Lo (15). Earle 387 (22 s.n. (22); Earle & ace ESOS n io (28); Eggert s.n. MO 117586 (23), s.n. MO 117588 (23); Eggleston € drag 18910 E 15); ved i (13); Ekman 13985 (25), 2019 (9), 2020 (9); Elias 10254 ey li s.n. (5); Ellis 258 (15), m et al. 964 (11; 010 (12); ne a 71934 (28), s.n. US 79348 ; Ertter 4783 (3), 5582 vermam 970 (28); E 197 (28); Ewan ds (1), 17704 (31); Eyerdam . Fabius 409 (13), 5270 (10); Fabris H. 5270 (10), das x al. 3283 (10), 3831 (10), 5436 = ; Faircloth 5204 (5), 72 Fahrenholly s.n. Fawcett 39 et al. 851 E pe he e es Fendler Ce 117577 (23); Ferguson Shc 6863 ae 2453 (25); Fernald & Long 10799 Q5) Ferris 2607 (18); Field & Lazar 530 (29); Fink 251 (28), 264 (30); ea Fisher 82 (31), 189 (12), 3762 (8), 35208 36122 (15), 46169 (8), woh (16; Flores 70 W, 133 x 154 (16); Ford s.n. US 45623 A ge 13 a». Foar DA, 12002 37559 (20), 38374 (20), 386 o ae 18613 — et al. 1 e 0o. aris (10); € 3132 LE 29), s.n. MO s.n. 6766 M0 116767 (29), s.n. o 117460 (29), s.n. ; ow rie s.n. MO sien (29), s.n. MO 764854 (29); García Gastony et al. 363 (16); Gentry 1341 Ea 6727 e € (16), d oe (18); Gentry & Barclay 1 A oa Gil _ pe Giler 31 (7); — 180 e 277 (25), € A pes 4 up 4), 317 (8; Gime 816432 (22); Gómez-Santiz 217 (4), i). zr 13); Frye 2474 gan Fryxell 1377 79 9702881 (13); ne 5): Greene 12505 (18); Greenman , (20); Graves 621 Sona E (6k Gino 3218 1953 (13); Greenway ; ee Annals of the Missouri Botanical Garden h 639 (25); Groth 187 (31); Guizar Nolazco 5082 (24). Haas 1673 (28); Halse 4422 (12); MN 200 (20); Hanson 148 (15), 1130 (18); Hardin 53 ; Harringto 9667 (15); Harrison 4778 (17), 5796 (18); a 1962 (30); Harvey 539 (18); Hassler 1668 (10); 10977 (27); user 3058 (28); H. — s.n. CS 2211 ora sn: US 221212 (3); Hazslinsky s.n. US 71958 (29); H et al. 4509 (3); Heiser 866 = "Heller 1 = (3), 5785 (14), 5919 an s.n. US 407055 (28); Henderson 9481 (12), 9518 (12), pes f 12), 95224 (27), 95225 (27), 95438 (13), fen ta ° 75 (27); spend 9159 (28); Hernández C. 154 (8), 209 an 11), 4890 a 5976 - 6158 p.p. (3), 6158 p.p. (16), 6591 (16); Hernandez R. 9287 (8); Hernandez Xolocotzi 3 4; Hicken 2 (20), 3 age 3411 (20); 4537 e 5764 c 7023 (23), 7065 (23), 7188 (23), 7317 (22), 7691 (28), 7803 (15), 8881 m 8996 (22), 10269 (22), 17176 (22), 23389 (15); Hi q 9964 (23); Hill 4619 (3), 12093 (15), 151 - i 23269 (5), 33066 peti 33107 (30); Hi 70 (3); Hill & Taller 3993 (3); Hinckley 170 (18), 1971 y 2134 (25), a (25). 4614 (3); Hind 727737 (20); Hinterthuer 497 (28); ), 16636 (3), 18487 (18); Hinton et al. 18244 (2 4); T s.n. (5), 269 (25); 916 (20); Hollister 110 (30); Holmes 76 dm iiim 4691 (15), 10022 (30); Holzinger s.n. US 245962 (20), s.n. US 660559 (18), s.n. US 660558 (18); Hood s.n. d Hoover 3613 (2), 9885 (2); Horr E76 (21), 3450 (28); Horr n spa E masa wes ‘cha nein a CD n. MO 10 n. MO 107: ii an P. Ra 1317 00, es (10), 9360 (10); Hyypio 2475 (13). Toara. Manriquez nton 5847 (11 Qu. 26191 1 (29, 20053 Holdridge 834 (10); Iuatsuki et al. 102 (19). Jackson 2106 ° Jacobs 50 (30); e: et al. 43 (12); Játiva & Epling 260 (7); Jerm 822 (20), 824 (20); Jessep — Jie 40 (1) 1 1067 (16), 2131 "e 4738 (25 n. (28), 1329 (30); Jones = = 5). 15926 (30), 1 e 03. n (13), qe (4), 44636 (13), s.n. MO 996338 (1 S 856990 et al. 10421 (10); Jonker ru s.n. pa 49726 (20); Joor sn. MO 1 waqa (25); Jergensen 2467 (10): Joseph 5408 (20). 2 (20); Kearney 1739 (30): & P. a 10506 o es 6540 (4); Kempton s.n. US 1081713 (4); Kensy 552 (30); Kiesling 3071 (10); Kiesling et al. 1613 En 9770 (10); Koelz 4769 (20), 1 EE E 44 (20); Koeppe 6961 (10); Krapovickas et al. 16634 (10), 23678 (10), E Krauss 151 (19); Krug & Urban 767 (25); Kuntz s.n. US 1994907 (20). Ladislaus C. Cutak 67 ns Lamson-Seribuer s.n. US 264002 (27); Lanfra 460 (10); Langlois 123 Gb, s.n. MO 996229 (31); Lansing 2806 (30), 2810 (28); Larson 3441 (13); Lassimonne 529 (20); 2 Laude s.n. MO 1071955 (30); Leadlay & Petty 108 (20), 274 (20); Lebgue et al. 3202 (18); Lee s.n. (13); Lehto et al. 11506 (15); (15); Lemaire 866 25); Lemam s.n. NY 150043 (20); Lemos 157 (20); León 769 X Leroy Abrams 3406 (16); Lesues Mex 53 (17); Lesueur s.n. US 71977 (31), s.n. US 986684 31 lee 5385 (16), 5530 (15), 5533 (22); Lewis & Oliver 2 : Dni al. 5422 (12), 5423 ge 5431 (12), 5457 (17); Lichvar 2. EN Liebmann 11339 M E 11341 (4); tó ons = s.n. NOE 1303 (25); Liu 890121 (20): oa ios 2740 (10); Lundell 5047 (18), 9930 "4 a (23), 10774 (3), 10823 ~ e 27 enia (31), 12209 (4), 13618 (6), 14135 (31); . 9886 (6), 10038 (23), 10076 twm eem = a (3), 10197 (23), 10308 (12), 10398 (12), 10843 (6), 11381 (23), 12391 T 14340 (17); Lyle 253 (3); Lyonnet 334 iino 20. 1 (13); Maguire 10884 Ds Malby 7221 (6); Maldonado s. (10), 473 (10); Manni 13); Mansfield 01225 (13); aicha 11338 (10); Margwe 29 (19); Marsh 1 735 (28); Martin 220 (4); Martindale £ Camde n s.n. 21414 (4); Meise 3822 (12); Maxwell 317 (16); Maysilles 7497 (11); McAtee 1953 (12); McCoy 166 (13); McDaniel 3501 (12); McDougall 1059 (27); McFarlin n (25); McGregor os (30), ns ES Mun r e e im S 8); 65 (4); McKechnie 68 (22); M 2997 (16); M Mearns 82 D 525 D "us (18), n dn a (3). 1974 (19), 2915 (16), s.n. US 649506 (28), s.n. US 670318 (30), s.n. US 670319 (30); Medina 391 (16); Medina et al. 4025 in n (18); Metcalfe 1568 (22); Miller et al. 540 (29); Mi e 16007 pe -a (o. ee ces et al. 1 6); 771872 (29); abate 972 (25), 7091 a peus (30), Ls (13), 18898 (13), 19024 (13), 19038 (13), 19122 (30), 19225 (30, 19372 (13), 20434 (13), 25758 (2); Moldenke & Moldenke 11740 (30), 19827 (4), 19837 (4), 19850 (4), 19852 (16); Moore 393 (20), 2810 (16), 3611 (22), 10478 (28); Moore et al. 3277 (1 23); Morales 786 (4); Moran 5066 (19), 13604 (26); More Greenman et al. 28 (23); Morello 3060 (10); Morris s.n. MO 996331 (30); Morton 6640 (28); Moseley s.n. US 431257 (27); Muehlenbach et al. 4240 (30); Mueller 2305 (3), 2392 ay, 8138 (18), = (17); Mulford 508 (18); Miilgura 3787 unby s.n. US 147591 (29); Murata sigs (20); Miisch pes a Nabil " Hadidi s.n. MO 1908725 (29); Nash 601 (5), 1248 (25); Nease 515 (30), 517 oa Nee 15432 (28), 15762 (1), 22919 (4), 23467 (11), 26747 (12), 30066 (12), 43670 (28), 43765 (13); Nee et (30), 44021 (12); Nelson 505 (28), 4577 (16), 4593 (1), 8354 (15), 11406 (22); Nelson et al. 2018 (18); Nicora 1140 (10), 3278 (10), 4894 (10), 17781 (10); Nieuwland 685 (27); Norton 391 (28); Novara 3784 (10). Okuhara & Sunagawa 22 (19); Oliver et al. 517 (18); Orcutt 3488 (4), 5423 ° 5717 (23), s.n. US 56176 (26); Ordetx s.n. US 2281149 (4); Palmer 78 (12), 135 (11), 141 (16), 191 (16), 2 (16), 308 (16), 339 (4), 356 (18), 364 (4), 397 (25). q (25). 1156 (4), 4341 (28), 7556 (31), 7564 (5), 10692 (25), 11257 (23), 13282 (23), 13730 (23), 15262 (27), 27462 (25), 30523 (23), 30791 (17), 33605 (3), 34370 (31), 35235 (5), s.n. US 316318 (27); Pappi (29); Parish 5713 (25), 14826 (25) Parker 5934 (15), 8204 (12), 75150 (30); Patterson s.n. U 1323125 (28); P 18875 (30); Pease s.n. US 147571 (23); Pedelaborde 12149 (10); Pedersen 4072 (10), 9791 (20), 13415 (10); Peebles et al. 3790 (18); Pennel jus te SRE ` s bo an E * ° i p E Y $ 3 es 12352 (15); Piper 6160 (20); Pollard 563 (25), 1191 es — 3341 (1); Pri s.n. (25), 1948 (8), 4784 (3), 4829 (23), 6539 (11). 2590 1. 8534 (16), 9135 aD, 13159 (11), 13597 es. ES (23). s.n. MO s nx 6515 (16); 1 (8); 3833 (10 peser 2419 Q9) R Rambo 30975 o; 2209 (29); Reclaire s.n. US 17503 19.20% al 15759 (28), 26281 (27), 27849 (6), 37941 (27), 37952 (27), 38232 (20) 38823 (20), 40998 (30), 42487 (21). 77921 (13). 93572 (28), Volume 97, Number 3 2010 O'Leary et al. Revisión Taxonómica de Verbena 95712 (12), 104671 (31), 111641 (21), 117677 (21); Reitz 3287 (20); Renvoize 10); Revercheron 737 (23), 2118 (31), 3904 (23); Richardson 780 (28); Ricketson 618 (15), 4551 (15); Ricksecker s.n. US 217441 (30); Rios 577 (10); 6); Ripley & Barneby 11151 C erem Me 10); Rodriguez 69 (9), 1 ; Rogers et al. 8453 (31); Rojas 2526 uM penes 191 (5); Rose 7741 (3), 13130 (16); hoe et al. 8382 (16), 8495 2b A AS 8971 3» 22851 (0 Rosengiatt: 1010 (10); el uo Roy 2789 (27), 3681 (27); Rueda et al. 11550 a. 12931 (4); P ^ (4). 121 (16); sea 1103 (10); 59 (10), 3057 (10); Runyon 629 463 (23 2518 @), 2 2559 (3), d (23), 2611 (6); Ruth o (12), 740 (27), 1 or : Rydberg 118 (28), 433 (28); Rydberg & £5 . Salazar s.n. US 1013228 (16), s.n. US 1013229 m s.n. US 1169860 (8); Samaule 3787 (20); g 266 (28); Saravia Toledo 1705 Pp Sargent 695 (25); Saunders 1162 (30); Sayago 2369 (10 fer 35931 ; Schery 32 O, 116 116 (16), 143 (16) 9865 (10); Schinini Be & Palacios 25911 (10); Schinini et E 18290 (10), 33037 x Schnee s.n. Lm. s.n. (30), s.n. SI 48038 (8); Scholes s.n. US 2630558 (19); Schrenk s.n. (20); Schuhwerk 90/219 (29); Schulz 518 aa 526 (3); Schumann 1070 (11); Schwarz 4811 (9), 6207 (9); oe ix s.n. man s.n. US 787347 (12); Seaton o: gura Reyes 100 (16) E 2233 (13); Semple x (18), 600 (18); Sennen 3413 20); Sennen & Mauricio 7657 (29), 8500 (29); 601 (30), 17219 (30), 21569 (30); Sharp 253 23) 23 (12); Shetler 292 (13); Shimck s.n. (13); Shiu Ying E 5732 (20), 10350 (20); Sh ( 9 (17); Singer 6 (25); Skeiger 1066 (22 "numo (20); Small s.n. (20), 4337 (25), ve (20), s.n. Ai A 2304 (31); Small & Heller (20); Small & Small 4341 25); Small 11774 (12), 11801 (12), 11998 (12), s.n. U 1739114 (12); Smith 50 (20), 211 (20), 224 (4), 3701 n 8 (28), s.n. US 1323136 (30); Snow 6039 (30), 6067 (13); Solbrig 2907 (1), 3186 (22); Solomon 2291 (12); Somes 3301 4927 (15), 8239 (15), 8311 (27), 21331 (4), 24443 (4); Stearn 2 de Steele 106 (13); Steibel 772 (10); Steibel & Troiani € Stephens 49032 (28); nson 200 (12), s.n. MO 1 (18); Stevens 1051 (1), 2299 (2 7); et al. 14942 (4); Serena 38 28 (20), 373 (25), 492 (20); Steyer- (28), 51655 (16); — 6169 (28); 3180 (25); Stud. x Rheno-Trai 230 (20); Studhalter 1. Tanaka et al. 11032 (19); Taylor 49 (18), 238 (4). 5322 (13). P agi n E (11); Taylor et al. 10456 (25); Tejada 72 (4); Teodoro 6772 (20); Tharp 253 (23), (23), 667 (31), 668 (31) 1361 (3), 2818 a. 43801 (23), 43804 (18, < 12721 (25), s.n. NY 25 e 1); Tharp & Janszen 4 Anm et al. 4870 (23); Thomas 2825 (12), 8185 an 97761 (30), 123426 hw 124356 (31) 128399 (12), 129400 (12). 137759 (31), 138391 (2. 140861 (30). 155457 ans Thomas & Amason 14 141651 (30); &3 u pu. Thomas et al. MT 6D, 105919 (31), isi I x 154 (28); Thorne 17397 (27); Tidestrom 872 (18), 13037 (19), 13282 (20); Tiehm 11887 (1); Tolstead s.n. MO (10); Troncoso 143 (10), 316 (10), € o 27762 (10); 635 (20); Tsu 658 (19); Tucker 1307 (4); 101 : i. 913 (4), 11651 pa € u US 147571 (3); Tyacke (20); Tyler s.n. 2). Umbach MAN (27). van der ver tase ae » Sickle s.n. US sare ee, Vanni et 80 (10); Ve an, n, rs (24), 217: 00.22 5726 a, foe (10), 11440 (11); Viereck 229 (3); MO 2344220 (11); n 18; Wahl 1388 (13); Walker Waller 2645 (10); Vasey eene i et al. 3949 8101 09, E 8); Wallace et al. 197 (18); 31); 9098 (15); Ward 11 orl i 21090 ( 21827 eh 46244 (3); Waterfall 1442 (1), 3795 (22), 4510 (22), 5172 (23), 5209 (22), e ch Tau: (30), 12464 (15), 13443 (16); Waugh s.n. US 266934 Weber (15); Weberling s.n. ee Welsh 684 (13); Welsh et (12); Wheeler 11917 (13); w ie 1577 00, 3836 (18), 4104 16426 (30 i 7019 (22); o Tz al. 99 (12), 236 (18); Wiegand et al. 1350 sns d ide 65, ss (26). Pr. (26), 11783 23); Demaree 4 ‘oan s.n. n. 21081 (11); a 7); Willya et al. 14230 (6); 176 (22); Wolff 2948 (12); Wooton 208 inter 20 (28); Witte y Wap PT CHD. cs. US 45 ed al 5625 (4). Zanoni et e g 2832 (10); Zetterstedt 1050 (20); Ziegler 240 n de et al. 2691 (10). oae aa V. neomexicana var. hirtella L. M. P. ertena africana R. Fern. & Verde.) P. W. Michael [= v. n at hast = C C. Krauss] i n í albiflora Moldenke [= V. canescens Lr dr roemeriana (Scheele) L. M. Perry [7 canescens unth] ds co Verbena cloverae f. othe Landa E . Verbena comonduensi, Verbena domingensis V. carolina L.] clorerae Moldenke] [= Benth.] f. foliosa de [= V. menthifolia V. menthifolia Benth Moldenke [= V. ode n ehrenbergiana var. richardsonii Moldenke [= V. carolina L.] : Verbena gentryi Moldenke [= V. carolina L.] U x Verbena glabrata var. tenuispicata Moldenke [= V. carolina et ha f. parviflora Moldenke [= V. halei Small] 424 Annals of the Missouri Botanical Garden Verbena halei f. roseiflora (Benke) Moldenke [= V. halei Smal Verbena hastata f. albiflora Moldenke [= V. hastata L.] Moldenk - hastata L. rima lasiostachys f. albiflora Moldenke [= V. lasiostachys te Verbena lasiostachys f. scabrida (Moldenke) Moldenke [= V. lunas Link] Verbena lasiostachys £ septentrionalis (Moldenke) Moldenke [= V. Vrime lasiostachys var. scabrida Moldenke [= V. lasio- stachys Link] Verbena lasiostachys var. septentrionalis Moldenke [= V. lasiostachys Link ] Verbena litoralis f. magnifolia Mol r Verbena longifolia f. albiflora Moldenke Ln carolina L.] — longifolia M. Martens & Cena! [= Y. carolina L.] erbena longifolia var. pubescens Moldenke [= V. carolina Verbena macdougalii f. albiflora Moldenke [= V. macdou- ¡e A. Heller] erbena macrodonta L. M. Perry [= V. macdougalii A. ] "M Ik [» V. meth Benth Verbena neomexic So SIM ES F iul ^3 1 v ML M Fay i- Y neomexicana (A-G Gray) Small var. neomexicana] — f. anomala Moldenke [= V. officinalis L. is] ad ne Doi V. halei Small Small] Verbena officinalis subsp. africana R. Fem. & Verdc. [= V. officinalis var. natalensis Hochst. ex C. Krauss] Verbena p var. africana (R. Fern. & re Munir [= V. officinalis var. natalensis Hochst. ex C. Krauss] Verbena officinalis var. eremicola Munir [= V. officinalis L. var. is] Verbena officinalis var. gaudichaudii Briq. [= V. halei Small] Verbena officinalis var. grandiflora Hausskn. [= V. officinalis L. var. officinalis] Verbena officinalis var. crga € [^ V. officinalis var. natalensis Hochst. e Verbena — f. oes (Moldenke) Moldenke [= V. plicata Greene] Verbena Le var. degeneri Moldenke [= V. plicata Greene] Verbena riparia Raf. ex Small & A. Heller [= V. officinalis L. var. inalis] Verbena robusta Greene [= V. lasiostachys mes Verbena roemeriana Scheele [— V. canescens Kunth] Verbena runyonii Moldenke [= V. neomexicana (A. Gray) Small var. neomexicana] Verbena russellii d [= V. neomexicana (A. Gray) Small var. neomexic Verbena scabra f. s Moldenke [= V. scabra Vahl] Verbena scabra f. ternifolia Moldenke [= V. scabra Vahl] Verbena sedula Moldenke [= V. carolina L Verbena sedula var. darwinii Moldenke [= V. carolina L.] Verbena sedula var. fournieri Moldenke [= V. carolina dr Verbena subuligera Greene [= V. bracteata Lag. & R Pru supina f. erecta Moldenke [= V. supina L.] supina var. erecta Vena Manis [ V. supina L.] rpa . Perry & Fernald ia var. ria (Raf. ex a & A. Heller) BT L. var. officina. e {= ¥. ENDEMISM IN NEOTROPICAL C. Thomas Philbrick,* Claudia P. Bove,* and PODOSTEMACEAE! Hannah 1. Stevens* ABSTRACT Podostemaceae. f pl d waterfalls, bes ocior docile dr m species endemism. We te sted this idea for oo members of the fundis using historical um holdings, personal field collections, and geographic information systems analyses. In contrast to estimates D based on the stu dies of P. van Hoyen (66%), we report 1 5%-37 7% based on y based 1 Xf regions (Amazon M o Paraná River ! System) and major a areas (eastem Brazil) are e to possess home unique mad ropose rivers and rive! floras. and consider one-river agi pá o-river endemics as narrowly distributed. Limitations in the current current taxonomy are discussed relative to lisboa of meaningful pares of local species endemism. We provisionally apply IUCN assessment categories to Neotropical Podceteuaciné and report that approximately one third of the species fall into one of three puppe -Data Deficient (DD), Least Concern (LO, and Vulnerable (VU). Ten species are Critically Fa Fadesgseed nna rge dams make long reaches of rivers inhospitable. Expanded use of hydropower i in Latin America will exacerbate Resumo x s z 1 , stal. emaceae, uma família botánica restrita a ambientes de corredeiras e cachoeiras, Tris x L e utilizando espécies com alto grau de endemismo local. Teenei esta hipó i I s 1 7 AN 9$ dados históricos da literatura, material deposit m herbário, col oletas P S sebo de P wa A. do sistema de info ormacáo geográfica ntrast d endemismo (66%), reportamos 15%-37% de espécies endêmicas, baseadas na taxonomia sd. Pa s d es. Grandes ados pela amplitude de ocorré cia e de maior eixo geogr euge nol: inm à AS d P: 4) idad mais apropriada acessar 0 i . distinta flora de Podostemaceae. Propomos rios e bacias — distribuição eo: no Bue. Podoste emaceaé, considerando endêmicas de um-rio e e de dois rios como E ç ie Pod ord de espécies. Aplic isori t tado d a encaixa com as categorias da IUCN, reportando que aproximadamente um terço das > espécies se e ae Dez estao Criticamente ados Insuficientes (DD), Náo Ameagada (LC) e Vulneraveis (VU). Dez especies es : ca. i š : ier tém sofrido os maiores impactos antrópicos—os di des dos rios inabitáveis. A expansão do uso de energia proveniente hidrelétricas na América Latina irão exacerbar este problema. odostemaceae. Key words: Aquatic plant, endemism, ydo IUCN Red List, large dam, P a ENS O UU U see z EB-0444589) and Connecticut State ¿This work was supported b iorum from the Nena! Se ae al Comas Nacional de Desenvolvimento University-American Association of University Professors (AAUP) to " e h Produtividade em Pesquisa Grant (2009- Científico e Tecnológico-Ministério de Ciência e Tecnologia (CNPq T MCT) ony ae 282/2005-52, 091/ u A mm 7073/20084) t C.P.B. Material were collected ir hui win prs ppp E 2006, ema d `. ¿k dos Recursos Renováveis t Recursos Hídricos e da Amazônia Legal, Instituto Br ees do "> Aspa iud ature Conservation Meter pcs collected in Soriname with a pesmit Even e SM Que (Cg ga CH, GUA, ICN, wx MG, € thank sh. cn c + ly their specim _ Dali. a. Pau K. B. : ilbrick, Garret E. Crow, and N hu M Y — NBA, NY, boi M help i earl desse RM R RB, U, VEN. WCSU. W E e aa ein i e ER re m Lt lo R. (1951- N 2 t ersity, Danbury, Connecticut mental Sciences, Western ( e - Department Biological and Environ - 06810, U.S.A. s Le e 3. 11 Ria de laneiro. Quinta da Boa Vista, 20940-040 Rio Musen N * al, Trt: E de Janeiro, d a en Boulevard, Bronx, New York 10458, a om Se — : doi: i: 10.3417/2008087 oo _ ANN. Missoum Bor. Gano. 97: 425-456. eee Annals of the Missouri Botanical Garden Podostemaceae are the largest family of strictly aquatic flowering plants. Approximately 20 genera and more than 150 species in this pantropical family are from the Neotropics (Royen, 1951, 1953, 1954; Cook, 1996a). Plants occur attached to solid substrata in swift currents of river rapids and waterfalls. There has been a resurgence of interest in the family over the past two decades. Considerable work has focused on interpreting the unusual morphology and development of vegetative structures (e.g., Rutishauser, 1997; Ameka et al., 2003; Jager- Ziirn, 2005), De placement of the family (e.g. Gustafsson et al, 2002; Wurdack & Davis, 2009), and infamis] phylogenetic patterns (e.g., Kita & Kato, 2001, 2004; Moline et al., 2007; Tippery et al., in press). T De sid addresses another aspect of the fami ` Weddell n "ha Will (1902, 1914) were among the earliest to discuss the prevalence of narrow species distributions in the family. For example, Willis (1914: 545) stated that species “... are usu y very local in distribution.” He noted that species of Castelnavia Tul. & Wedd. (Brazil) are endemic to few waterfalls: “...some ies differ at every caras. Rives (1951: 13) reflected the same idea: ing to descriptions given by botanists each cataract and each set of rapids would have its own species.” It is commonly stated in the literature that Podostemaceae have a high proportion of species with narrow distributions (e.g., Royen, 1951; Taylor, 1953; Sculthorpe, 1967; Graham & Wood, 1975; Philbrick & Novelo, 1995, 2004; Cook, 1996a, b; Ameka, 2000; Rutishauser & Pfeifer, 2002; León . 2006; Cook & Rutishauser, 2007). The present ins. however, are not aware of any detailed analysis of the taxonomic or geographic extent of endemism in Podostemac. Analyses of distribution patterns, and dp initial assessments of species endemism, are based on taxonomic studies most comprehensive taxonomic studies of Neotropical Podostemaceae were by Royen (1951, 1953, 1954). His works indicate that many species were known from few collections; a remarkable number were “once collected" (Royen, 1951, 1953, 1954). Possible relationships between n coll pecies ected once and those that are > actually caine to narrow regions : more than 50 years of systematic species m remains large Herein we consider this issue and provide the first detailed assessment of narrow species distributions (i.e., endemism) i in Neotropical a rivers are under intense threat k oe a Ç T oh study have occurred since Royen’s works, the topic of endemis: unaddressed. ing in Latin America has had dramatic negative impacts on river biota (e.g., Pringle et al., ; Pol & Hart, 2002). With few exceptions, Podostemaceae are restricted to tropical rivers. Consequently, it is important to assess the degree of narrow species endemism such that possible conservation concerns can be identified and addressed. The current study has several objectives. First, provide an updated list of Neotropical species and an overview of their geographic distributions. Second, establish the scale and incidence of species ende- ism. In doing so, the landmark papers of Royen (1951, 1953, 1954) will be used to develop a standard against which to compare insights gained over the past five decades. Geographic information systems (GIS) will be used to assess the distributions of a subset of Neotropical species based on the number of river systems and rivers they occupy. Three general issues relating to conservation will also be considered: (1) the importance of river systems and rivers, as opposed to specific sites, for assessing the distribution of these riverine species; (2) application of IUCN Red List categories for estimating the degree of extinction threat faced by species; and (3) the significance of arg asa pervasive threat to Podostemaceae in the Neotropics. METHODS Two estimates of endemism were produced. The first was derived from information provided exclu- sively in Royen’s (1951, 1953, 1954) treatment of Podostemaceae in the New World. Although Royen (1951, 1953, 1954) recognized forms and varieties for some species, only species-level taxonomy is dis- c here as subspecific taxa are difficult to identify. Geographic distributions of species recog- nized by Royen (1951, 1953, 1954) were based exclusively on voucher specimens he liste stimates were then calculated — on the current taxonomy, i.e, Royen (1951, 1953, taxonomic studies subsequently on. 1969; Royen & Reitz, 1971; Tur, 1975, 997, 2003; Burger, 1983; Hollander & Berg, sext Novelo & Philbrick, 1993a, b, 1995, 199%; Werkhoven & Peeters, 1993; Velásquez, 1994; Philbrick & Novelo, 2001, 2004; Philbrick, 2002; Berry, 2004; Philbrick et al., 2004a, b, 2009; Bove et al., 2006, in press; Rial & Bove, 2007; Philbrick & Bore, 2008). We also used information derived from holdings in the following herbaria: BBS, C, CAR, EAP, GH, GUA, ICN, L, MEXU, MG, NHA, NY, R, RB, U, VEN, WCSU. emaceae are restricted to rivers. We propose that the number of rivers in which a species occurs Is Volume 97, Number 3 2010 Philbrick et al. Endemism in Neotropical Podostemaceae Table 1. Number of river systems (number of rivers in parentheses) from which 22 representative species and two taxonomic forms were documented from each of five hydrogeographic regions. These data are a summary of Appendix 3. Amazon Fastern Guiana Orinoco Paraná River System River System — EOO (km?) River System Brazil Area Area Castelnavia fluitans 3 (7) 0 0 0 0 321,772 : 1 (1) 0 0 0 0 41 C. multipartita f. multipartita 3 (6) 0 0 0 0 162,683 C. multipartita f. 2 (3) 0 0 0 0 29,019 E noveloi 1 (1) 0 0 0 0 10 princeps 3 (6) 1 (2) 0 0 1 (3) 1,566,044 Ceratolacis scan 0 1 (4) 0 0 0 6010 Cipoia insert 1 (4) 3 (9) 0 0 0 118,706 C. ramosa 0 1(1) 0 0 0 10 Diamantina lombardii 0 3 (3) 0 0 0 3060 sp. A 0 7 (10) 0 0 0 74,671 Monostylis capillacea 3 (10) 0 0 0 880,715 temum comatum 0 0 0 0 6 (13) 535,545 P. distichum 0 0 0 0 12 (44) 1,164,242 P. flagelliforme 1) 0 0 0 0 10 P. irgangii 0 0 0 0 1 (2) 20,536 P. muelleri 0 0 0 0 8 (83) 461.353 P. ovatum 0 4 (7) 0 0 0 28,087 P. ruifolium subsp. rutifolium 0 0 0 8 (47) 781,899 P. nhanum 0 3 (4) 0 0 0 50 P. scaturiginum 1 (3) 4 (6) 0 0 1) 290,965 P. weddellianum 12 (34) 0 0 1 (6) 205454 Weddellina squamulosa 7 (19) 0 7 (8) 1 (5) 0 4,352,897 the most appropriate geographic context against which lo judge species distributions. Documenting a species at one location within a river is a reliable predictor that the species will occur elsewhere in that river. A Species documented only a single river, regardless of the number of collections from that river is scored as a "one-river endemic." Similar Procedures were followed to determine two-river endemics. on of species distributions within and between (1) main areas and hydrographic regions, (2) river systems, and (3) rivers were conducted for 22 representative species in eight genera (Castelnavia, Cipoia C. T. Philbrick, Novelo & Irgang, C Wedd., Diamantina Novelo, C. T. Philbrick & Irgang, ul., Monostylis Tul., Podostemum Michx., Weddellina Tul.) (Table 1). Species selected were clearly circumscribed taxonomically, with geographic distributions that were relatively well documented. species included occur primarily south of the Amazon River, ranging from central to southeastern Brazil, Argentina, Uruguay, and Paraguay. Only a single species (Weddellina squamulosa Tul.) was included that ranged into northern South America. nm Voucher specimens are cited in Appendix l or ` — PS atas E | brick & Novelo, 2004; Philbrick et al., 2004a, b, 2009; Bove et al., 2006, in press). The hydrographic regions and/or main areas demarcated by Ziesler and ed kiwan (1979) were assessed relative to the 22 representative species noted above. The majority of species occurred in one of three hydrographic regions or areas: Amazon Ri ver System, Eastern Brasil M and Paraná River stem. Two additi iana Area, Orinoco River System) were considered relative to one species ithin each of these regions, defined as “river systems.” The name used for each river system was that for the largest river. Two sources of information directly influence estime of endemism: » net on species distrib nge i of “ - * i l ] AAHUY TI 15 is also important, e.g., speci c endemic may be placed in synonomy under more species or new species being described. for the extinction threat of - Preliminary m t taxonomy only) are provided. It was Annals of the Missouri Botanical Garden at C) — "s CIAR > 10s aE y EO 4 y" E Q ^ E s 2d ° D 9 s O o A t 2 ` * < 2 c y D 5 5 e 3 = ea o o o e S F m 3 +. a SORA $ a a 9 déc 5 9 $ N P Š al 1 l L —. Á Figure 1 form of Podostemaceae in three hydrographic pe: or major e Amazon River System, Orinoco River System, Guiana Area. n. are included. Inset shows a region of t itans, C. T - Princeps occur. Open square, Castelnavia fluitans; asterisk, C. monandra; o C. multipartita á I dis: : É x > > e ; open riangle, p qe ERA as E RARE I. T. Philbrick & Bove; diamond, C. nde "filled circle, C. princeps quare, Woddellina aoe itele, Monostylis capillacea; star, Podostemum flagelliforme; filled triangle, P. scaturiginum: file wasis to — ig the degree and type of Twenty-two species were mapped and analyzed mao a species. Consequently, using GIS software (ArcMap 9.3). River systems were . poi w were based on numbers delineated following the hydrographic zones demar- List I pecies occurs. The IUCN Red cated by Ziesler and Ardizzone (1979) and using OROS UCN, 2009; ; 16 June 2008). While these estimates are rough, they provide a reliable approximation of minimum reservoir length and are sufficient for issues discussed herein. RESULTS ROYEN’S TAXONOMY AND ESTIMATES OF ENDEMISM Royen (1951, 1953, 1954) recognized 19 genera and 152 species (Table 2, Appendix 2). Genus size ranged from a single species (Ceratolacis, Devillea Tul. & Wedd., Lonchostephus Tul, Macarenia P. Royen, Monostylis, Tristicha Thouars, Tulasneantha P. Royen, Weddellina) to 48 species (Apinagia Tul.). Sixteen of the 19 genera recognized by Royen included at least a single one-river endemic species (Table 2). The percentage of coral endemism per genus ranged from zero in three genera (Lophogyne, Tristicha, Weddellina) to 100% in six (Ceratolacis, Devillea, Lonchostephus, Macarenia, Monostylis, Wett- steiniola Suess.). Five of the six genera with 100% one-river endemism were monotypic, while Wettstein- i had 56%, 21%, and respectively. It is notable that eight of the nine species (89%) of Castelnavia were also one-river endemics. Overall, 73 (48%) of the species recognized had three. Twenty-seven species were two-river endemics. In Royen’s treatments, 100 (66%) of the species ized were either one- or two-river endemics. CURRENT TAXONOMY AND T OF ENDEMISM Synopsis of current taxonomy. Twenty genera and 135 cae wie | recognized by us in the current prepa (Table 2 Appendix 2). Nine € were i. Midi Trisieba, Filesnantha, rn —G Novelo & C. T. Philbrick, Weddellina), and the largest number of species (51). We did not €: two genera recognized by Royen (1951, 1953, e n Mart., Devillea) and included Annals of the Missouri Botanical Garden Table 2. Comparison of taxonomy of beide (1951, 1953, 1954) with current taxonomy. For each genus, the number of species recognized is listed along with th and two-river endemic species. For current taxonomy, number of species scored as Data Deficient (DD) is dn listed. See text for discussion. n.a., Genus not recognized. Royen (1951, 1953, 1954) Current taxonomy No. of One-river — Two-river No. of One-river Data Two-river Data ndemi Genus species endemic endemic species endemic Deficient endemic Deficient Api. 48 27 (56%) 10 (21%) 51 22 (43%) | 19(8670) | 9 (419) 1(119) Castelnavia 9 8 (89%) 0 5 2 (40%) 0 0 0 Ceratolacis 1 1 (100%) 0 2 1 (50%) 0 0 0 Cipoia n.a. n.a. n.a. 2 1 (50%) 0 0 0 Devillea 1 1 (100%) 0 n.a. n.a. n.a n.a. n.a Diamantina n.a. n.a. n.a. 1 0 0 0 0 Jenmaniella T 3 (43%) 3 (43%) 7 3 (43%) 3(100%) 2(29%) 2 (100%) Lonchostephus 1 1 (100%) 0 1 0 0 0 0 Lophogyne 2 0 0 1 0 0 0 0 Macarenia 1 1 (100%) 0 1 1 (100%) 0 0 0 Marathrum 19 4 (21%) 3 (16%) 10 2 (20%) 0 2 (20%) 1 (50%) Mniopsis 5 2 (40%) n.a. n.a. n.a. n.a. n.a. Monost ylis 1 1 (100%) 0 1 0 0 0 0 Mourera 6 1 (17%) 3 (50%) 6 1 (17%) 1 (100%) 2(33%) 1 (50%) Oserya 6 4 (67%) ? 5 (71%) 4 (80%) 0 0 P. 17 5 (29%) 3 (18%) 11 1 (9%) 0 1 (9%) 1 (100%) Rhyncholacis 23 11 (48%) 5 (22%) 22 7 (32%) 7 (100%) 6(27%) 1 (17%) Tristicha 1 0 0 1 0 0 0 0 Tulasneantha 1 1 (100%) 0 1 1 (100%) 0 0 0 Vanroyenella n.a. n.a. n.a. 1 0 0 1 (100%) 0 Weddellina 1 0 0 1 0 0 0 0 Wettsteiniola 2 2 (100%): 0 3 3 (100%) 1 (33%) 0 0 Totals 152 73 (48%) 27 (18%) 135 50 (37%) 35 (70%) 22(16%) 7 (30%) three genera described since his monographs (Cipoia, Diamantina, Vanroyenella). Published literature: geographic pins of - cies. Schnell (1969, Guyana) re broade: geographic ranges than Royen (1951, 1953, 1954) for several species of Apinagia (A. divertens Went ex Pulle, A. guyanensis (Pulle) P. Royen, A. longifolia (Tul.) P. Royen, A. marowynensis (W ent) P. pea A. richardiana (Tul.) P. Royen, A. secu Oserya perpusilla (Went) P. — Berry (2004, Venezuela) documented the e of species in several genera that Royen (1951, 19 1954) did not report for the country: Apinagia (A. longifolia, A. guyanensis, edd.), Oserya Tul. & Wedd. (0. perpusilla), pper (R. hydrocichorium Tul., R. applanata K . KR. flagellifolia P. Roven Weddellina ( * — Berry (2004) tul distributional information for nine Species in four genera that indicated broader di stributions than reported ne Royen (1951, 1954): A. kochii (Engl.) P. a Royen, A. multibranchiata tata (Matthiesen) P. > A. ruppioides Tul., Jenmaniella pon dr Engl., M. capillaceum, O. perpusilla, R. coronata P. Royen, R. divaricata Matthiesen, R. ia Matthiesen. Lastly, Berry (2004) confirmed the narrow distribution of some species as reported by Royen (1951), e.g., A. brevicaulis Mildbr. and M. aeruginosum P. Royen. Werkhoven and Peeters (1993, Suriname) present- ed floristic data for 24 species in seven genera. Information provided for 15 species differs little from Royen (1951, 1953, 1954): Apinagia divertens, A. hulkiana (Went) P. Royen, A. longifolia, A. richardi- ana, A. secundiflora, A. staheliana, A. treslingiana (Went) P. Royen, + versteegiana (Went) P. Royen. Marathrum capillaceum, Oserya minima P. Royen, perpusilla, Rhyncholacis cristata P. Royen, R. dentata P. Royen, Tristicha trifaria (Bory ex Willd.) Spreng.» and Weddellina squamulosa. They also listed d secundiflora and R. cristata as restricted to the Suriname River, which corresponded to Royen (1951. Two species that Royen (1951) documented from a single collection each were listed as more widespread by Werkhoven and Peeters (1993): Apinagia imthurnii (K. I. Goebel) P. Royen and A. penicillata (P. Royen) P. Royen. Four species of Apinagia listed by Werkhoven and Peeters (1993) for Suriname had not Volume 97, Number 3 2010 Philbrick et al. Endemism in Neotropical Podostemaceae 431 previously been documented for the country by Royen (1951): A. digitata P. Royen, A. flexuosa (Tul) P. Royen, A. guyanensis, and A. marowynensis. A (1997, Argentina) repaid that. Podostemum ri Warm. . rutifolium Warm. occurred in E. while Royen (1954) did not. Although Tur (1997) reported other species of Podostemum (e.g., P. comatum Hicken) as restricted to small areas, the revised taxonomy of the genus provided by Philbrick and Novelo (2004; see below) presented a markedly different view of species distributions. Novelo and Philbrick (1997, Mexico) documented the following species to be more widespread in Mexico than reported by Royen (1951, 1954): Marathrum tenue Liebm., M. foeniculaceum (as M. schiedeanum Cham.), and Oserya coulteriana Tul. Moreover, O. longifolia Novelo & C. T. Philbrick was endemic to one river in Jalisco, while Vanroyenella plumosa Novelo & C. T. Philbrick occurred in two rivers, one each in the states of Jalisco and Oaxaca. Philbrick and Novelo (2004, Podostemum) reported that several species of Podostemum had wider geographic ranges than reported by Royen (1954), e.g., P. distichum (Cham.) Wedd. and P. rutifolium subsp. rutifolium. In their studies, both Royen and Philbrick and Novelo indicated that P. flagelliforme (Tul. & Wedd.) C. T. Philbrick & Novelo (previously treated by Royen as Devillea flagelliformis Tul. & Wedd.) occurred only in a single river. Podostemum flagelliforme was the only species in the genus that was documented from a single location. Several other species, however, had narrow geograph- ie ranges. For example, P. weddellianum (Tul) C T. Philbriek & Novelo oecured only within the Brazilian states of Minas Gerais, Rio de Janeiro, Espírito Santo, and Sao Paulo. Podostemum ovatum C. T. Philbrick & Novelo was only known from northeast Sáo Paulo, Rio de Janeiro, and central Espírito Santo, while RB irgangii C. T. Philbrick $ Novelo had been documented from a small region of Santa Catarina and adjacent Paraná. Podostemum saldanhanum (Warm.) C. T. Philbrick & Novelo, which occurred singly in the central part of the state of Rio de Janeiro, had the second narrowest distribution of species in the genus after P. flagelliforme. Philbrick et al. (2009) recognized five species of Castelnavia, two of which were one-river endemics. Castelnavia monandra Tul. & Wedd. occurred along an approximately 25-km region of the Araguaia River, While the present known distribution of C. nove spanned a 0.5—1 km length of the Taquarucu River in south-central Tocantins State. In contrast, two of the remaining species (C. fluitans Tul. & Wedd. and C. multipartita Tul. & Wedd.) were documented from TU Han six. rivers each end ranged enm T approximately 1400-km region in south-central Brazil. Castelnavia princeps Tul. & Wedd. was the most widespread species in the genus, occurring in more than 10 rivers in Goiás, Mato Grosso, Minas Gerais, Pará, and Tocantins. Velásquez (1994, Venezuela) listed 10 species for the country that were not reported by Royen (1951, 1954), T Apinagia longifolia, A. Marathrum ame, and Overye sii Two A swihilranchinin, An ) were iii š Velásquez (1994) to occur at e nae e is notable that A. and A. reported for Venezuela by Royen (1951) and Ne (2004), but not by Velásquez (1994). Published literature: neu taxa. Thirteen new species were published from the Americas since Royen (1951, 1953, 1954) (Appendix 2). Schnell (1969) and Hollander and Berg (1983) deseribed one inagia species each, the former from Guyana (A. itanensis Schnell) and the latter from Suriname (A. petiolata Hollander). Six new species were described from Brazil, d ien i Philbrick and Bove (2008) desc Castelnavia noveloi from Tocantins. Philbrick et al. (2004a) described the genus Cipoia (C. inserta C. T. Philbrick, Novelo & Irgang), while Bove et al. (2006) published a second species (C. ramosa) for the genus. Single species were ished for um C. T. Philbrick, Novelo & Irgang; Philbrick et al., 2004b) and and Diamantina (D. lombardii Novelo, C. T. Philbrick & Irgang; Philbrick et al., 2004a). Lastly, Podostemum irgangu (Philbrick & Novelo, 2001) was documented from Paraná and Santa Catarina. is iie new ies were desc ex Pu dem Novelo & C. T. Philbrick (Novelo i Philbrick, 1993a), Oserya longifolia (Novelo & Philbrick, 1995), and Vanroyenella plumosa (Novelo & Philbrick, 1993b). (Novelo et al. [2009] subse- quently placed M. M. rubrum in synonymy under M. foeniculaceum Humb. & Bonpl.). Lastly, two new period, but al represent a new Philbrick € Novelo, 2004, Mniopsis Warm.). Cook and Rutishauser (2001) species (see C: e species of Mniopsis Mart. to Crenias Published literature: names placed in synonymy. The —— o enr Annals of the Missouri Botanical Garden reduced relative to Royen (1951, 1953, 1954; Appendix 2). Burger (1983) questioned the validity of several species of Marathrum reported for Costa Rica. Novelo et al. (2009), in their treatment of Podostemaceae for Flora Mesoamericana, synony- mized eight species of Marathrum previously recog- nized by Royen (1951) under their broadened concept of M. foeniculaceum. Philbrick and Novelo (2004) proposed a broader interpretation of the genus Podostemum than Royen (1954), — Devillea and Crenias (Mniopsis) with Podostemum. The species pri: employed by Philbrick nd: Nr (2004) w markedl expanded. Royen (1954) pua 23 species (and six varieties) of Podostemum (including Devillea and Crenias), while Philbrick and Novelo (2004) reported 11 species and two subspecies in the single genus Podostemum. Philbrick et al. (2009) proposed five species of Castelnavia, compared to the nine recog- nized by Royen (1954). Lastly, Bove et al. (in press) reduced the number of species recognized in Lophogyne from two to one. Insight from herbarium holdings. Examination of herbarium holdings (Appendix 1) indicated broader distributions for many species than reported by Royen (1951, 1953, 1954). Royen (1954) reported Monostylis capillacea Tul. and Lonchostephus elegans Tul. only from the Amazon River in the Brazilian state of Para. Herbarium holdings documented a broader distribu- tion for both. The former exhibited a broader range in Brazil (Mato Grosso, Rondônia, Tocantins; also see below) and also occurred in Bolivia (Santa Cruz). The latter species was also documented from Mato Grosso and Tocantins (Brazil). me species of Apinagia and Oserya were more widely distributed than idend reported. Apinagia pe (We occurred in Ecuador, although Royen (1951) had listed it from only Peru. Werkhoven and Peeters (1993) reported that A. nana Went, a species not recognized by Royen (1951), occurred in two river systems in Suriname. Field collections by one of us (Philbrick) indicated that this species is abundant in Suriname and Venezuela, as is 0. perpusilla (Appendix 1). Even species that Royen reported as common in the Amazon River (northern Brazil, Colombia, Venezuela, Guyana, Suriname). Field and herbarium studies indicated that it ranges south of the Amazon River in Brazil in Goiás, Mato Grosso, Rondónia, and Tocantins (Appendix 1; also see below). Marathrum utile Tul, a species previously reported from Venezuela and Colombia to Costa Rica, has also been documented from Hon- MAJOR AREAS, HYDROGRAPHIC BASINS, RIVER SYSTEMS, RIVERS Distributions for 22 species documented using GIS varied in terms of the number of major areas, hydrographic basins, river systems, and rivers in which they occurred (Table 1, Figs. 1-3, Appendix 3). Eleven species occurred in the Amazon River System hydrographic basin (Fig. 1), with seven taxa restricted to the region: Castelnavia fluitans, C. mo a, both forms of C. multipartita, C. noveloi, Daub capillacea, and Podostemum flagelliforme. Castelnavia fluitans, C. multipartita (both taxonomic forms), and Monostylis capillacea were documented rom the Madeira, Tapajés, and Tocantins river systems, where they occurred in at least six rivers. ree of the species restricted to the Amazon River System hydrographic basin (C. monandra, C. noveloi, P. flagelliforme) were documented only from the Tocantins River System; all three were single-river endemics. Castelnavia monandra and the apparently extinct P. flagelliforme (cf. Philbrick & Novelo, 2004) were documented from the Araguaia River. Castelna- via noveloi occurred only in the Taquarugu River, a tributary of the Tocantins River. Four species that occurred in the Amazon River System hydrographic basin also occurred in other major areas or hydro- graphic basins (see below). The number of species per river system ranged from one to nine. The Tocantins River System was the most species rich (10 species), followed by the Madeira and Tapajós river systems (six species each). Eight species occurred in the Paraná River System hydrographic basin (Table 1, Fig. 2, Appendix 3), with five taxa restricted there: Podostemum comatum, P. distichum, P. irgangii, P. muelleri, and P. rutifolium subsp. rutifolium. Podostemum distichum and P. rutifolium subsp. rutifolium spanned greater than 40 rivers each; the former in 12 and the latter in eight river systems. In contrast, P. comatum had a narrower distribution (six river systems, 13 rivers), while P. irgangii was known from a single river system and two rivers. None of the species that occurred in the Paraná River System were single-river endemics. Three species documented from the Paraná River System also occurred in other major areas or hydrographic basins (see below). The Paraná hydro- graphic system contained the most species (seven), closely followed by the Uruguay River System with five. The remaining river systems had one to four Annals of the Missouri Botanical Garden pedunculatum and Cipoia ramosa occurred only in the Sáo Francisco River System; the former in four rivers and the latter in one. Four species in the eastern Brazil area were shared among other major areas or hydrographic basins (see below). Six species occurred in the Sáo Francisco River System. The Doce and Paraíba do Sul river systems each had five species, with one to four species occurring in the remaining systems. Five species were documented from more than one major area or hydrographic basin (Castelnavia prin- ceps, Cipoia inserta, Podostemum scaturiginum (Mart.) C. T. Philbrick & Novelo, P. weddellianum, Weddel- lina squamulosa) (Table 1, Figs. 1-3, Appendix 3). Podostemum weddellianum (Table 1, Figs. 2, 3) occurred in the Eastern Brazil Area and Parana River System. Castelnavia princeps and P. scaturiginum both occurred in the Amazon River System, while Cipoia inserta was documented from only the former two gions. Eastern Brazil Area, and Paraná River Sytem Only one species considered herein (W. m occurred in the Guiana area and Orinoco usr System regions, as well as the Amazon River System (Fig. 1). Species that sp d tł single major ar or hydrographic basin did not wasa equal distin tions in the respective regions. For example, as man rivers in the Amazon River System had Castelnavia princeps as the Eastern Brazil Area and Paraná River System combined. Both P. hice Brazil Area, with Weddellina squamulosa being most common in the Amazon River System. The number of species per river ranged from one to five dar 3). Only a single species was documented from a majority (> 65%) of the ca. 200 rivers apnea Two rivers (Aripuana, Teles Fass) in the Amazon River System had five species each. Several rivers in the Amazon and Paraná hydrographic systems each had four species. Current taxonomy: estimates of endemism. Thirteen of the 20 genera possessed at least a single one-river endemic species (Table 2). All species in three genera (Macarenia, | sp.; Tulasneantha, 1 sp.; Wettsteiniola, 3 spp.) were one-river endemics. For the other 17 genera, the percentage of one-river endemism ranged 0% (Diamantina, Lonchostephus, Lophogyne, Monostylis, Tristicha, M ELM 71% (Oserya). The two larges genera (Apinagia, Rhyncholacis) had 43% (22 a and 32% (7 spp.) one-river endemism, respectively. Podostemaceae occur in 22 Latin American countries, 10 of which have at least a inse one- river endemic (Table a Brazil had the number of one-river endemic species (26). Within Brazil, the number varied by state. Eight states had at least a single one-river endemic species; Pará (7) and Goiás (6) had the most. It remains unclear where three of the one-river endemics were collected in Brazil. Guyana had eight one-river endemic species, while three countries (Argentina, Colombia, Suriname) had three each Seven genera possessed at least one two-river endemic species (Table 2; Apinagia, Jenmaniella, Marathrum, Mourera, Podostemum,. Rhyncholacis, Vanroyenella). The percentage of two-river endemism in these genera ranged from 9% in Podostemum to 100% in ce Pe MIRO UM The two largest genera (Api 1 41% (9 spp.) an 27% (6 os Maive endemism, respectively. IUCN Red List assessment. Species were placed preliminarily into one of five IUCN categories (Table 4, Appendix 2). Forty-one species, represent- ing seven genera, were scored as Data Deficient (DD) , Lo of questionable taxonomic status) Most DD were in Apinagia (19), Rhyncholacis (8), and ou. (6). Forty-five species in 13 genera were scored as Least Concern (LC). Genera with the most LC species were Apinagia (13) and Podostemum (9). Of concern from a conservation perspective were species in the last three categories: Vulnerable (VU), Endangered (EN), and Critically Endangered (CR). Eleven genera contained species that were scored as VU D2 (with a restricted distribution), with the most in Apinagia (18) and Rhyncholacis (9). Species in five monotypic genera (Diamantina, Lonchostephus, Ma- carenia, Tulasneantha, Vanroyenella) were also VU. Ten species in eight genera were scored as EN or CR (Table 4, Appendix 2). Apinagia peruviana and Marathrum striatifolium P. Royen were scored as CR by León (2006); we follow León's designations here. Ceratolacis erythrolichen (Tul. & Wedd.) Wedd. and Podostemum flagelliforme were assessed as because they have not been collected since their initial description in the 1800s, despite field studies in the region where they reportedly occurred (Phil- brick & Bove, unpublished data). Two species of Castelnavia (C. monandra, C. noveloi) were docu- mented each from a small region in a single river. Lophogyne sp. A was scored as EN Blab(iii) by Bove et al. (in press), because its populations are scatter and it occurs in rivers heavily impacted by dam construction. The remaining two CR species are in Wettsteiniola (W. accorsii (Toledo) P. Royen, W. apipensis). Available evidence indicates that there have been extensive impacts from pollution and dam 8, respectively, at the only known locations for are not scored as extinct because e i wx OLD EIL MEE a ec dC RR EL EM Ea adc ME LC ndo: Volume 97, Number 3 E et al. 2010 in Neotropical Podostemaceae efforts to locate them in their respective regions are as Table 3. The number of species and one-river endemics yet insufficient to make that determination. Estimates of geographic range based on the IUCN (2009) EOO criteria illustrate considerable variation among species (Table 1). Of the 22 species scored, six were restricted to areas less than 100 km?. Not surprisingly, these latter species. occurred in oly a 100,000 km”, and 10 species had > 200,000 km? most widespread species had values in excess of 1,000,000 km? (Castelnavia princeps, Podostemum distichum, Weddellina squamulosa) (Table 1). Regres- sion analyses indicated a significant relationship EOO for a species and the number of rivers cies occurred in (P < 0.05). The relationship, however, was weak (r^ = 0.23). Discussion Endemism is a relative term that can be applied at 1 ceratophyllum Michx., Tristicha trifaria) are endemic to the Neotropics. Species in South America, with the exception of P. rutifolium (cf. Philbrick € Novelo, 2004) and two species of Marathrum, are restricted to that continent. However, in our examination of endemism we us on species with narrower - geographic distributions. Our aim is to establish means for oo. which species are in need of conservatio eitis understanding is fundamental to inter- preting the degree of species endemism in Podoste- maceae. A goal of this study is to provide estimates that reflect current taxonomic understanding, realiz- ing that in much of the family "current" does not mean adequate. Such genera as Apinagia, Jenmaniella, Marathrum, and Rhyncholacis remain in need of taxonomic stu Clearly, the distribuon of species of Podostema- ~ “eae throughout Neotropical countries is not uniform. Brazil, Guyana, and Suriname are especially rich in Species (Table 3), while Central American countries _ have one to four species each. Not unexpectedly, one- Tiver endemism is highest in the most species-rich Countries, with Brazil (26 spp.) having the most. We propose that a river, rather than a location o where a given species occurs along a river, is the most o e way to assess species distributions for . Such a focus is also useful for i mpa terns of species diversi- Y, apan events that aaa rise to that biodiversity, Bei impacts that are detrimentally affecting it it. in each country. States are listed for Brazil. No. of No. of one-river Country species ^ endemic species (76) Argentina 8 3 (3196) Belize 1 0 Bolivia 4 1 (25%) Brazil 58 26 (45%) Amapá 3 2 (66%) Amazonas 13 4 (31%) Bahia 2 0 Ceará 1 0 Espírito Santo 4 0 Goiás 9 6 (67%) Mato Grosso 8 0 Minas Gerais 14 3 (21%) ik 14 7 (50%) Paraná 4 o. Piauí l 0 Rio de Janeiro 6 0 Rio Grande do Sul 5 0 Rondônia Í 0 eius 12 1 (8%) Santa Catarina 5 0 Sao Paulo 9 2 (22%) anti 10 3 (30%) Unclear state 3 2 (66%) Colombia 10 3 (30%) Costa Rica 5 0 Cu 1 9 Dominican Republic 1 0 Ecuador 1 9 El Salvador 1 x : French Guiana 8 Ó Guatemala 2 37 8 (22%) Guyana I 0 Mexico 6 1 (11%) Nicaragua ; > roams i 1 (25%) “asme 2 1 (100%) 0% Suriname a U 28 2 (7%) ruguay Q : Venezuela | — The latter ise—the nature of human impacts on cogent when one in 'eotropical pi of the family. — Elements of both — —_— of _ and the 1 * -yation units. Lo That is, sets of cataracts (or e cos Annals of the Missouri Botanical Garden Table 4. Summary of preliminary IUCN assessments for species in each genus recognized in current taxonomy. Total percent is based on the number of total species in the Neotropics (135). Genus Data Deficient (DD) Least Concern (LC) — Vulnerable (VU D2) Endangered (EN or CR) Apinagia 19 (37%) 13 (27%) 18 (35%) 1 [Cr Bla,b(iii)] (2%) Castelnavia 0 3 (60%) 0 se Ceratolacis 0 1 (50%) 0 1 [Cr B1b(iii)] (50%) Cipoia 0 1 (50%) 0 1 (50%) Diamantina 0 0 1 (100%) 0 Jenmaniella 6 (86%) 1 (14%) 0 0 Lonchostephus 0 0 1 (100%) 0 e Lophogyne 0 0 0 1 [EN Bla,b(iii)] (100%) Macarenia 0 0 1 (100%) 0 T Marathrum 1 (10%) 5 (50%) 3 (30%) 1 [Cr Bla,b(iii)] (10%) Monostylis 0 1 (100%) 0 0 Mourera 2 (33%) 2 (33%) 2 (33%) j 0: 4 (57% 2 (29%) 1 (14%) ha 2 ! 9 (82%) 1 (9%) 1 [Cr B1b(iii)] (9%) Rhyncholacis 8 (36%) 5 (23%) 9 (41%) 0 Tristicha 0 1 (100%) 0 0 Tulasneantha 0 0 1 (10092) 0 Vanroyenella 0 0 1 (100%) 0 ina 0 1 (100%) 0 0 Vettsteiniola 1 (33%) 0 0 2 [Cr B1b(iii)] (67%) Total 41 (30%) 45 (33%) 39 (29%) 10 (7%) waterfalls) separated by expanses of quiet water support populations that interact genetically via seed dispersal. Large dams have the most pervasive detrimental impacts on species of Podostemaceae in the Neotropics. Both the reservoir upstream of a dam and the long reaches of rivers downstream that experience manipulated water levels are detrimental to populations. ONE- AND TWO-RIVER ENDEMISM parison of the current taxonomy with that of Royen (1951, 1953, 1954) indicated a reduction in the estimated number of one-river endemics from 48% to 37%. Ina general sense, such change is not surprising as the latter reflects five decades of additional study. Castelnavia and Podostemum, for instance, have recently been monographed (Philbrick & Novelo, 2004; Philbrick et al., 2009). In both, the proportion of one-river endemics has been reduced. Reduction in the number of recognized species of Marathrum by almost 50% is also notable (Novelo et al., 2009) in that th. k r : Rs 1 11 Guceda Dy only one. The taxonomy of much of Podostemaceae remains problematic (cf. Philbrick & Novelo, 1995; Ty, 2004). Future studies will no doubt result in -Tt is remarkable that of the 50 species (37% of the family in the Americas) currently interpreted as one- river endemics, 35 (70%) are DD; their taxonomic status is uncertain and including them in estimates may be misleading. Indeed, incomplete understanding of the taxonomy and geographic distribution of species hinders accurate estimates of endemism. Consequent- ly, we present two estimates. If upon further analyses all DD species remain recognized as taxonomically valid, then the 37% estimate of one-river endemism is meaningful. Conversely, if further analyses of DD o E i: 1 Ja nvmv then the percentage of one-river endemism would be reduced to 15%. As a result, our best estimate of one- river endemism in Neotropical Podostemaceae is between 15% and 37%. It is notable that 22 species (current taxonomy) are two-river endemics and about one third of them are DD. If all DD one- and two-river endemic species are supported as valid by further study, more than half of the family (54%) would be included. By contrast, if all DD one- and two-river endemic species (42 spp. total) are shown to be synonymous with other species, then 33% of the family would be one- or tweet endemics. Even if the latter is the case, one third is a significant proportion. À key issue, of coursa; 18 whether the presently documented species distribu- tions are accurate representations of actual distribu- tions. Results of ongoing field studies by the first mo authors (Philbrick, Bove) support the prediction that . for many species, they are not. Volume 97, Number 3 2010 Philbrick et al. 437 Endemism in Neotropical Podostemaceae Perhaps not surprisingly, the incidence of one-river _ (18.2%) and two-river (9.1%) endemism was mark- edly lower for the 22 species included in the river-by- river component of this study (see below) than e estimates based on Royen (1951, 1953, 1954) an current taxonomy. Many of these rai species were in genera that have recently been monographed. Consequently, their geographic ranges are more thoroughly documented. Reports in the early literature (e.g., Willis. 1902) . indicated that some species only exist at one small area in a river, e.g., a single waterfall or single set of river rapids. The whole-river approach utilized here does not allow us to test this idea, per se. It should be pointed out, however, that during field studies throughout Mexico and Central and South America over 15 years, only a single specks (Castelnavia noveloi) occurred at one “location.” Castelnavia noveloi is suwa known from only a 0.5-1-km region of the Taquarucu River, Tocantins, Brazil. Whether the species has a broader distribution in that river remains to be determined. MEASURES OF GEOGRAPHIC RANGE AND SPECIES ENDEMISM Geographic ranges for many Neotropical Podoste- maceae remain poorly documented. Representative species studied with GIS, most of which represent taxa south of the Amazon River, illustrate a diversity of geographic ranges. For these species we “sq ae two regional categories for discussion. “Narro regional species are those with a range of =500 bi along the longest geographic axis of their distribution, while the longest axis for “broad” regional species is a 750-1500 km. These categories, although arbitrary, provide meaningful reference points for discussion as they s presently documented species ranges. . Eight species, representing five genera, have narrow regional distributions in south-central Brazil. x One species of Cipoia (C. ramosa), the single species U of Diamantina, and one of two species of Ceratolacis (C. pedunculatum) occur only in central and south- eastern Minas Gerais, i.e., the Eastern Brazil Area —Ç — ee 3). The single species of Lophogyne (Lophogyne _ §p- A) is restricted largely to the state of Rio de Janeiro (Bove et al., in press; Fig. 3). Podostemum occurs in North, Central, and South America, yet the Ç majority (eight of 11) of the species are restrieted to the Paraná River System hydrographic region and . Eastem Brazil Area (Figs. 2, 3; cf. Philbrick & Novelo, Bue Podostemum flagelliforme is docu- _ mented a single location in Tocantins (Fig. 1). Podostemum irgangii, P. ovatum, and P. saldanha- "um all occur in several locations but have narrow pue 1-3; cf. Philbrick & Novelo, 2004). The former occurs in a small region in the states of Santa Catarina and adjacent Paraná. documented from a small region in the state of Rio de Janeiro. Among species in Mexico, where species distribu- tions are well known (cf. Novelo & Philbrick, 1997), there is only one narrow regional species (the one- river endemic Oserya longifolia). Although Podoste- mum rutifolium subsp. ricciiforme (Liebm.) Novelo & C. T. Philbrick has a narrow distribution in Mexico, ok E : £ ] If, * LES Ax (see fig. 26 in Philbrick & Novelo, 2004). A historic collection documents it for Costa Rica, but during recent fieldwork there it could not be relocated (G. E. Crow, pers. comm.). Many species have broad regional distributions. Species representing nine genera are presented as examples. Two occur in Mexico (Oserya coulteriana, Stu o plumosa), both on the western slope of the country. The former also is documented from Baja California Sur (Novelo & Philbrick, 1997). Apinagia nana and 0. perpusilla range from central Venezuela to southwestern Suriname (Werkhoven & Peeters, 1993; Appendix 1). The other examples occur primarily in Brazi il. Cipoia inserta spans from southeastern Minas Gerais northwest to eastern Monostylis capillacea, Lonchostephus elegans, d Tulasneantha monadelpha (Bong.) P. Royen span from northern Pará to western Mato Grosso . The former is also documented from to western Mato Grosso (Fig. 1). Five species (and one subs ies) of Podostemum are also broadly regiones Fig. 2). Podostemum scaturiginum n ur north of the previously mentioned four num occ Espírito Santo west to The former spans from m while the latter is common in Minas Gerais and Rio de Janeiro (Fig. 2). Moreover, Kelloff and Funk noted that seven species of J are endemic to the distribution of the family in Central and South nd also in the America (Mexico to Argentina) à Old World (e.g. Royen. 1951). The largely FORA P. ceratophyllum ranges acrose across eastern 438 Annals of the Missouri Botanical Garden Figure 3. Distribution of 10 — a s. aco lL.7: e em e oe eset ied ie Teque ER i mat lat A: filled Renesas ipota ramosa; diamond, IRA open triangle, Lophor yne Sp- - Square, ovatum; Poe plus sign, P. saldanhanum: filled filled triangle, P. scaturiginum; open asterisk, Volume 97, Number 3 2010 Philbrick et al. 439 Endemism in Neotropical Podostemaceae north to New Brunswick and Nova Scotia, c with disjunct populations in Honduras e Dominican Republic (Philbrick & wre 2004). Weddellina squamulosa exhibits a wide distribution across Venezuela, the Guianas, and northern and central Brazil (Fig. 1). Mourera fluviatilis Aubl., the most easily recognized member of the family, is broadly distributed across northern South America (Venezuela, Guyana, Suriname, French Guiana, northern Brazil). Several species of Apinagia (e.g., A. longifolia, A. richardiana) also show a broad distribution across northern South America. Estimates of EOO (IUCN, 2009) also demonstrated a diversity of geographic ranges among species. Not poe species with the lowest EOO values (i.e., « 100 so occurred in the smallest number of rivers (one or two). Overall, however, EOO was shown to be a poor predictor of the number of rivers a species was documented from. As is true for other riverine . Species, EOO has notable limitations as a measure of geographic range of species of Podostemaceae. Such geographic estimates cannot account for the extent of appropriate habitat (i.e., river rapids and waterfalls) within an identified geographic range or selected river. Assessment of the number of rivers that a given species occupies is informative, but this measure is also limited in its value. A more useful measure of Species range is one that integrates the extent of appropriate habitat within a river. Such a measure has not yet been developed for Podostemaceae. MAIN AREAS, HYDROGRAPHIC BASINS, RIVER SYSTEMS, AND RIVERS Consideration of species distributions within hydro- graphic regions, major areas, river systems, and rivers, although limited in taxonomic scope (22 species), was revealing. All three main focal areas or hydrographic basins (Amazon River System, Eastern Brazil Area, Parana River System) were similar in the number of Species they contained (eight to 10), yet each had unique elements of its podostemad flora. For example, the monotypic genus Monostylis occurred only in the Amazon River System, as did most species of . In the Eastern Brazil Area were species : E Ceratolacis and Diamantina, which did not occur - Although no genera were restricted to the Paraná River System, five species of Podostemum were. None of the three primary main areas or hydrographic ~ basins possessed a completely unique podostemad Mora, Conversely, some > of Castelnavia, Cipoia, and Podostemum hydrographic regions. In Some Lr maces, a majority | of a ee — tion hacin tha bises — regions. M sets "— ers. In the Amazon River System basin, three of the seven river systems contained six or more species; the Tocantins River System contained 10. The Eastern Brazil Area and Paraná River System also varied, with the number of species per river system ranging from one to six. Detailed analyses of broader taxonomic samples that consider how species diversity is related to drainage basin, river length, and other elements of river systems (e.g., geology, extent of appropriate habitat, latitude) are Werkhoven adi Peeters (1993), in their consider- ation of Podostemaceae in Suriname, were the first to distributions. Such contained more than one. more than a single species ranged from 15 (24%) in the eastern Brazil area, to 35 (34%) and 12 (39%) in the Paraná and Amazon river systems, respectively. Clearly all rivers se nat equali in ae quip. hi is also jes occur in tiba bend m channel Perhaps this is not pa as tributaries comprise proportionally more river system length than main man kaqt. IMPACTS ON PODOSTEMACEAE Rivers are heavily impacted tropical — Mito & E- Sioli, vw d et » 2006). ant threat patterns 1 in rivers is an especially important factor that reduces river. biodiversity (Young-Seuk r al., of dams (eg. h pd UN functions) seni in major changes to riverine biota (e.g., Petts, 1 on et al., 1989; Allan, 1996; Nilsson 200: Pringle et al., 2000; Odinetz et al s ; populations of de of Podostemaceae a & Nove 2004): seasonal water level change (crucial for sexual and seed ), solid substratum, duct Sr (i leas. seasonal) high light nd and a biofilm of bacteria. Field observations i 440 Annals of the Missouri Botanical Garden Table 5. Examples of large dams in Argentina, Brazil, Paraguay, Suriname, Uruguay, and Venezuela. For each, the river name, and estimated ir length upstream of dam are indicated. name, dam sais iini Me ES A Md c E M E Ma E M LM A tl dc cM. din DM EM A E KE M Med Lm CDU Country River Dam name Estimated reservoir length (km) Brazil Tocantins UHE Lageado-Palmas 110 Brazil Tocantins Serra da Mesa 130 Brazil Araguaia Tucuruí 110 Brazil Paraná Itaipu 140 Brazil Tieté Trés Irmáos 150 Brazil Paranapanema Jurumirim 70 Brazil Uruguai t 71 Brazil Uruguai Machadinho 40 Brazil Grande Água Vermelha 95 Brazil Grande mbondo 80 Brazil Grande Porto Colómbia 40 Brazil G: Volta Grande 60 Brazil Grande [unclear] 61 Brazil Grande Jaguara II 25 Brazil Grande Estreito 26 Brazil Grande Mascarenhas de Moraes 75 Brazil Grande Furnas 100 Brazil Sáo Francisco Sobradinho 320 Suriname Suri Afobaka Venezuela Caroní Guri 125 Argentina-Uruguay Uruguay Salto Grande 90 Argentina-Paraguay araná yretá 100 indicated that altering natural fluctuations in water levels disrupts sexual reproduction, and consequently recruitment via seed, which is fundamental to maintaining populations. Obviously, dams have a dramatic influence on water flow. Upstream of a dam the lotic hydrologic regime is changed into a lentic regime; a river becomes a reservoir. Inundation of river rapids and waterfalls by reservoirs makes them inhospitable to Podostemaceae. Such reservoirs can extend many kilometers upstream. Table 5 lists representative large dams in Argentina, Brazil, and Venezuela that multiple dams. For example, three are constructed ong the Tocantins River, with a combined reservoir length of about 280 km. The Grande River, which forms much of the boundary between the Brazili geomorphic effects (Graf, 2006). For example, pat- ao. ein, ad iming of peak d (e.g., Ward, 1982; Petts, 1984; Pringle et al., 2000). Poff et al. (1997) emphasized the importance of the timing of high/low water levels to river biota. Management of water release from dams results in temporal changes to flooding patterns relative to natural water flow, and thus impacts river biota. Nilsson and Berggren (2000) discussed how riparian communities are influenced downstream of dams, and Kingsolving and Bain (1993) showed that fish remarkable that water released from a major reservoir in Suriname remained low in oxygen for more than 100 km downstream (van der Heide, 1976). Change in on populations of Podostemaceae, which have been shown to be negatively influenced, or lost altogether, downstream of large dams (Jégu & dos Santos, 1987; Odinetz-Collart et al., 2001). We predict that negative effects downstream of dams will extend as far as managed water level manipulations persist. Conse- quently, a large dam can have negative impacts 0n Podostemaceae populations for considerable distances both upstream and downstream. Anecdotal accounts indicate that large dams have resulted in the loss of populations of Podostemaceae. Dam construction was evidently a central factor n the t extinction of Wettsteiniola apipensis in the of Paraná River, Argentina (Tur, 1997). In Peru, one O O a aae ec cdd O Mab: A i EN A Ri CER cC PR dia - Volume 97, Number 3 2010 Philbrick et al. 441 Endemism in Neotropical Podostemaceae few locations for Apinagia peruviana is now covered by a hydroelectric dam (B. León, pers. comm.). Some of the locations in which ecological studies were conducted by Grubert (e.g., 1975, 1976) in the Caroni River (Venezuela) are now beneath the reservoir of the i Dam. The only known location where Podoste- mum flagelliforme (Philbrick & Novelo, 2004) y was documented is now covered by the reservoir associ- ated with the Lajeado Dam (Tocantins River, Tocantins, Brazil). Apinagia guairaensis Fiebrig an Wettsteiniola pinnata Suess. could well be extinct as a consequence of the submergence of the Sete Quedas waterfalls when the Itaipu hydroelectric dam was constructed in the Paraná River. In addition, the only known Brazilian population of Apinagia yguazuensis Chodat & Vischer has been lost from the Itaipu location. We predict that populations of many other species of Podostemaceae have been extirpated because of dam construction even though relatively few have yet been documented. Podostemaceae are restricted to habitats that are heavily impacted by human activities. Our prelimi- nary assessments of species of Podostemaceae using the IUCN categories are revealing. About one third of the species can be confidently assessed as being LC, i.e., occurring in enough rivers such that there is little current danger of extinction. The remaining two thirds are either DD, VU, EN, or CR. Taxonomic study is central to establishment of reliable estimates of species endemism and clarifica- tion of which species are in need of conservation. Many of the species presently recognized, and scored as DD, are based on single and/or incomplete _ tive plasticity. Understanding patterns of variation is key to establishing reliable taxonomies, and taxonom- ie understanding remains unreliable for about one ird of the species in the Neotropics. Increasing demand for hydropower has the potential to result in major negative impacts on Podostemaceae. x The Report of the World Commission on Dams (2000) estimated that > 90% of power generated in Brazil is from hydroelectric sources. Indeed, reliance on hydropower i in Brazil is projected to increase in the — - Pringle et al. (2000) reported that 70 dams are : — planned fo or the Amazonian region of Brazil alone, while : the Report of the World Commission on Dams (2000) E listed 140 “new hydro investments" for the next (decade. The degree of current and future dam _ onstruction is a key issue relating to conservation of Podostemaceae in Latin America, especially Brazil. the distribution of species in river systems and rivers provides a means of predicting where new large dam construction will have the most detriman wpa Such insight » petunt for disi CONCLUSIONS The present study provides an assessment of species distributions in in Neoimpienl Podostemaceae, with a focus on those that have the smallest geographic ranges. Species in the family exhibit a range of geographic distributions. Some are wide- spread, while others display progressively smaller ranges. One-river endemic species account for 15%- 37% 37% of the family. Further refinements of these estimates will only be possible after understanding of the taxonomy and distribution of species is enhanced. The percentage of one-river endemic species that are pony known taxonomically is neue (70%). species whereby the number d river systems and rivers is taken into account provides more meaningful insight for Podo- stemaceae e measures based solely on overall eographic ran E Systematic ds enhance understanding of the nature of species and their geographic distributions. Not surprisingly, pun in which specie eo mscocarphed: In each, the number of one-river endemics was reduced. Humans continue to bave wet ipae on gen rivers; Podost rivers for their eid. ‘Large dams disrupt the natural flow of rivers and thus negatively impact populations of Podostemaceae. Increasing pressures to tap the vast hydropower potential in South America will have negative consequences on the diversity of Podostemaceae on the continent. Literature Cited : Allan, J. D. 1996. Stream Ecology: Structure and Function Running Waters . Chapman & Hall, sif : Ameka, K. G. 2000. 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Ve Petts, . 1984. Impounded Rivers. x Wiley & lon. Philbrick. C. T. 2002. samanan aceae. P. 585 in S. A. Mori, G. Cremers, C. A. Gra J.-J. de AMEN S. V. Heald, M. Hoff & J. D. Mitchell | (editors, Guide to the Vascular Plants of Central French Guiana, Part 2: Dicotyledons. Mem. New York “ig Card 16. — —— & C. P. Bove. 2008. A new species of Castelnavia sls from s Brazil. Novon 18: . & T. . 2009. Nessun of Costabissio da om Bot. 34: 715-7 & A. Novelo R. 1995. New World Vododisueae: Ecological and evolutionary enigmas. Brittonia 47: 210- 222. — —— & — —. 1997. Ovule number, seed number and seed size in t and North American Podostemaceae. sp —— ——-. 2001. A new .. of Podostemum o e the states of Paraná and Santa . Brazil. Novon 11: 92-96. 2004. Mon h of Podostemum (enema) Syst Bot. Monogr. 70: 1-106. E. Irgang. . Two new genera of CR ith the state of Minas Gerais, Brazil. Syst. Bot. 29: 109-117. —",mO > € 2004b. A new species of Ceratolacis (Podostemaceae) from the state of Minas Gerais, Brazil. Novon 14: 108-113. - Volume 97, Number 3 2010 ——,J-D. o! M. B. Bain, J. R. Karr, K. L. Pestegaard, _ B.D. Richter & R. P. Sparks. 1997. The natural flow -~ regime: Å paradigm for river conservation. BioScience 47: | . 169-784. —TT ID. D. em a m Merritt & D. M. Pepin. 2007. S river dynamics by dams an m RE Proc. Natl. Acad. Sci. U.S.A. 104: 5732-5737. Pringle, C. M., M. C. Freeman & B. J. Freeman. 2000. Regional dinde of hydrologic simi nae on riverine macrobiota in the New World: d LL com- parisons. BioScience 50: 807-82. Report of the World Commission on I . 2000. Dams and Development: A New —€— = Decision-Making. Earthscan — Lid., 2007. Mene alcicornis (Tul.) P. familia E" temaceae en m P. van. 1951. The Podostemaceae of > New World. - Meded. Bot. Mus. Herb. Rijks Univ. Utrecht 107: Ls 53. The ee of the New World. II. Acta da Need. 2 54. The eit of the New World. III. 15-263. R. R. 1971. Podostemáceas. Pp. 2-36 in P. R. Reitz (odio, Finn Ilustrada Catarinense , Part la. Conselho Nacional de Pesquisas—Instituto Brasileiro de a Florestal, Herbario Barbosa Rodrigues, tajai Rutishauser, R. 1997. Structural and developmental diversity temaceae (river-weeds). Aquatic Bot. 57: 29-70 E. Pfeifer. 2002. Comparative morphology of Cladopus (including Torrenticola, Podostemaceae) from East Asia to north-eastern Australia. Austral. J. Bot. 50: 125—730. —. Schnell, R. 1969. Contribution : ipn h Podostémacées 1967. The Bis 2 uë Vascular _ Plants. St. Martin’s Press, New York. Sidi, H. 1986. Tropical virt init aquatic habitats - Pp. 383-393 in M. Soulé (editor), ein Biology. p Sinauer Associates, Sunderland, Massa Ee : Taylor, G. 1953. Notes on Podostemaceae for the revision of the Flora of eM be aia Africa. Bull. Brit. Mus. (Nat. Hist), Bot. 1: Tipper, N. P. E du C. P. Bove & D. H. Les. 16: tina: Wettsteiniola apipensis. Bol. Soc. A Poco 1987. Podostemáceae. Flora — de Entre Rios. Colece. E Inst. Nac. Tecnol. A. 6: 43-54. 1 1997. T, onomy of Podostemaceae in ee _ Aquatic Bat, s: 213-241. a especie de Marathrum (Podoste- emn cila pe bns para la Argentina. Hickenia 3: van der Heide, S. 1976. Hydrobiology of the Man-made Brokopondo Lake, Utrecht: [NSFSNA] eb Re- Search Report, Suri lijke Studiekring as. name, Part 11. Natuurweten-schappe- Nede Endemism in Neotropical Podostemaceae - pef, N. L. & D. D. Hart. 2002. How dams vary and why it Ve icas Vasculares de . qatters for me emerging science of dam removal. Venezuela. Central de Venezuela, Consejo BioScience 52: 659—668. llo Científico y Humanístico, Caracas. 9: 50-52. Werkhoven, M. C. M. & G. M. T. Peeters. 1993. Aquatic macrophytes. Pp. 99-112 in P. E. Over (oit) Freshwater of Suriname. Kluwer Academic Publishers, Dordrecht. Willis, J. C. 1902. A revision of the Podostemaceae of India ee 8 Ann. Roy. Bot. Gard. (Peradeniya) l: WWF International. . Rivers at Risk: Dams and the future of freshwater ecosystems. Pret quae 12 May 2010. oung-Seuk, P.J. P Lek, W. Cao & S. Brosse. 2003. Ld egies for endemic fish species threat- eli he The Ges Dun. Coen Bint 17: 1758. ; G. D. Ardizzone. 1979. Las aguas continentales fcis 8 & s ul Latin A ica. E MA 1 Cami de Ps Pesca nental pm sth bn Latina Tech. Pap. e m» pp- IA. La Paz: Apinagia boliviana P. Royen. BOLIVIA- Y ^u arinilla River, 18 May 1996, Ritter 3198 n eet River, E M" 1996, Ritter 3196 (NHA). em | P 7 July 2006, 2006, Philbrick 11145, e AAN, 27 l pre WCSU); Novo River, 10°15 1307S, 46°53'2°W. 15 June 2010, Bove et al. EE nana Went 40127. ls 55:28'46 W, 27 Oat 2007. o €— 2007, bebe et River. pineg suat Yn Oct. dg Philbrick = al. TR IN, 552323 "W, 30 da. a aa aa 6232 (BBS, W: WCSU); A 4°0'34.4°N, `54°48'36.1"W, n od cd WCSU); Maroni (Marow ^ e d Nov. 2007, Philbrick et al. 6258 (BBS. mA Sucre, pias n 6°28'5.5°N, easy. 9 Jan. 2007, a Engl. Pana Azuay: Patu Rives, 28 May 1943, Apinagia nana = ie RNA NES t EIER E cc EL ARA AA UM MEN EEUU 444 Annals of the Missouri Botanical Garden Cipoia inserta C. T. Philbrick, — & Irgang. BRAZIL. Para perpusilla (Went) P. Royen. SURINAME. Sipali- Goias: Alto Paraiso ros River, 14^9'38'S, Amotopo, Lucie River, 3°34’49’N, 57739'0"W, 21 Oct. 47735'39"W, 11 June 2010, Bove gn t 2205 (R, WCSU); 2007, Philbrick et al. s ess WCSU); Bufuhulu, Suriname Alto Paraiso de Goias, Preto River, 14°9'28"S, 47°50'10"W, — River, 4^1'27.7"N, 55? .6"W, 27 Oct. 2007, Philbrick et 11 June 2010, Bove et al. 2208 (R, WCSU); Alto Paraisode al. 6212 (BBS, cu nées Tapanahoni River, ias, Cobras River, 14°9’42"S, 47^3750"W, 12 June 2010, — 4?1'52"N, 54?47'57.7"W, 1 Nov. 2007, Philbrick et al. 6240 Bove et al. 2212 (R, WCSU); Teresina de Goias , Almas River, (BBS, WCSU); Jaba-Kondre, hen e River, 4%5'16.2'S, 13°46'42"S, 4725'22"W, 13 June 2010, Bove et al. 2222(R, 55%27'9.4"W, 27 Oct. 2007, Philbrick et al. 6216 (BBS, WCSU); Keyserberg, Zuid River, 3?4'6.7"N, 56^29'1.2"W, 15 lombardii Novelo, C. T. Philbrick & Irgang. Oct, 2007, Philbrick et al. 6145 (BBS, WCSU); Poeloegoedoe, RAZI Gerais: Lassance, Corrente River, [awa River, 4°19'23.5"N, 4°23'31.9"W, 3 Nov. 2007, T 442156"W, 21 June 2010, Boe et al. 2253 — philbrick et al. 6254 (BBS, WCSU). VENEZUELA. Bolívar: (R, WCSU). Sucre, Caura River, 6°53'59.7"N, 64°50'7.2"W, 9 Jan. 2007, elegans Tul. BRAZIL. Mato G Lasso et al. 6014 (CAR, We Idem, Nichare River, wa E > So. a LONE > 21, 6732/8. N, 64°49'48.9"W, 1 12 Jan 2007, Lasso et al. 6040 WCSU) T šo João E a E (CAR, WCSU), Sifontes, € aragua River, Vies Falls, 518/2855, 48°55'342"W, 22 s. € ap 61873'N, 633722 6"W, i Jan. 2007, Lasso et al. 6047 597 R. west) (CAR, WCSU). Weddellina squamulosa Tul. BRAZIL. Goiás: 60 km NW a Jilamito, c "e — of Portelandia, Matrincha River, 16°58'11"S, 52°37'15’W, Mass 8495 (EAP). e May 2000, Philbrick a al. 5587 acn, MEXU, hem aiapónia, waterfall of Bonito River, °48'51”. Veo. Nene Nd ee pilo: pri e June 5V42'11"W, 20 May 2000, Philbrick et al. se (ICN. al. 4410, 41 e 4413 (NHA, WCSU). . WCSU); Idem, Ribeiráo Monte, 16%57'7'S, min Mae Done Apiacós River, Cachoeira 50’0"W, 20 May 2000, Philbrick et al. 5600 (ICN, dos d Daie. 9°]9'11 95, "STA IBS W, 2 Sep. 2007 MEN WCSU). Mato Grosso: Apiacás, Apiacás River, 878 (R, WCSU); Apiacás, co River, Cachoeira dos Papagaio, 9°19’ 11. JS, 574 18.8"W, 21 Sep. e, 57°4'5.2"W, 21 Sep. 2007, Bove & Philbrick 2007, Bove & Philbrick 1879 (R, WCSU); M Pistas 1073, Aripuaná River, 109'50.9'S, 59%27'12.8"W, 23 Se rg & Steward P18570 (U); Aripuaná, Aripuana River, Bove & Philbrick 1895 (R, lg P Suan Cachoeira dos Dardanelos, 10°9’50.9"S, 56°27'12.8’W, 23 River, 9°57'2.3"S, 56°13'45.7"W, Sep. 2007, Bove & et 2007, € & Philbrick cs (R, WCSU); Juruena Philbrick 1889 (R, WCSU); A icum (Panelas) Roosevelt ver, Cachoeira Salto Augusto, 28 May 1977, Rosa & Santos River, 979'52.]"S, 60^44'11"W, 25 Sep. 2007, Bore 205 so es (Panelas), Roosevelt River, 9^9'49.2"S, — Philbrick 1902 (R, WCSU); Paranaíta, Teles Peres River, 8'W, 25 Sep. 2007, Bove & Philbrick 1906 (R, — 914'33.6/5, 565031.7"W, 19 Sep. 2007, Bove & Philbrick YGU. Alta Floresta, Teles Pires River, Porto de Areia, 1876 (R, WCSU); 29 km from rain Peixe River, ; ilbric 1852 (R, WCSU). Pará: Cachoeira Bobiré, Tapajóz River, 29 5580 (ICN, MEXU, WCSU). Pará: Jacareacanga, Sáo July 1923, Ducke s.n. (RB). Rondónia: Cachoeira de Sta. Benedito River, 9%3'11.5'S, 56°35’7.3’W, 18 Sep. 2007, Cruz, Jamari River, 28 June 1965, Pires & Martin 9974 (NY). Bove & Philbrick 1862 (R, WCSU). Rondônia: Pacaás Tocantins: Lajeado, Lajeado River, 9°50'9’S, 48°17'38"W. s 27 Mar. 1978, Santos et al. 280 (RB); Porto Velho, 18 7 July 2005, Philbrick et al. 5825 (MEXU, R, WCSU); Aug. 1963, Maguire 56718 (VEN). Tocantins: Lajeado, ueg, Taquaruçu River, 10°18'21"S, 48°10'18"W, 6 Lajeado River, 950'9S, 48°17'38"W, 7 July 2005, ug. 2005, Philbrick et al. 5832 (MEXU, R, WCS SU). Philbrick et al. 5822 (MEXU, R, WCSU). of riv hich gnized by Royen (1951, 1953, 1954) and current taxonomy, country in which each occurs, n number ers in whic ud was reported by Royen, and the current taxonomy, IUCN determination for each species, and source of i ion provided subsequent to Royen. Cook and Rutishauser (2001) transferred species of Mniopsis to Crenias. For vity, these nomenclatural changes are not shown hese: —a No. of No. of See rivers: rivers: iN Country’ Royen? Current? IUCN? Source Su., Fr. Gu. 2 ea MAJ ) P. hon Br. 1 5 " Bo. (2) (3) VU Appendix 1 s Mile. Ve. 1 1 VU Berry (2004) Br. Co Guy. 5 @ LC Berry (2004) Su., Ve - U 1 1 DD Volume 97, Number 3 Philbrick et al. 445 2010 Endemism in Neotropical Podostemaceae APPENDIX 2. Continued. No. of No. of rivers: rivers: Species Country! Royen? Current? IUCN Source cd digitata P. Royen Fr. Gu., Su. (2) 2 VU Werkhoven & Peeters P (1993) A. divaricata Tul. & Wedd. Br. 1 1 DD A. divertens Went ex Pulle Guy., Su. 1 4 LC Schnell (1969), Werkhoven & Peeters — (1993) —. Á. exilis (Tul.) P. Royen Em Sas Ve, 3 3 VU ) __ A. fimbrifolia P. Royen 1 2 VU A. flexuosa (Tul.) P. Royen i Gu., (2) 4 LC Schnell (1969), Werkhoven & (1993) Á. fluitans P. ag Bo. 1 1 DD .. À. fucoides Tul Br. 4 4 LC A. glaziovii (W. arm.) P. Royen Br. 1 1 DD A. goejei Went ex Pull Su. 2 2 VU D. guairaensis Fiebrig Par. 1 1 DD A guyanensis (Pulle) P. Royen Fr. Gu., Su., (6) > LC Ve A. hulkiana (Went) P. Royen Guy., Su 2 2 VU unie & Posters A. imthurnii (K. I. Goebel) P. Royen Guy., Su 1 2 vu aon pr di » ES 1 VU Schnell (1969) _ A. kochii (Engl.) P. Royen Br., Fr. Gu., 1 > 15 LC Ph E Ve A. latifolia (K. I. Goebel) P. Royen Guy. 1 1 DD A. E (K. I. Goebel) Guy. 1 1 DD Ee Schnell (1969), x A. inde (Tul.) P. Royen Fr. DUM (5) >15 LC Werkhoven & Peeters Su., (1993), Velá (1994), Berry (2004) a | Schnell (1969), E — A. marowynensis (Went) P. Royen Guy., Su. (2) 2 rH Werkhoven & Peeters Es — (1993) x A membranacea Tul Br. 1 T “as A. minor P. Ro: yen Br. 1 1 Velásquez (1994), Berry A ulibranchiata (Matthiesen) Ve. 1 4 (2004) C hi nana Went Su., Ve. n.a. 7 a (1993), Appendix 1 P. Royen) P. Royen Su. 1 3 (1993) : Blabüi) scored by León (2006) A. peruviana (Wedd.) Engl Ec., Pe. 1 x ew NA Hollander & Berg (1983) Petiolata Ho Su. n.a. 1 DD A. pilgeri Mildbr. Br., Su 2 a DD 4 Plabstigma P: Royen Br. 1 1 U DD A. psyllophora Tul. & Wedd Br. 1 ! DD pusilla Tul. Guy. 1 1 00 Á. pygmaea Tul. Br. y : DD A. rangiferina P. Royen Br. 1 : A eee id Annals of the Missouri Botanical Garden APPENDIX 2. Continued. No. of No. of rivers: rivers Species Country! Royen? C IUCN? Source A. richardiana (Tul.) P. Royen Fr. Gu., Guy, > 20 > 20 LE Schnell (1969), Su., Ve. Werkhoven & Peeters (1993), Velasquez (1994), Philbrick (2002), Berry (2004) A. riedelii Tul. Br. (6) (6) LE A. ruppioides Tul. Co., Ve. 1 3 VU Velásquez (1994), Berry i (2004) A. secundiflora Pulle Guy., Su. (2) (3) VU Schnell (1969), Werkhoven & Peeters (1993) A. spruceana (Wedd.) Engl. Br. 1 1 DD A. staheliana (Went) P. Royen Guy., Su., Ve. (5) >15 Le Werkhoven & Peeters (1993), Velásquez (1994), Berry (2004) A. surumuensis (Engl.) P. Royen Br., Guy., Su. (3) (3) VU A. tenuifolia P. Royen Br. 1 1 DD A. treslingiana (Went) P. Royen Su. (4) (4) LC Werkhoven & Peeters : (1993 A. versteegiana (Went) P. Royen Su. 2 2 VU Werkhoven & Peeters 1993 A. yguazuensis Chodat & Vischer Ar. 1 1 VU = nok gos parit P. Royen n.a 1 in. id Philbrick et al. (2009) pnnceps LE & E n.a. 1 n.a. n.a. Philbrick et al. (2009) : fluitans Tul. & r. Br. 1 7 LC Philbrick et al. (2009) C T Pg x w edd. na. 1 n.a. n.a. Philbrick et al. (2009) a —— ti TA I 1 1 CR Philbrick et al. (2009) C : i C. T. Philbrick 2 e 1 9 LC Philbrick et al. (2009) C. P. Bove - n.a. 1 CR Philbrick & Bove (2008), cC >: Tul. & Wedd i Philbrick et al. (2009) C : ed j Tul. & Wedd : (8) 11 LC Philbrick et al. (2009) [see C. fluitans] na. 1 n.a. n.a C. serpens Tul. & Wedd Kx 1 ` [see C. fluitans] = ins Ceratolacis erythrolic (Tul. & Wedd) ae Br. 1 1 CR Blb(ii) Philbrick et al. (2004b) oe . T. Philbrick, Br. n.a. 4 VU Philbrick et al. (2004b) Cipoia inserta C. T. Philbri Tank & Irgang epee T Ws 13 LC Philbrick et al. (20044). b Appendix 1 r. n.a. 1 CR Bove et al. (2006) me. 1 n.a. Kd Philbrick & Novelo (2004 Br. na. 3 VU Philbrick et al. (20042). Appendix 1 Guy. 2 (7) LC Velásquez (1994), Berry : 2004 Br. l 2 vU pes Guy. (l) (1) DD Guy. 1 1 DD Guy. 2 2 DD X ME UE M C kipya aun UE E S Volume 97, Number 3 Philbrick et al. 447 2010 Endemism in Neotropical Podostemaceae x — APPENDIX 2. Continued. No. of No. of rivers: rivers: s Species Country! Royen? Current? IUCN’ Source T J. tridactylitifolia Engl. Guy. 2 (2) DD ~ Jvarians Engl. Br., Guy. 4 4 DD Lonchostephus elegans Tul. Br. 1 3 VU Appendix] - - Lophogyne a a & Wedd. n.a. (8) n.a. n.a. Bove et al., in press [see Lophogyne + >a Tul. ES cd n.a. (4) n.a. n.a. Bove et al., in press sp. do a Lophogyne sp Br. n.a. 10 VU Bove et al., in press x erg P. Royen Co. 1 (1) VU —. Marathrum aeruginosum P. Royen Ve. 1 2 VU Velásquez (1994), Berry (2004) _ M. azarensis Tur Ar. n.a. 1 VU Tur (2003) . M. capillaceum (Pulle) P. Royen Er. Gu. Cuy, 3 (7) LC Schnell (1969), Su., Ve. Werkhoven & (1993), Velásquez u (1994), Berry (2004) M. cheiriferum P. Royen [see M. na. (6) n.a. n.a. Burger (1983), Novelo et m al. (2009) M. cubanum C. Wright Cu. 2) 2 DD a M. elegans P. Royen [see M. ia. 3 n.a. n.a. Novelo & Philbrick foeniculaceum] (1997), Novelo et al. ( M. foeniculaceum Humb. & Bonpl. Be., Co, CR, (Ge A LC Burger (1983), Novelo et Ec., Gua., al. (2009) Ho., Me., Ë Ni., Pa. & Philbrick ieniculaceun "m i it m x (1997), Novelo et al. E Novelo et M. leptophyllum P. Royen [see M. n.a. 1 n.a. GIE Boer (1969) — Joenic um] s esa. “t |` M. minutiflorum Engl.* [see M. - 0 — na wg eit —. V. oxycarpum Tul. [see M. n.a. (7) "- € € 2 Ere “al, 2008) x M. pauciflorum Tul.* Guy. (3) (3) e M. pusillum P. Royen [see M. n.a. 1 .. An ] Novelo & Philbrick M. rubrum Novelo & C. T. Philbrick n.a. n.a. nr v. n 1997), [see M. foeniculaceum] Novelo et al. (2009) Burger (1 Novelo € na > 20 n.a. ns. š ( d A, Novelo et al. (2009) Velásquez (1994), Berry Br., Ve 2 (6) M (2004) — x ` ao on Burger (1983) n. - seored by León (2006) Pe. 1 J "s EM > Burger (1983). Novelo & C.R., Gua., >p >» Philbrick (1997) Me : name; Novelo $ Me. : (2) n. Philbrick (1997) a cde DE Annals of the Missouri Botanical Garden APPENDIX 2. Continued. No. of No. of rivers: Species Country! Royen? Current? IUCN? Source M. utile Tul Co, CR, Ho, (IO > 20 EE Burger (1983), Be e (2004), Appendix 1 Mniopsis erulsiana Warm. n.a. 1 n.a. n.a dubious species; Philbrick & Novelo (2004) M. glazioviana Warm. [see n.a. 7 n.a. n.a. Podostemum ovatum] M. saldanhana Warm. [see n.a. 1 n.a. n.a. Philbrick & Novelo Podostemum saldanhanum] 2004 M. scaturigina Mart. [see n.a. (9) n.a. n.a. Philbrick & Novelo Podostemum M. weddelliana Tul.* [see n.a. (12) n.a. n.a Philbrick & Novelo Podostemum weddellianum] (2004) lis capi Tul. Bo., Br. 1 10 LC Appendix 1 Mourera alcicornis ies P. Royen Br., Ve. z 3 VU Rial & Bove (2007) M. aspera (Bong.) Tul Tul Br. (13) (11) LG M. fluviatilis Aubl. Bi, Caya Sa, > 25 2-25 LC Schnell (1969), Ve. Velásquez (1994), B 2004 M. glazioviana Warm Br. 1 1 DD ari ' M. schwackeana Warm Br. 2 2 DD M. li Br. 2 (2) VU Oserya biceps Tul. & Wedd. Br. 1 1 DD > Me. (3) > 20 LC Novelo & Philbrick O. flabellifera Tul. & Wedd. Br. 1 1 DD 0. n & Me. n.a. 1 VU Novelo & Philbrick . i. MDTIC! xr (1995, 1997) O. minima P. Royen Su. 1 1 DD Werkhoven & Peeters : (1993) O. perpusilla (Went) P. Royen Guy., Su., Ve. 5 7 LC Schnell (1969), Werkhoven & Peeters (1993), Velásquez (1994), Berry (2004), Podostemum agui Chodat in 3 ih Vischer [see P. distichum] Jd 5" P. atrichum Chodat & Vischer na. 2 [see P. distichum] s "S ci Micha” N.A., Do, Ho. >50 >50 LC Philbrick & Novelo P * comatum Hicken € Br., Par., 1 13 Hé Philbrick & Novelo r. P. A P. Royen [see ee ee l P. muelleri] x 1 n.a. n.a. Philbrick & Novelo P 2 PR (2004) eren [nce am l n.a. n.a. Philbrick & Novelo F "e Cham.) W. ; isum e Br., Par, — (4) > 25 LC Philbrick & Novelo P. flagelliforme (Tul. & W T MERE edd)C.T. Br 1 1 CR Blb(ii) Philbrick & Novelo P. fruiculosum (Tul. & W ond edd.) Wedd. Br. 1 n.a. n.a. dubious species; a U O M Philbrick & Novelo A E A RISE ETET - Volume 97, Number 3 Philbrick et al. 449 - 2010 Endemism in Neotropical Podostemaceae APPENDIX 2. Continued. No. of No. of rivers: rivers: Species Country! Royen? Current IUCN* Source P. galvone Warm. [see P. muelleri] n.a. (3) n.a. n.a. Philbrick & Novelo 2004) P. glaziovianum Warm. [see P. n.a. (1) n.a. n.a. Philbrick & Novelo distichum P. irgangii C. T. Philbrick & Novelo Br. n.a. 2 VU Philbrick & Novelo (2001, 2004) P. muelleri Warm. Ar., Br., Ur. (5) > 20 [G Philbrick & Novelo ; (2004) P. ostenianum Warm. [see n.a. (3) n.a. n.a. Philbrick & Novelo P. rutifolium subsp. rutifolium] (2004) P. ovatum C. T. Philbrick & Novelo Br. 7 d LC Philbrick & Novelo (2004) P. riccüforme (Liebm.) P. Royen n.a. 2 n.a. Ra Philbrick & Novelo [see P. rutifolium subsp. ricciiforme] m P. rutifolium Warm. subsp. rutifolium Ar., Br., Par., 4 >45 LC Philbrick & Novelo Ur. (2004) P. rutifolium subsp. ricciiforme Be., Me., Co., n.a. > 20 LC Philbrick & Novelo (Liebm.) Novelo & C. T. Philbrick C.R. — P. num (Warm. r. 1 4 VU Philbrick & Novelo C. T. Philbrick & Novelo (009 P. scaturiginum (Mart) C. T. Philbrick Br. 9 12 LC Philbrick & Novelo & Novelo e: P. schenckii Warm. [see P. distichum] n.a. (10) n.a. n.a. n Novelo P. undulatum P. Royen* [see P. n.a. (5) n a Pulbeick & Novelo comatum — P. uruguayense Warm. [see i: 2 iK na. Philbrick & Novelo P. muelleri (2004) A P. weddellianum (Tul.) C. T. Br. (lo) > w a "T Philbrick & Novelo vU ) Rhyncholacis apiculata P. Ro G 3 3 i . Royen uy. f i R. applanata K. I. Goebel* Guy., Ve. 1 (6) n T M enr (2004) R. brassicifolia P. Royen Co. 1 1 es I brevistamina P Royen Guy. 2 A e carinata P. Royen Br. 1 á Velásquez (1994), Berry R. coronata P. Royen Guy., Ve. 1 2 Y: (2004) E crassipes Spruce ex Wedd. Br. 2 a Werkhoven & Peeters - cristata P. Royen $a. 1 (2) (1993) VU Werkhoven & Peeters R. dentata P. Royen Su. 2 2 (1993) E LC Velasquez (1994), Berry R. divaricata Matthiesen Ve. 1 * (2004) Berry (2004) x Jlaeellfolia P. Royen Ve. 6) = ~ guyanensis P. Royen Guy. á (1994). Berry a LC Velasquez pone R. hydrocichorium Tul. Guy., Ve. (3) (6) (2004) LC i Engl.* Guy. 3 e Velásquez (1994) R. linearis Tul. e Guy., Ve 2 (3) ed elásquez ( : minor P. Royen Br. 1 : DD $ nitelloides (Wedd ) P. Royen Br. 1 1 DD > P. Roy a) Berry (2004) Annals of the Missouri Botanical Garden APPENDIX 2. Continued. No. of No. of rivers: rivers: Species Country Royen? Current? IUCN? Source R. penicillata Matthiesen Ve. 1 6 Le Velásquez (1994), Berry (2004) R. unguifera P. Royen Br. 1 1 DD R. varians Spruce ex Wedd.* Br. 2 (2) VU Tristicha trifaria (Bory ex Willd.) widespread > 25 > 50 LC Burger (1983), Cusset & Spreng. Cusset ( Velásquez (1994), Novelo & Philbrick (1997), Berry (2004) Teu monadelpha (Bong.) Br. (1) (1) VU Vanroyenella r^ Novelo & Me. n.a. 2 VU Novelo & Philbrick C. T. Philbri (1993b) Weddellina pens Tul.* Br,Co. Guy, (10) 225 LG Werkhoven & Peeters Su., Ve. (1993), Velasquez 1994), Berry (2004) Appendix 1 Wettsteiniola accorsii (Toledo) Br. 1 1 CR Blb(ii) V. Bittrich, pers. comm. P. Royen W. apipensis Tur Ar. n.a. 1 CR T Tur (1975, 1997) W. pinnata Suess. Br. 1 1 Abbreviations: Ar., Argentina; Belize; Bo., Dominican Republic, Ec., cie de F r. Gu., French Guiana; Gua., merica; n.a., not applicable; Ni., Nicaragua; Pan e Uruguay; Ve., Venezuela. Bolivia; Br., — Co., Colombia; C.R., Costa Rica; Cu., Cuba; Do., Mtn. Guy., Guyane Ho., Honduras; Me., Mexico; ; Par., Paraguay; Pe., * Species in which infraspecific taxa are recognized but not listed here. ; en is listed only E. ^ ln ERAT in the current taxonomy. rivers in parenthese T E. explanation of IUCN nen E. see IUCN (2009). Peru; Su., Suriname; Ur., Volume 97, Number 3 Philbrick et al. 451 . 2010 Endemism in Neotropical Podostemaceae APPENDIX 3. The Vence of 22 representative species and two ti ic forms in each of fi e hy drographic regions or - major areas as demarcated by Ziesler and Ardizzone (1979). Withi hh th and rivers that ae ts taxon is documented from are indicated with a "ei one. The last dn lists the total species documented from each river. š 3 š š š 23 š " a ES ás š r : sag S j | sË, tea ii s$334.:3 2 1333122312333 E blils ii š SE Titer p S ii :33131322:2:3238211]32 33351 SSSESSSSESERE Ë Š Ë Ë 3 FEEEEEEEHHHHEHHHHEEHHETE River & š Š Š Š š 8 š ° E £ 3 ' 0 Region System River S L LLZ AzS II IRRA Amazon Cumina umina 11 River Japurá Apaporis Ki System Uatuma ri Malus — Agde 1 1 ds Aripuana 1 I d > Guariba 1 1 1 amari 1 : Juruena 1 1 * i 11 Pacáas Novos 14 Roosevelt 1 1 1 11 gro aupés 1 Tapajós Itenez i (Guaporé) 13 Juruena 1 1 Nob 1 15 Teles Pires 1 I 1 14 Sao Benedito l| I 1 1 Tapajós A 1 4 Tocantins Araguaia 11 1 12 Bonito 1 l1 Cachoeirinha 1 Cobras 1 1 1 1 2 Das Almas l 12 Lajeado l 1 1 Macaco 11 Matrinchá 11 eixe 1 R 1 li Ribeiráo Monte I Sao Patricio 1 1 2 Taquaruçu 1 1 l Ur it Trombetas Cachorro 11 Paru do Oeste 60400 0100010 00 003 019 o Total rivers 7 1 6 3 1 ispa a Missouri Botanical Garden Annals of the APPENDIX 3. Continued. Jaau tad saroadg Dso]mupnbs vuiappoA wnupiyjappam wnuasopog wmuigiungpos umwuejsopog umuptuppgps umwuojsopog wngofima *dsqns umiofirna wumuiajsopoq wumjpao uumauəlsopo,] 149]]omu UNUIISOPOJ tumənsip uumuəlsopo,] UMIDULO) UNUISOPOF D920/1d09 SYÁISOUO JA] y ‘ds audsoydoT pasur modi) wunpogmounpod s190]010.19/) sdaoutd viapujajsp?) 109004 DIADUJ95D/) nsompued *j nybdumu viapujoisp?) ppiapdugmu ^y oyiapdimu viavujaisp) Dapupuoui piaDujo1sp?) supmmjf miapujaisp?) River River System Region — 0) = = N A — — — — — p p i pd pd p 4 = r p| Bonito Cascatinha Caxambu Cidade Grande Imbé Leitáo uriaé Paquequer Paraíba do Sul Paraíba Preto Unknown river names (10) Monjolo Paraitinga* Volume 97, Number 3 2010 Philbrick et al. Endemism in Neotropical Podostemaceae APPENDIX 3. Continued. š i ii š 31 š E & T $9 5 Ë SET 3 da e i ile Lalitha fila, Jaana: SPP iE ETEN E A š 2.3 3 3.9 š Š 8 2 E R Midi dl 3 iver 2 š ` š A Region System River SIII ššš: $3332 São Francisco Bicudo ] 1 2 ue 1 1 2 Corrente t 1] 3 Imbaiacaia 1 1 Pari 1 1 2 Paraüna 1 1 Paraopeba 1 1 icáo 1 1 2 Santo António 1 1 Sáo Bento 1 1 bl 1 l Sao Joao Aldeia Velha 1 i 2 Pelotas 1 1 Quartéis l | Sao Joao poy Sertáo Taquari 1 1 Soberbo 1 1 P. l 1 Vitória Cachoeira da 1 1 Gruta da Oneca Preto 1 1 Timbui 1 Total rivers ovuseri1n1i3N 008491 9504M? Guiana Corentyne Toekoemoetoe I1 Area Essequibo ssequi 11 Potaro 11 azarum i 11 i ; 11 Nickerie Nickerie $ Oyapock k + Saramacca Saramacca + Suriname iname Total rivers oeeneeeeeeees eee ee eee fe River Cataniapo + € bid = | d ics oops ria... 000 05 Paraná Caí* Caracol 1 River Pinto : i System Santa Cruz Ei : Camaquá* Apiüna Missouri Botanical Garden Annals of the APPENDIX 3. Continued. RC ee a Ie PARDON a a at aspas A R E ETIR l9Au 19d soroodg — — NS - C] m — — NS — — — m -= = ld NA q — — — = — == = c 04 + CN € nsomuipnbs vuijoppoA umiofima 'dsqns umiofima wumuojsopog EH MA ca doge md = = m= _ - — wumpoao umuojsopog 119]]amui umuia1sopoq "t wp oye t pu. ui m — == pu pu pa, NÍUDIA UNUISOPOJ ao f1930]f wumuojsopoq UNYINSIP VUNWMIISOPOS | A 07 07 m m _ = m e e= — — - — UMIDUO) wumiwuajsopog m e rnt — n32njndvo sijÁjsouopy y 'ds ou£goudoT Dpanquioy OUIpUDUIDNT Dsoum4 modi) Dj40su1 v10di7) umgppnounped sioDjoqp427) sdoound viapujotsp7) pus - 10]2ü0u v1aDuja1sp?) nsompuoad *j oymdimu viapujojsp?) oyodinu ^y opupdimu mapujajsp?) DIPUDUOW DIADUJOISD/) supnni/ —A— £ ° š š Ë $ 3 Debt sists nda og oar dl ral = |: 334.1233. 0] gilt š P 8H 12.1181 iB ng arid B BEP RH Volume 97, Number 3 Philbrick et al. 455 2010 Endemism in Neotropical Podostemaceae APPENDIX 3. Continued. j : Sg š $3 š ER £ ` 3 | iii sss = E] BI. E. site dades O dali GEEESRRBBORE š š ŞE iib P PB gk 222222522885 283 1 Rive 433503 iiiiii i Region System River OgdoooooOooaS3s4ázaaignaizlaorak Ribeirão dos Fd San Ignacio l l Sapucai 1 Gran Tabay 1 : Tebicuary 1 : Trindade l : Verde 1 ! : Unknown river 1 Eos name Piratini* Lajeado p A ; ° Ribeira do Iguape ! y Igua| * 1 Sinos* Chuvisqueiro 1 1 Unknown I l Taquari* Antas ; 2 Camisa : 1 1 1 3 Fao 1 1 Forquetinha 1 2 Moraes I 1 1 Arroio Tatim 1 Tijela i 1 1 Unknown river a z 1 i Tubaráo* Tubaráo 1 1 Uruguay Barra Grande 1 l xe Do Castilhos : J iil 1 4 hapecó 1 d 1 3 Chapecozinho 1 1 Chimira 1 1 2 Conceição 1 1 2 l 1 1 l Guarita 1 1 1 l 4 Irani 1 1 - Jacutinga 1 1 2 aguari 1 1 Lageado 1 1 1 3 Paraíso 1 1 Pardo 1 1 1 3 Ass eR eae Na See er MTS LIE IRR REESE IIT D Jaa 1od seroedg | cu eX — — — e — c c 09 RENN HN nsopupnbs vuijoppoA, umiofima 'dsqns wnyofima wnuasopogd =o m SS o om meei o wungpao wnuasopod 119]]9NU UNUIISOPOF m P TA Tm nigupda1 wnuojsopog aui2ofijjadpjf umuia1sopoq unyousip tunuasopog | 7 ia = rs = e uNIDUOY UNUIISOPOJ | — et et "^ n3opjndvo siKqj50u0]py y ‘ds 2u&SoidoT MPLDQUO] DUYUDUDI Dsotubi piodhr) Dj12su1 D10di7) umppnounpoad $190]010.497) sdaoutd viapugjojsp) 10/9004 piaDugjajsp") nsompuod *j onimdigmu viapujojsp?) omuodanu ^y ppaodinui viapujojsp) DIPUDuou DIADUJI]SD/) Missouri Botanical Garden Annals of the supqmjf mamyaso) = : š fie e 8 & TE py > s 2 Ble PS38334 8353883 PPisbllrikbiliiilib A A A YN A&déa5bbsjscscd River st Region APPENDIX 3. Continued. tly into the Atlantic Ocean or coastal lakes, 0000030000 0 013 4 0 2 3304703 60 J € i.e., not into the Paraná River drainage basin. Grande Unknown river name Total rivers HONDURODENDRON, A NEW MONOTYPIC GENUS OF APTANDRACEAE FROM HONDURAS! Carmen Ulloa Ulloa,? Daniel L. Nickrent,? Caroline Whitefoord,* and Daniel L. Kelly* ABSTRACT Hondurodendron C. Ulloa, bie Whitef. & D. Kelly, a new monotypic genus endemic to Honduras, . urceolatum C. Ulloa, Nickrent, Whitef. & Di Kelly, is a dioecious tree, distinguished by its and illustrated. The new re minute flowers born totally enveloped a Cue accrescent c. small subunit [SSU] ribosomal nsely tomentose inflorescences, unique ——— DNA DNA]. chloroplast rbcL, matK, a is here described three valves, and a characteristic fruit placed this genus in a clade with Apiandra D) Miers, Harmandia Pierre ex Baill., Chaunochiton Benth., and Ongokea Pierre in the family Aptandraceae M RESUMEN Se describe e ilustra un nuevo género monotípico Hondurodendron C. Ulloa, Nickrent, Whisef. & D. Kelly ' endémico de onduras. La nueva especie H. urceolatum C. Ulloa, Nickrent, Whitef. & D. K inflorescencins densamente rt las — únicas que se i. por forts diminutas en ca Un análisis molecular con cuatro n (SSU ADN ribosómico nuclear, rbcL del _ mak y accD) ubica al género en un clado junto con Aptandra Miers, armandia Pierre ex Baill., Chaunochiton Be Key words: Adit Cusuco "a Park, Honduras, y Ongokea Pierre en la familia A Hondurodendron, 1U ptandraceae IUCN Red List, Olacaceae. During a plot-based survey of the forest vegetation of Parque Nacional El Cusuco in northwest Honduras in 2004 and 2006, specimens of an unknown tree were collected that proved difficult to place into any known Central American genus or family. The plant had distichous leaves and fine pubescence on the very young inflorescences, features reminiscent of the genus Acanthosyris (Eichler) Griseb. (Santalaceae), but it also possessed a greatly enlarged (accrescent) calyx that projected beyond the fruit as a conspicuous flared limb, thus suggesting Olacaceae s.l. The plant was dioecious, with remarkable anthers opening by three valves. Neotropical olacaceous genera with Field. We are gr accrescent calyces include Aptandra Miers, Chauno- chiton Benth., and Heisteria Jacq., but none of these genera possess the combination of morphological characters seen in the Honduran specimens. Compared with other Central American countries, Honduras is poorly known botanically with no published flora. The country checklist of Molina (1975) and the new í de las asculares de Honduras (Nelson Sutherland, 2008) were . but none of the Olacaceae - relatives onto in those lists the samples from Cusuco. Additional field cusa tions and collections that included both flowers and AAA Á0— — ‘All collections resulted from the a. of the odo e of Cusuco National Park, funded and organized ate var acea úñez-Miro, A. Tier, Fagan, C. Lenn kh, G. Sandoval, A. Bergoénd, € g sees E t School, St Alban' s. For collecting permi and its successor ization Í guides «c Ramírez, and others. For trastructure. Helpful —€— = m “Missouri Botanical Garden, * Departme ° Department of Botany, The Natural History Muse useum, C ` Department of Botany, Sohail of N. doi: 10.3417/2009040 Ann. Missouri Bor. Gap. 97: 457-467. a E rone For stint in the Geldwork, we d Graphics E of Harma microsc and to V. Malécot f vidi the Berhari specimen ul da b i ba PA yv. Malécot, Z. Rogers, and P. e improved the manusc . Louis, Missouri 631 .À. carmen nt of Plant a oa hern Illinois Universi, Natural Sciences, Trinity College, University of thank in particular R. Fritch, K. ve School, Birmingham, and 1 (COHDEFOR) and teachers of South ii fully ce istanc our nstituto de Conservación Fra RE Yee voii =s N. Robson kindly — the photographs, we utiful “asema add Hidalgo helped with determinin: n T and 6. ID to D. Gates and J. -Boszola (Southern ioi Harmandia ed Sr assistance with Pollen manuscript. .ulloa@mobot.org. í run qun. U.S.A. romwell Road, London SW7 5BD, United Kingdom of Dublin, Dublin 2, Republic of Ireland. PUBLISHED ON 10 OcroBER 2010. Annals of the Missouri Botanical Garden silica gel—dried leaf samples were obtained in 2008; ese have allowed the phylogenetic position of this mysterious plant to be confirmed MATERIALS AND METHODS PHYLOGENETIC ANALYSIS The specimens used for DNA extraction are listed in Table l. Samples were taken from (2008), except that the automated sequencer used to generate the new sequences reported here was an AB3130xl capillary system. (Applied Biosystems, Carlsbad, California, U.S.A.). PCR primer sequences for nuclear small subunit (SSU) ribosomal DNA (rDNA) and chloroplast rbcL, matK, and accD were reported in Rogers et al. (2008). Eight ingroup taxa were used in this study, representing all genera of Aptandraceae. Maburea trinervis Maas (E topology of the tree in Malécot and Nickrent (2008). Nine of the 40 sequences used in the alignment were generated in the present study, whereas the rest were reported by Malécot and Nickrent (2008). The sequences were aligned manually using SeAl version 2.0 (Rambaut, 2004), and this alignment is available weer —— bem -—- A , ace January 2010. BoranicaL GARDEN was published on 10 October 2010. vinim 5/14 www.mbgpress.org CONTENTS A Floristic Study of the White-sand Forests ofPeru |. Paul V. A. Fine, Roosevelt _ García-Villacorta, Nigel C. A. Pitman, Italo Mesones & Steven W. Kembel A Gaito Classification of the Danthonioideae (Poaceae) —_ H. Peter Linder, Marcelo Baeza, Nigel P. Barker, Chloé Galley, Aelys M. Humphreys, Kelvin M. Lloyd, David A. Orlovich, Michael D. Pirie, Bryan K. Simon, Neville Walsh & G. Anthony Verboom Revisión Taxonómica de las Especies del Género Verbena (Verbenaceae). II: Serie Verbena Nataly O'Leary, María Ema Mülgura & Osvaldo Morrone Endemism in Neotropical Podostemaceae — — — C. Thomas Philbrick, Cida P foie & Hannah I. Stevens Hondurodendron, a New Monotypic Genus of Aptandraceae from Honduras. < —— Carmen Ulloa Ulloa, Daniel L. Nickrent, Caroline Whitefoord & Daniel L. Kelly bo 83 Cover illustration. Ginoria pulchra (Ekman & O. C. Schmidt) S. A. Graham, drawn by Taciana Cavalcanti. Volume 97, Number4 Annals of the . ti Botanical Carden St a ed. Pate ens are e poerteviened by quid, in- lò Ant g tire Tammy Charron . Associate Editor, — Cirri Moran E Press Coonlinalos | Missouri Botanical Garden ee ae NIS ‘Charlotte Ta is Missouri Botanical Gib Rt Missouri Botanical Carden = -Henk van der Werff Missouri Botanical Garden For subscription. informations contact. Aandi x OF THE Missouri BOTANICAL - GARDEN, % Allo Mar- ki KS 6 $915 all The journal Ne o a A ie m 7. Sabac e price for 2010 L = $180. S E US., $190 Canada & Mexico, d me of the Annals. ce NT UOL We Tux ANNALS i OF m "m: Boranica, GARDEN (ISSN (09 6.6A00| ; erly by the u “Mason Botanica] Cada 2345 Tower Grove —— | = Avenue, St. Louis, MO 63110. Periodicals j post- 4 Ç age paid at St. Louis, MO and additional mail x ing offices. P ddr E ANNALS OF THE MISSOURI BOTANICAL. Dien % Allen Marketing & Mere Po. Box 1897, HY Hee: KS S GORG BONT. Ee pass sP SY ERE O y DOI A O NO: POSO TO O TO O O O ION TERR NNUS A PER IR O Volume 97 Annals Number 4 of the 2010 Missouri Botanical Garden THE POLLINATION OF MID Conrad C. Labandeira- «poh MESOZOIC SEED PLANTS AND A THE EARLY HISTORY OF wes? LONG-PROBOSCID INSECTS! jS ABSTRACT A defining event for Mesozoic Oe cea interactions is the angiosperm radiation, which extended the reach of pollinating insects during the Early Cretaceous in a brief interval of geologic time. Recent evidence indicates that events beginning in the Early Permian and increasing Suite the Middle Jurassic ata repeat opportunities for insect feeding on pollen, polline ion drops and mirpductire. tissues % esimi yas perm lineages. Polli ina tion was an associat e development. St d f tubular ue of gymnosperm ovulate organs that previously w were considered anomalous ‘and diffi cult to interpret. One mout thpa powered m a eben pum p. often assisted with a distal proboscis s sponging organ. These proboscises were received in ovulate organs through often: intricate Expres integume md tubes, interovular — i sapin tubuli, pappus tubules, M micropyles, and These ovulate stru also are consistent with insect access to — inm meing pollination repe, nectarial s Po E pollen. gs E for pollination is the and in insect guts, nutritional levels of sain soigne drop fluids similar to angiosperm nectar for supporting metabolically hia. activity levels of mci active insects, ani t-host outcrossing. While the long-r eo 'This and the following six articles are roceedings of the 56th Annual Systematics Symposium of the Missouri Botanical Garden, “Angiosperm DT. har js Trees, but Insects, F pi^ and Much More." The symposium was held 9— 11 October — * E Missouri Botanic: al Garden in St. Louis, Missouri U.S.A 2 This i tha Nat; 1 Teens Foundation T REA The meet ing w. organized and moderated hy. Peter s P. Mick Richardson ible for the smooth running of the symposium, M nA dE the welcome and able assistance of Mary McNamara, Donna e and William Guy; Victoria C. Hollowell, Beth Parada, Allison i and Tammy Cone | (Missouri Be Botanical Garden Press) were responsible for the publication of the symposium proc *] thank Peter Ph ia Fet etet Stevens for i invit ting and fun nding my pricipal i in MA Phylogeny and Biotic Evolution," at the 56th A tober 2009. I thank Ren Do en Capital Normal ee in Beiji jing, China, for funding travel to China for the spet n loan of Mesozoic fossil insec specimens, upon which new data are presented herein. In addition, I am Lome to Finnegan Marsh for rendering all figures Wenying Wu for technical assistance, and Mary Parrish for reconstructing the two plant—insect pollinator sid UC. depicted in Figure 5. Two reviewers improved the manuscript cons rip d Alexandr Rasnitsyn of the Paleontological Institute in Moscow, Russia, kindly loaned a specimen of tTschekardithonopsis ?oblivius for study. Xiang Wang provided data and images for +Problematospermum ovale. This is contribution 179 of the Evolution of Terrestrial Ecosystems Consortium at the National Museum of Natural History *Department of Paleobiology, N ational M um of Natural History, Washington, D.C. et tee U.S.A. labandec@si.edu. ? Department of Entomology, Univer of of Maryland, D Park, Maryland 20742, doi: 10. 3417/2010037 ANN. Missouni Bor. Ganp. 97: 469-513. PUBLISHED oN 27 DECEMBER 2010. 470 Annals of the Missouri Botanical Garden deployed uni l ducti t dist: from each other, either on the same or on different plants, another eS T T . . . . Ls ee a wee oe: * 11 EE £ Fiz. PA ab ac AN e a > ] nm R. I d - TES t E 61.123 f r Zak associations t new pollinator associations with angiosperms. Key : Bennettitaleans, Caytonia, Ch a E x t ¿KO OY J 3 > J eE $ T An irretrievably altered as angiosperms diversified during a 35-million-y patterr ist a i z E ie. = ae sb ss 1 \ TL P A I mM: + Z. $ F eo r r è : T ear interval of the Early Cretaceous, evident in three X d cs ak 1 go wl: X "D P D Joar, DCLCOLHU Was hat continue tod. relicts; and third was emergence of Cretaceous, Daohugou, Diptera, gymnosperm, Jurassic, long-proboscid , China, insects, Mecoptera, Neuroptera, pollination drops, seed ferns, Yixi & s> £ as ab s n r1 E £L + of flowering plants, commencing during the mid Early Cret. ] tinuine i | ly Late Cretaceous from 125 million years ago (Ma) to ca. 90 Ma. During this 35-million-year interval there were significant shifts in the major ecological associations among plants, fungi, insects, vertebrates, and other organismic groups domi- nant on land. This ecological chang lted i l transformation of terrestrial communities such that, by the end of the Cretaceous, there were few remaining taxonomic, ecological, or biogeographic biotal elements that were present at the beginning of the period (Friis et al., 1987; Lucas et al., 1998). These ecosystem-wide ñ. £f L A E £ 1.1 l f£. > ok sabi cobs ths ak ias: > + life on land, of y n > ] M t + L 1 F slk T. Y hd r er = ° eo a world that is familiar to us today. Discussions of the magnitude and consequences of the event associated with the diversification of angiosperms historically can be contrasted with what is known of the immediate, preangiospermous world of the earlier Mesozoic flora dominated by extinct gymnospermous seed plants of seed ferns, cycads, conifers, bennettitaleans, and gnetophytes, as well as ferns, sphenopsids, and bryophytes (Willis & Mc- Elwain, 2002; Taylor et al., 2009). Similarly, speciose insect clades that interacted with these plants included lineages that either became extinct or were represented by closely related, but early groups of extant lineages (Grimaldi & Engel, 2005). These major insect clades include mid Mesozoic representatives of the four major groups that have complete metamorphosis, the Coleop- tera (beetles), Hymenoptera (wasps, ants, and bees), Diptera (true flies, such as mosquitoes, midges, and rseflies), and Lepidoptera (moths and butterflies). Also included were representatives of currently less Ju L Kai a Y 3 : 1 1. the earlier Mesozoic, such as the Mecoptera capis flies), Neuroptera (lacewings, owlflies, mantispids, and antlions), and Trichoptera (caddisflies), and among clades with incomplete metamorphosis, the Hemiptera (aphids, whiteflies, scale insects, and bugs), Blattodea (cockroaches), and Orthoptera (katydids, grasshoppers, and crickets). Interestingly, the pattern for insects does not hold for the dominant megafaunal elements of the Mesozoic; dinosaurs and other lesser well-known lineages became extinct at the end of the Cretaceous. Recent evidence provides a broad understanding of how some gymnosperms were used in different ways by phytophagous insects. The expansion of earlier esozoic insect phytophagy was a worldwide event that began during the Middle and Late Triassic n addition, recent data have documented the reproduc- tive biology of pollinator relationships between preangiospermous plants and their insect associates. APPROACH In this paper, fossil occurrence data of pollen and nectar feeding, as well as known pollination modes between modem plants and insects, are mapped onto recent phylogenetic syntheses of major clades of extinct and extant seed plants and insects (Figs. 1, 2). A variety E xx š J ahii J 11 £ i uas EE w ae ] POE ÁG- eS fal distribution of inferred associations between gymno- sperm hosts with deep structures and their matching long-proboscid pollinators (Figs. 1, 2). Estab- lishment of the long-proboscid pollination mode is supported by recent and ongoing examination of the renmdiuct $ r ] J especially of co-occurring long-proboscid insect mouth- known from late Middle Jurassic and mid Early Cretaceous examples from China and temporally intervening deposits from elsewhere, espe- cially Eurasia (Engel, 2005b; Labandeira, 2005a; Labandeira et al., 2007a; Ren et al., 2009). Other types of inferred mid Mesozoic pollination modes also are i Lastly, I discuss the evolutionary and ecological patterns resulting from the gymnosperm to angiosperm transition in pollination style and its implications for angiosperm and insect history. Types OF EVIDENCE y A fon al v ell as pollination mutualisms in the fossil record requires " * ee a O kis a Ga ushika aaa a a a A ERAN IR S OREN NIRE ERE I A AE : x I Volume 97, Number 4 2010 Labandeira Pollination of Mid Mesozoic Seed Plants multiple types of evidence. The most important aspect of this evidence is consilience, particularly the interplay 1. = +L 47 X 1 To + features such as Oynlate ae architecture and pollen type (for a modern example, see Patt et al., 1997). The . evidence needed for recognition of a particular pollina- tion mode originates both from candidate insect and plant taxa as well as the environmental context of the ILI i NEL edi: s E Hi > several techniques; specifically, anatomical or morpho- logical reconstruction, use of various exploratory and confirmatory instrumentation, and the application of plants, suggesting a reward structure for a broader plant-pollinator association (Crepet, 1974; Norstog et al., 1995; Nishida & Hayashi, 1996; Klavins et al., 2005). Last, involving more modern fossils, the known biologies of particular plant and insect clades can be used to infer the associational dynamics of recent fossil ancestors (Labandeira, 20022). THE INSECTS The most obvious feature of an insect that reveals consumption of nectar or pollen, or the existence of a pollinator association, is the mout head Nee sh P re, 1990). asa. di Ë functional morphology. Establishing types of direct and donet paleoecological mo is pem Ww re- "erdt: x E m " Sx go : (D yes , 2009) Seven types of Ae are d to d the presence of palynophagy (pollen consumption), nec- tarivory (nectar consumption), and pollination in the fossil record (Labandeira, 1998, 2002a). First are insect mouthpart structure and its functional inter- pretation, including details of surface setation, cuticular ornamentation, specializations of the pro- boscis tip, and adjacent structures such as palps, sucking pumps, and antennae (Rasnitsyn, 1977; Rayner € Waters, 1991; Novokshonov, 1998; Ren, 1998; Szucsich & Krenn, 2000; Borrell 2005; Krenn et al., 2005). Se significant, are plant structures receiving the mouth- parts. For gymnosperms, such features would include catchment funnels, integumental tubes, pappus tu- bules, and micropylar extensions in ovulate organs consistent with i Bt pollination (Harris, 1933, 1940, 1951b; Kvaéek, 2000; Sun et al., 2001; Santiago-Blay et al., 2005; Anderson et al., 2007; Krassilov, 2009). Third, pollen size, shape, ornamentation, clumping, presumed stickiness, and abundance level indicate entomophily (Courtinat, 1980; Haslett, 1989b; Alvin et al., 1994; Zetter & Hesse, 1996; Axsmith et al., 2004; Hu et al., eae Meis is the occurrence of pollen on insect con surfaces such as the head capsule or oa (Caber 1972; Jervis et al., 1993; Nicholson, 1994; Labandeira, 2005a). Also, its preservation as intestinal contents directly links the based c on xu uk consumers of solid. food, typically that may bib "t or icai sap or cellular protoplasts, or alternatively surface fluid feeders that imbibe nectar; and (3) particle consumers that mostly access spores and pollen ME 1997; Krenn et al., 2005). When considering mouthpart structure, there are three groups of pollinators: (1) biting and chewing mandibulate mouthparts involved in palynophagy; and two modified, haustellate mouthparts involved in fluid feeding, put 2) Poenis, sponging, and lopping sucking mouthparts, particularly stylate esa Thy that puncture plant tissues and pollen grains for their contents, and effect lina S in the process. MANDIBULATE MOUTHPARTS of insect mouthparts used in nectarivory and palyno- phagy for effecting pollination, paper by biting and chewing, th dcdit tiom used for the coloniam; piis- ing, and consumption of pollen (Schicha, 1967; Fuchs, 1974; Kevan & Baker, 1983), although specializations for nectarivory are known for some taxa (Handschin, 1929; Schremmer, 1961). The ancestral condition in insects is mouthparts, which extends to the Early Devonian in primitively flightless insects, such consumer and consumed (Holloway, 1976; Krassilov as bristletails (Labandeira et al., 1988), occurring as & Rasnitsyn, 1983, 1996; Haslett, 1989b; Krassilov et peptic’ weak, milling mouthparts were housed in al., EER 3008, 2008 Afonin, D. "— onm intemal ponch os € pued e The more ERICO tH ES et d 1993; Labandeira, 2005a). Fifth, ühlousk š weaker source of evidence, dispersed coprolites often contain dicia pollen grains but rarely indicate the nsible palynophage (Harris, 1945; C 1974; Pa: Pant et al., 1981; Labandeira, 2002a; Lupia et al., 2002; Hu et al., 2008). Sixth, related plant damage an document herbivory or seed predation on host ~- and herbivorous lineages of ala (grasshop- pers and early relatives), Blattodea, Psocoptera (book- lice), and Coleoptera (beetles) were present in the Pennsylvanian and Early Permian (Labandeira, 1997). During the Permian, several insect lineages bore mouthparts forwardly directed on the head capsule that had palynophagous adaptations (Rasnitsyn, 1977; Missouri Botanical Garden Annals of the 472 Ea uoneuijod uiseJ/IO E= uolgulllod juəuudenu3 epoyy uoneutjod mem sjoesut prosoqoud Duo piosoqoJd Buo EN sioəsu; posoqosduou jews EN ee^e|jeuo]ju / eneeq jnpy q unoujeo P s}oəsu; əƏejnqıpuew əßIe7 [7 uongulllod Buryons-pue-uound m yoesu| = epiexeu JejeAA Ald pua pul © — =a səpoW uongulllod mes mu py AJOALIEJDON * gis B yog lw ADeudou/Aed suonei2ossy DuipeeJ poejejex : @ 941493404, i z Im mn m "Fos UN Pus N moeg ing j 00L - NN no mon ma [d ® e > © ¿ oseug Uv P ^ x V , — š $65 THE o : E 7 4 A c * E š : Ë ; š š E 3 i ; E š è g $ š j sj, 829g [58 8 suuedso¡Bue sjuejd pees jeuBju | — seyAudouejiuoo (sey IN Se. = eee A Y OAE EN nf ne eee TREY | E E x B | E x x : : E L —Ç Volume 97, Number 4 Labandeira 473 Pollination of Mid Mesozoic Seed Plants Novokshonov, 1998; Novokshonov & Rasnitsyn, 2000), often with robust, asymmetric mandibles reminiscent of a mortar-and-pestle mechanism for crushing pollen (Schicha, 1967). In some instances, these lineages pre- served gut contents enriched in fossil pollen (Krassilov et ab. eee a De » em MEI kak the early - such as Ad Duae noptera: Jervis & Vilhelmsen, 2000), Micropterygidae and Agathiphagidae (Lepidoptera: Kristensen, 1997), era currently includes the greatest diversity of iar dim taxa (Samuelson, 1989), an expansion commencing during the Middle and Late Jurassic (Arnol'di et al., 1977; Hunt et al., 2007). Mandibulate, palynophagous insects process pollen in many ways. They may collect pollen and swallow the grains whole, as in anthophilous sawflies — 1961), beetles Pr a bees s & Peng, 1984), a ewings Picker, 1987; Popoy, 2002). e fossil ud may be found in contents and in dispersed coprolites (Willemstein, 1980; Caldas et al., 1989; Labandeira, 2006b). A variety of unique mouthpart modifications may accom- plish the d of — pollen grains, best documented i tles . 1985; Krenn et al., 2005). Such Rim ond: jutting, alas mouthparts, lacin with several types o hairs that didi gene. xi spoonlike or other an = ui DM or modifications Eo aned shaped concavities dada. 1967). Hairs ee coa- lesce to form brushes or combs that sweep and deliver pollen to the mouth (Nel & Scholtz, 1990). Mandibles are often extensively modified into laminar flaps that assist the collection and kneading of pollen into a consumable mass. Once in the intestinal tract, recent studies indicate that h as osmotic shock (Dobson & Peng, 1997) and chemical degradation by ip ass area cells Micka _ al., 1990) can oth oran EI bens: juiritiqpélly icd: ing protoplast contents, yet leaving grains that appear intact (Barker & Lehner, 1972; Baker & Baker, 1979). Similarly, ingestion of whole pollen grains through siphonate mouthparts has parallels in some fluid- feeding Diptera, such as Syrphidae (hover flies) and Bombyliidae (bee flies), ae in oud hake (nympha- lid butterflies) of the Le era (Holloway, 1976; Erhardt & Baker, 1990; ce & Krenn, 2000). These entire pollen grains are ingested either as a primary diet source or secondarily in a nectar diet. Nectar and pollen may be eS, by anthophilous insects more commonly t either. two food sources are complimentary and are red for insect nutritional balance (Gilbert, 1985; His 1989a; Roulston & Cane, 2000). The — seca is to use sena: mandib erains as or similar device. da we “hayo seen, this "x of palynovory is evident in the phylogenetically basalmost lineage of the Hymenoptera, xyelid sawflies, with a fossil record extending to the Middle Triassic (Rasnit- yn, 2002). Modern Xyelidae feed mostly on gymno- spermous, especially pinaceous pollen (Burdick, 1961), and their mandibles are highly asymmetrical and «— ; Fem L "TL. bosco at £ Ji st 1 E So 1: ght Seed plant li k t 51 feeding associa horizontal bars, defined in the center-right legend and keyed to the 20 (and other) fossil | kee, from fossil fructification structure, pollen size and surface bien ons -fron surviving eeiam. vun polliostion hop nutritional status and especially numerous studies of the š: da -r prp modes is based on evidence from deke 1 E three most common modes. Lineages with dashed segments indicate inferred presence, often L NS M Sox shown as thick vertical, colored ucl deben d up to the major extinction events. Small horizontal bars within the lineage columns indicate fossil evidence for em nectar, or both, presented for insect indicated consnmpltion Note th g di a. <4 Dew menie een i s mph: ized. S ] plant phyl ' J bal. MANR Esla Sula DO Andersen et al 2005; Burleigh et RI t KL £ 1 ] “< re ye F ü s al ocn. 1 QU lr 2009) C L G L d by a horizontal TRE band from 130 to 20 Ma. £41 EI ip OOK) HT! š in t al. (2008). Ovulate struct Coins id bo nri iM E por maar pansa N dar (2) Petrie lla triangulata ae (Tayar et al., 1994) Pula on Alvinia bohemica ne (Kralek, 2000) (Coniferales: Leptostrobus r Harris (Harris, — lat (sheni . 2007a; (4) Problematospermum ovale Tarot tor rama) bd Ñ T lb) (Czekanowskiaceae); (5) Carnoco a Mini 2009. Wang Lo ); (6) nites S b, EK @ Catonia sewardi Harris s (Harris, 1933) (Caytomiaceae); (8) Monimia -s TE. ¿M > s dE po X V (10) Paleorosa similk is (Ros ) = & Roth 11, 1993); md (11) Vanilla planifolia Andrews (Orchidaceae). Annals of the Missouri Botanical Garden Long roboscid Phases K-Pg 1 ERES P-Tr Both [zz Lepid. ,eepioBÁiejdojotN, [esajdooay sayo pepiyoAsdojainouy = ur Pe ES x < "v < > S | < e Meco. None [EE] Palynophagy Fe Minor EE ^ Nectarivory 3 Y ° s ° = € S — s & © a (see Fig. 1 for key) eJejdeuoudis eJneuou93 Diptera w = Š * ° E G a P | eudiouioÁuione ns ,BJeoojeuieu, Long Proboscid Pollination Mode Holometabola Neuroptera eepioiuouy| &ieydojeBejw eJeidoipiudes gəponKjəsso|o ZZ eJeidouesÁAu 1 N NN UN NN esajdiwaH = z A Paraneoptera “Polyneoptera” r E ho. HE|BEB s Ji £ Ë + — — Dy £ s$ asso Ss “< š f š 2 š 2 O Ë g g "+ ¿ š * x i š ul le 8 5 +] qu Š RE o m 9uoDoare Snoeotjar) = > 21OZON32 - v ueuueg —[uuechiddrssssr a e SIOZOS3N eo o z T 90203 Vd e o Volume 97, Number 4 2010 Labandeira 475 Pollination of Mid Mesozoic Seed Plants designed to crush pollen (Jervis & Vilhelmsen, 2000). The crushed pollen is further processed in a capacious oral cavity that is lined with modified teeth (Vilhelmsen, 1996). There are Triassic insect coprolites containing fragmented pollen within Triassic cycad cones vins et al., 2005). Late Paleozoic evidence for this feeding mechanism also includes dispersed coprolites with fragmented palynomorphs (ati 2006b) and some mn — Fe Permian insects with — jt niis 1977) iy have seda in i this way (Schicha, 1967). Another ho bolonsetsheloas ss and the Repudio, has early di Agathiphagidae, Hi bathmiidae, and rady the Early Jurassic-Early Cretaceous Eolepidopterygi- dae—with pollen-grinding mou (Hannemann, 1956; ii 1984, 199 7: Labandeira, 2009, pers. obs.). The basalmost extant lineage of Coleoptera, the archostematan Cupedidae (Hunt et al., 2007), processes pollen with similarly comminuting mouth- parts (Hórnschemeyer et al., 2002). Other groups of iones ah as 6 the Pose is or ENS 1990), E UE while iron such as ie Blattodea (Vlasáková et al., Aa are e commonly palynophagma hawt A but do not use pollen HAUSTELLATE MOUTHPARTS A second, distinctive, and more recently evolved group of mouthparts involves the modification of ancestral mandibulate mouthparts into the derived haustellate condition etiam 1990). This modifica merous times in insects and involved airidas qasin behavior common in the Hemiptera iptera, as well as surface fluid eeding in the major holometabolous lineages of Diptera, Lepidoptera, and Hymenoptera, and less commonly in Coleoptera and Trichoptera (Labandeira, 1997). The focus here is on external surface s which are the pre-eminent haustellate clades. Vari permutations of the labial, maxillary, and nei adjacent regions became modified into an elongated structure, s as a tubular proboscis or a labellum, r nonpene probing and imbibing of fluids (Ulmer, 1908. ort 1929; Takeuchi & Toku- naga, 1941; Eastham & Eassa, 1955; Holloway, 1976; Houston, 1983; Szucsich & Krenn, 2000; Krenn et al., 002, 2005; Borrell & Krenn, 2005). Piercer-and- suckers play a minor role; examples some dipterans where female individuals have a “dual role of puncturing integument for blood and surface feeding on nectar (Kneipert, 1980). In some haustellate mouthparts, the labral, maxil- lary, and labial structures variously nw to produce a siphon. The siphon may be composed of conjoined maxillary galeae, as in dinis glossate Lepidoptera and nemognathine Coleoptera, or sutured labial palps, without or with additional elements, as in the Diptera. In addition, the terminus of the siphon may bear cuticular structures such as ridged crests or —— ribbing, dense patches of hairs, special- setae, sponging . or even several slits ala to scooplike structures for efficient capillary Figure 2. Pollination modes of mid Mesozoic insect lineages, cys? le distribution of major insect pollinator types as etus eciam hes perm » legend. at t lower right. Insect lineages co co Me on evidence meres from mouthpart structure, gut contents, —— matching structure of nec nee associations as smaller Assignment of pollination pollen can on insect es, and eed plants ( n see Fig. 1). Each lineage id Fr 96 documented Í , up to the th t domi ( key in Fin. 1); rin imen pollination may b k x T. L 1 gn rae = eh ye ag ç = + I 1 LI I all horizon’ tal bars "Lu. L Be ge Ir š fl n Hestar or hoth p ly opte Is + Lake Tt sa: where n z zi c x 1 lepntine heec ai » 130 to Note e e presence of Pe rer Res of the | angiosperm radiation, indicated by : a ends deed horizontal rey from 90 ier provided f for e a Paleozoic and Cenozoic. Insect phylogeny is principally from Grimaldi and Engel (2005), a b: (2005a) for onmi acquired the condition i basal neuropteran); (2) Heterokal. (3) Ne Nemognatha sp- (Coleoptera: Meloidae, a modern — E (4) P. y); (5 ulcherrimus Ren (Di n Labandeira Diptera subclades, and Labandei Geochmnelogy : " left; is from Ogg et al. (2008). M a is apps on the LR el ira et al. (in [nie for Neuroptera subclades. M pedbuscid p ination bras gte A ns o a Pekan ?oblivius Vilesov Ram lihemerobius 'onius R strinidae, a tanglevein fly); (6) Protapiocera sp. (Diptera: en, Labandeira € Shih ychi — (1941). Ren (1998) L “asawa (2005a, pers. obs.), and Ren et al. (2009). 476 Annals of the Missouri Botanical Garden uptake of fluids and particulate pollen (Schremmer, 1961; Elzinga & Broce, 1986; Jervis et al., 1993; Faucheux, 1999; Krenn & Kristensen, 2000). Sipho- nate mouthparts are powered by a suction pump of a series of compressor muscles attached to chamber walls in the front of the head, often adjacent to the antennal bases (Eastham & Eassa, 1955; Ren et al., 2009). There may be a second salivary pump formed of region (Gouin, 1949; Zaka-ur-Rab, 1978; Eberhard & Krenn, 2003). Consequently, most siphonate mouthparts operate by a single or a double —À pea area en capillary or other means of fluid absorption at the proboscis lineages, two extinct lacewing lineages, wasps and is beetles, and caddisflies. A modification occurs in two modern lepidopteran lineages where the siphon cradles digestive enzymes for subsequent intake and digestion (Boggs et al., 1981; Eberhard et al., 2009). — RN pollen may Se — in — ME that. collect polls for delivery to the esophagus (Schicha, 1967). Assisting these movements is hydraulic protrusability of mouthparts and their retractability, powered by intrinsic musculature within "dmn denm " sd gens ee unte hathor add to the reach of the uoethparts: A added example of such a mouthpart mechanism is the labial- maxillary small parasitoid wasps and larger bees (levi & Vilhelmsen, 2000), which has been trans- formed into a distinctively concealed, nectar extraction apparatus that can be folded and collapsed when not in use by lever-based muscles (Gilbert & Jervis, 1998; Jervis, 1998). This tubular proboscis has originated many times among wasps and other hymenopteran taxa (Krenn et al., 2002), but the wealth of mouthpart diversity in these forms is beyond the scope of this contribution (see Jervis [1998] and Krenn et al. [2005] for brief reviews). Another — for — fluid T is we mO IO n) kmi region, e.g., the Aaltie, fcd labellum of flies (Peterson, 1916; Elzinga & Broce, 1986) and the haustorium of caddisflies (Crichton, 1957). The labellum consists of expansions of the labial ps that form a single, conjoined, sponging organ that is adpressed to surfaces for imbibing fluids; solid es may be liquefied by salivary enzymes (Graham-Smith, 1930; Szucsich & Krenn, 2000). The fly labellum consists of pseudotracheae, or small, linear channels that ramify into larger collecting tubules that move fluid to the proboscis food canal and ultimately to the esophagus (Bonhag, 1951; Elzinga & Broce, 1986; n & Krenn, 2000). Flies with labella are often nectarivorous (Kevan & Baker, 1983; Larson et al. 2001; Labandeira, 2005a). Structural analogs to the labellum occur among the pseudolabellae of extinct scorpionflies (Ren et al., 2009) and the haustorium of extant caddisflies (Crichton, 1957), which are used to imbibe surface fluids, presumably pollination drops and nectar, respectively. Sponging structures in these two groups lack true dipteran pseudotracheae, although 3. > + K LE ub. £ 4 c PIERCING AND SUCKING The Hemiptera, Thysanoptera (thrips), and many Diptera have invasive stylate mouthparts. These mouthparts penetrate plant and animal tissue. They generally ed ve a housed as two pairs of short to very long Ta one mandibular pair and an i o penetrate tissue. ae is considerable iatis of the number and arrange- ment of stylets. The ur bear two pgs pairs that are collectively ensheat whereas the Diptera frequently have an eect fifth fed stylet. By contrast, the asymmetrical mouthcone of the Thysanoptera contains three stylets and lacks the right mandibular stylet. Some piercer-and-suckers are blood feeders that target the capillary blood or subdermal lymph in vertebrates or consume the fluidized contents of small arthropod prey (Lehane, 1991). Alternatively, other piercer-and-suckers are phytophagous and con- sume mesophyll and cambial tissue protoplasts, sap oe phloem and xylem, petal or secretory tissues of wers, or contents d individual pollen grains Grac 1959; Weber, 1968; Lewis, 1974). Some mycophagous and feed on fungal tissues or individual vane (Lewis, 1974; Ananthakrishnan & James, 1983). A few Hemiptera, ao phyto- phagous bugs, are pollinators (Ishida et al., 2008). Thrips commonly are associated with on (Pellmyr et al., 1990; Totland, 1993; Momose et al., 1998; Jiirgens et al., 2000) and use the punch-and-suck grains (Grinfel’d, 1959; Kirk, 1984). This technique apparently was used by thysanopteran ancestors on Permian noeggerathialean spores (Wang et al., 2009) and evolved separately in some modem ceratopogonid midges of the Diptera (Billes, 1941; Downes, 1955). With the exception of thrips, piercing-and-sucking mouthparts are minimally important to pollination. THe PLANTS Several major seed plant clades with gymnosper- mous reproduction were probable sources of nutrition for diverse guilds of mid Mesozoic insects feeding on Volume 97, Number 4 2010 Labandeira 477 Pollination of Mid Mesozoic Seed Plants mos leonis Mamata, hisp'andiphewinia rhaps exposed anion of iun bisexual (hermaphro- deo strobili and cones, typical of cycads, bennettita- leans, and probably pentoxylaleans. Internal, mostly parenchymatic, tissues were consumed by She whereas external tissues, such as micropylar secretions p pelles drops naq pripale. ind pollen, provided mui benefit of Filliostita for the host plaito INSECT POLLINATORS Mid Miscieie plants, peng sycada,. Realia s being largely pollinsted. by — insects e ie 1972, 1974; Klavins et al., 5; Labandeira et al., 2007a). During the Early Ape a few ae of basal angiosperms with large, showy flowers undoubtedly were similarly pollinated (Gottsberger, 1988; Bemhardt, 20009. Faly men such as the Nymphaceoeae, gnoliacea leans. that mimicked m gymnosperms, being similar in gross morphology and thermogenic behavior (Dieringer implicated i these convergent associations were dominantly eiit that ranged an order of magni- tude in size (cf. Thien et al., 2009). The larvae consumed internal tissues while the adults ate accessible pollen probably associated s and vegetative tissues. Other mandibulate taxa, such as anthophilous Neuro tera, based on modern nemopterid pollinator biology (Popov, 2002), may have played a role as fluid or pollen feeders. Other vectors probably included Blattodea, Orthoptera, and Trichoptera (Porsch, 1958). Four major modifications of gymnospermous seed plants are associated with pollination predominantly by nsects. First is the evolutionary develop- mental compaction of unisexual ovulate and pollen compound, bisexual (hermaphroditic) idis didi et Ma me see S 2009. I pecht & Bartlett, or reviews) short-distance He by relatively A sedentary insects, uch as beetles, is easy. However, there is a potential Deo cost of inbreeding det me: mechanisms to enhance A second mediation & is establishment of a reward cycads, bennettitaleans, and presumably pentoxyla- leans — emphasized pollen, but only subordinately pollination drops (Tang, 1987a). This is inferred from studies of extinct and extant insect taxa responsible for damage of fertile strobilar tissues as well as the adult insect mouthpart structure of likely descendant or analog al., 1995; Schneider et al., 2002; Laban 2007a). However, there are some beetle pollinators that do not E feed on pollen but instead cover their bodies wi sumed grains, some of which result in delliniien: Donaldson, 1997). The nance of a pollen-based reward in these gymnosperms contrasts with the dominance of fluid-based rewards that provide highly mobile, occasionally hovering insects with carbohydrate rewards to provide calories uired for longer distances and powered flight (Haslett, 1989a; Wickers, 2002; Nepi et al., 2009). Third is protection of the ovulate part of the strobilus from the potentially destructive feeding domi- damage by mess-and-soil pollinators such as es. The closest gymnospermous analog to the E ovule of angiosperms is the cupule of TCayto: (Specht & Bartlett, 2009), if reduced to a ing ovuled structure. The inner wall of ovulate tissues is celtas separate from an outer wall form by t heisictitalodts, pibditiod from insects would be afforded to ovules by extraovular structures, including encompassing bracts, thickened microsporophyll tis- sue, interseminal scales, and/or timing changes such as the retardation or acceleration of pollen maturation and ovular receptivity (Crane & Herendeen, 2009). Distinct from the primary pollinator rewards (pollen, pollination drops, nectar) is a fourth type of plant-host specialization for mandibulate insects, specifically the production of decoy tissue. Decoy tissues deflect or deter pollinators from consumption of essential repro- i zs L 1 y 11 p sd receptacular tissue and interseminal scales may be decoy tissue Nue on eidem n et tunneling Crepet, 1972, ihe Labs et al, 20073) and p E ED (Nishida & Hayashi, 1996). Abundant receptacular tissue could have protected the reproduc- me organs a me spee of renee ee in Late manv of ewe have borings overwhelmingly in reproductively inessential tissues (Labandeira et al., 2007a). Some early angiosperm lineages with large flowers "e et al., 1999; Seymour & Matthews, 2006) favor use of vegetative tissues ostensibly to reduce “ew extent of damage to reproductive organs. Another decoy example is strobilar thermogenesis in cycads, attracting insects for mating and brood sites (Tang, 1987b; Roemer et al., 2005). Decoys were variably and independently elabo- tated in early angiosperms, culminating in modem Annals of the Missouri Botanical Garden insect-mimicking pseudocopulation in orchids (Paulus & Gack, 1990), i £ il agi Las igir cc E. the latest Cretaceous (Ramírez et al., 2007). J CYCADALES pondo probably kad. an hong during the Pennsyl- with vyvau foie (Mamay, 1976; Anderson et al., 2007; Taylor * etal., 2009). They evidently were pollinated by insects, based on circumstantial evidence structure, surrounding vegetative and other possible insect-reward tissues (Mamay, 1976; Taylor et al., 2009). More convincing documentation of palyno- phagy on a male cone comes from the Middle Triassic of Antarctica (Klavins et al., 2005), and reproductive features for the similarly aged TAnarcticycas, a member of the Cycadaceae, indicate insect pollination (Hermsen et al., 2009). Insects are involved in the pollination of the most plesiomorphic, extant cycad taxon, Cycas L. of the Cycadaceae (Ornduff, 1991; Yang et al, 1999; Kono & Tobe, 2007). Extant Zamiaceae and Stangeriaceae, whose earliest occur- rences are Jurassic, are obligately insect pollinated by a spectrum of beetle pollinators, such as Boganiidae, Erotylidae, Belidae, and Curculionidae (Norstog, 1987; Norstog & Fawcett, 1989; Crowson, 1991; Donaldson, 1992; Forster et al., 1994; Norstog et al., 1995; T. 1997. Wilson, — non a al, 209%; Oberprieler, 2004), and al hrips Cycadothri (Okajima, 2000; Mound & e 2001; Bee et al., 2005). It has been suggested that most of these associations are ancient and mid Mesozoic in origin. This inference is probably correct, as several beetle and thrips lineages have mid Mesozo ic body-fossil records (Arnol'di et al., 1977; Farrell, 1998; Gratschev « Zherikhin, 2003; Grimaldi et al., 2004) and all extant cycads are dioecious (Norstog, 1987). ermian cone ` sobyt BENNETTITALES The Bennettitales are a moderately diverse group of arborescent, Laurasian seed plants with cycadlike foliage and pachycaulous or perhaps woody stems, but with characteristic unisexual or bisexual strobili. The group consists of two morphologically distinctive and temporally disjunct clusters of assemblage contains several poorly known lineages occurring during the Middle and Late Triassic (Anisian-Rhaetian) that bear unisexual strobili but with the ovulate strobilus not typically differentiated into ovulate and interseminal scales (Pedersen et al., 1989; Anderson et al., 2007). Minimally overlapping with this assemblage are three, better known, family- level lineages ranging from the Late Triassic to Latg Cretaceous (Carnian-Campanian), comprising the Williamsoniellaceae, Williamsoniaceae, and Cyca- deoideaceae (Watson & Sincock, 1992). These taxa frequently possessed bisexual strobili with female portions differentiated into ovulate and interseminal (Crane Jurassic and Early Cretaceous floras, often co-existing with gnetaleans and later with angiosperms, and shows evidence for insect pollination, inferred to be mandibulate insect associates, particularly beetles. Networks of galleries traverse receptacular, micro- ass ell. and Peal tissues, med at the contact between ovulate and pilis organs (Crepet, 1974; Labandeira et al., Ta). Based on the structure, solid tissues. Also, this type of insect interaction is similar to that of extant cycads, where weevils consume strobilar tissues and effect pollination (Norstog et al., 1992, 1995). Presumably, there was enough migration of adult beetles among conspecific bennettitalean individuals to prevent inbreeding depression PENTOXYLALES The Pentoxylales, by some accounts, are closely related to bennettitaleans (Anderson et al., 2007) and A three-dimensionally preserved, silicified fructification bearing an arc of ca. 12 seeds embedded in fleshy tissue was described by Nishida and Hayashi (1996), which was assigned to the Pentoxylales, most likely a new lineage similar to +Pentoxylon (Bose et al., 1985). In this specimen was an Seen: peeved, reflexed larva enclosed in a li nal fleshy tissue, adjacent to seeds (Nishida & Hayashi, 1996). The larva was assigned to the Nitidulidae (sap "e a vie jua cid with Saiora (Gazit et al., 1982; Kirejtshuk 1997). PLANT FEATURES ASSOCIATED WITH HAUSTELLATE INSECT POLLINATORS In contrast to mid Mesozoic seed plant clades that bore com i wasipas. insects, other gymnosperm clades pos- sessed dioecious ovulate and pollen organs loosely arranged on branches. The ovulate organs of these plants provided nutrient-rich fluids as a reward for aerially mobile fluid-feeding insects, such as various long-proboscid taxa. These gymnosperms had in common insect-related modifications of the basic ÓN AAN cr t itt s mm Volume 97, Number 4 2010 Labandeira Pollination of Mid Mesozoic Seed Plants pollination drop system used extensively for wind pollination that currently is best demonstrated in e ancestral pollination mode i uu is wind pollination, wherein the distal an of an vule bore a short, tubular micropyle that became filled with secretory fluids originating from vacuole- laden, secretory tissue adjacent to the nucellus. reted pollination fluid fills the micropylar tube, forming a bubble, or drop, at the terminus to trap ng ambient pollen (Chesnoy, 1993; Takaso & Owens, coniers. 1996). This is followed by fluid resorption or evaporation ithdraw. e drop with trapped pollen to the nucellus where fertilization occurs en tube (Gelbart & von Aderkas, 2002). This condition has been demonstrated for late Paleozoic medullosan seed ferns (Rothwell, "iS and a variety of fossil fructifications that e been described with ovules bearing relatively ih adi flaring micropyles consistent with wind pollination. Modifications consistent with insect pollination are xe for the ui du im in several lineages of seed plants, based o structure and pollen types doc 1932; lei testa, 1973; s et al., 1990). This shift i li significant changes in plant morphology as E veli as mouthpart and presumably behavioral changes in co- occurring, haustellate insects. l. For Jurassic gymnosperm lineages, the micropyle came significantly lengthened and its inner diameter became wider to accommodate narrow- proboscis lengths extended to 15 mm or longer, approximately matched by micropylar lengths in certain species of the gnetalean TProblematosper- mum and some bennettitalean ovulate organs. 9. pS IA sus E e £ ` cupulat structures that connected deeply hidden micropyles to surface orifices by tubular structures that ranged in length from ca. 3 to 15 mm. These tubes were surrounded often by fleshy tissues, " with an outer sclerified layer (Ren e ) These tubular structures bore surface aie points— salpinx tubules, integumental tubes, catchment funnels, tubuli, elongate m are not homologous but represented c nt solutions for accessing — seen ; fluids by long- proboscid insects (Labandeira et al., 2007a; Ren et al., 2009). Shorter dicke i structures would afford access to W and other insects, similar o the pollin fluid feeders on modern gne da ak 1914; van der Pijl, 1953; Bino et al., 1984a, b; Marsh, 1987; Carafa et al., 1992; Kato et al., 1995; Wetsching & Depisch, 1999). . Studies of the nutritional value of insect-consumed secretions occurring in present-day plants, includ- ing extranuptial nectary secretions in pollination drops in gymnosperms, and nectar and nectarlike secretions in basal angiosperms, suggest a third modification (Pacini et al., 2003; Nepi et al., 2009). Fern nectaries produce watery, nutritionally poor secretions, whereas carbohy- drate acid concentrations of pollen drops from the four major lineages of gymno- e Ginkgo L., cycads, and gneta- eans—show gnificantly more elevated nutri- tional levels, bérteddiciy š in the two latter insect- pollinated clades (Labandeira et al, 20073). Nutritional levéls in pollination drops of the four gymnosperm clades are similar to those of nectar from basal angiosperm lineages ee et al., 2007a; Wagner et al., 2007; Nepi et al., Lipid levels were not measured. Pollen i» associated with wind pollination may be exaptation (Gould & Vrba, 1982), being eid y insects that used the resource for an alternative feeding function, as high levels of carbohydrates and amino acids are important for sustaining the high levels of inctabulit activity for highly mobile, winged € (Baker & Baker, 1983; Gottsberger et rhardt & Baker, 1990; Tang, 1997; Wiickers, pe 4. Studies of modern pollen indicate that characters consistent throughout the palynological fossil record. Most obvious is size. Pollen larger than ca. £ i maximum diameter tend to be insect vectored, and almost obligately so for larger-diametered taxa (Whitehead, 1969). Pollen shape also is significant; insect-pollinated grains typically lack bladders or sacci and frequently are spheroidal to ellipsoidal in shape (Ackerman, 2000). Related is the functional unit of transmission, in which the individual grain often is not the transported unit, but rather a larger llen aggregaie,. Halen % me Soir ope laca — + £ 3 1 £C. t, 1980); this increases elective diameter during transporta- 2 as = various types of ee caused by ich as viscin cok or pollenkitt (Nixon & tock "1993: Zetter & Hesse, 1996; Hu et al., pose A pollinium is another way of bundling o ing grains to achieve an efficient Ghent size. Pollinia are nown in several angiosperm lineages, such as orchids (Micheneau et al., 2009), but do not occur in gymnosperms. Similarly, certain surface orna- mentation and exine ultrastructure indicate ento- mophily in modern angiosperms (Osborn et al., Annals of the Missouri Botanical Garden 1991a; Hesse, 2000) and in fossil gnetophytes where taeniate pollen preferentially occur in — — guts PA: et al, 2001). 5. Th mous seed plants tends to emphasize outcrossing. or are X hermaphroditic, with male and female monax into a single, 171 m das E Hital ee or iue angiosperm flowers. CORYSTOSPERMALES The AS ding a Loe Tie od aaa bui cnitiiéd ing through- out the Triassic, a diverse Gondwanan assemblage of arborescent, wind-pollinated plants bearing t Umkoma- sia ovulate organs, t Pteruchus pollen organs, t Rheoxylon trunks and branches, and tDicroidium foliage (Retallack & Dilcher, 1988; Anderson et al., 2007). However, two ba £ 1 shed. rare hahi +, A from the Late Triassic Molteno Formation contain considerably elongated micropylar extensions that suggest insect pollination (Labandeira, 2008, pers. obs.). Depending on the species, Pteruchus pollen organs produce tAlisporites-type, tPteruchipollenites, or *Fal- cisporites pollen. These grains can be large, some ranging from 88 to 115 pm in maximum length (Taylor € Taylor, T or Em oe rnm et al., 1995), t other than wind. Nevertheless, piled smaller pollen sizes were documented for bisaccate }Alisporites neri de Jersey, affiliated with TUmkomasia granulata Thomas (Retallack & Dilcher, 1988), supporting iid pollina- tion, undoubtedly the norm for the group. PENTOXYLALES Pentoxylales were first described from India (Sahni, 1948), based on Pentoxylon, an anatomically distinc- tive trunk form-genus that ranged from late Early Gondwanan distribution. The best-known, whole-plant pentoxylalean is a shrub, with affiliated Pentoxylon stems, tNipaniophyllum foliage, tCarnoconites ovu- late organs, tSahnia pollen organs, and monocolpate pollen often affiliated with some TC ycadopites species, which were 17-22 um long (Bose et al., 1985; Osborn et al., 1991b). "and of ovules breaching the surface of conelike organs are very short, from 1 to 3 um deep, presumably requiring the smallest of long- proboscid or small nonproboscid insects for pollina- tion. Pollen drops would have been a reward in lieu of pollen, which could have been wind dispersed, suggesting ambiphilous pollination. CZEKANOWSKIALES As members of a broad ginkgoopsid alliance, Cankanqiakinkka, of "m bepispobecene i is one of I Late Triassic Rhaetian to the earliest Lath Cioni Cenomanian of Eurasia and North America. The form genus TLepto- strobus, of unknown growth habit, consists of TCzeka- nowskia foliage, TIxostrobus pollen organs, and Lepto- Cycadopites species (Harris, 1951b; Anderson et al., 2007). The ovules are bivalved and apparently had a hard exterior, with ovules anatropously positioned such that ovule anceps were directed simia furis 205 1b; OW ot Te * 1 2009) iint channel, between the Loustolos backwardly directed ovular micropyles that bore pollen drops and the terminal slit or aperture, was ca. 4—7 mm, depending on the species. The presence of pollen drops is inferred from micropylar structure and presence in Ginkgo (Dogra, 1964). This short T probably represents an independent, seemi nique, innovation for accessing plant pollen dm be fluid-feeding, long- proboscid insects. CHEIROLEPIDIACEAE Cheirolepidiaceous conifers were a dominant seed plant clade during the Late Jurassic and Early Cretaceous, although they have their origin probably h 007). A well known, Early Cretaceous, European member of Cheirolepidiaceae is the arborescent whole-plant TAlvinia bohemica Kvatéek, whose namesake is based on the ovulate cone. Alvinia bohemica is affiliated with the conspecific, smaller pollen cone, tF; renelopsis alata (Feistmantel) Knobloch, which produced distinctive Classopollis pollen, both of which are associated with Sad that is also known as A. bohemica (Kvacek, - The ovulate scales on the cone of A. bohemica are one of the most complicated female reproductive structures known in seed plants (Labandeira et al., “ie pes scale has ca. 10 — Med some of Cüneo, pers. comm., April 2 while on the adazidi t les, one of which i 1$ usually aborted, “hoe Moppi i are ben Mee ally Open Volume 97, Number 4 2010 Labandeira Pollination of Mid Mesozoic Seed Plants surrounded by conspicuous lobate processes, is a funnel-shaped structure oriented lengthwise within the scale. th apert E r 1: A d by ong, unicellular trichomes that decrease in abundance as the gullet of the funnel narrows. Lining the narrowed el base are thickened, squat, multicellular, nectary-like glands that probably were secretory in nature. At the very base of the funnel, where the nectary-like structures end, there is an opening where the funnel merges into a linear, tubular extension or a pipe (Kvacek, 2000). This pipe traverses the rest of the inner tissue of the ovulate scale to end at the adaxial aspect of the scale, immediately adjacent and almost f m eer of the ee, UP ovule. long, somewhat ge cl p the n pipe p abaxial to adaxial pyle complex is a n for insect pd Two types od pollinator ported ss winged. m hovering insects able i insert a long tubular siphon and imbibe a nectarlike secretory reward, or considerably more diminutive insects that could have walked into the funnel and a probe the trichome- and nectary-lined wall for Labandeira et al., 2007a). In either case, Classopóllis pollen would have been deposited at the base of the funnel, near the entrance to the pipe, which would have served as a conduit for the pollen tubes to the short micropyle. Given this hypothesis, the funnel, perhaps visually by colorful external lobes, can be considered an inverted stigma with nectarial secretory rewards (Kvacek, 2000). The Classopollis- bearing pollen organ would have provided a reward as well, perhaps the pollen itself, or alternatively a £d 1 IL 1 + ht srl CU ClU1y Í J to those of the ovulate organ. GNETALES Gnetales were a diverse group that originated in the mid Triassic, were present in many Jurassic floras, and experienced a radiation during the Early Cretaceous, largely synchronous with that of angiosperms. Modern gnetaleans consist of three disparate lineages that represent a reduction of major morphologies compared to the diversity found during the Early Cretaceous Creme, 1656). With pissibie exceptions in Ephedra- ceae, 1 (Bi tal b Me et ss aon Wetsching & Depisch, To n Weluitichin Hook. f. (Welwitschia- Sm and Gnetum L. (Gnetaceae)—are a broad array of “akapa or nonproboseid insects, pre- flies, moths, and wasps, but also incon- spicuous beetles with mandibulate mouthparts, as well as thrips vith modified pioch end ank mouien: Modern reward- ing gnetalean pallizatitio drops (Porsch, 1910; Meeuse, 1978; Carafa et al., 1992; Kato & Inoue, 1994) an often Pts se Priksa ps take up surface fluids fro gi ny of the tinet ] ta rides i esie. edt ogy siiri to the three extant lineages are mo island to have been similarly pollinated by small-winged insects (Lloyd & Wells, 1992). However, a few ovules, such as Problematospermum (Sun et al., 2001), bore exception- ally long micropyles (pappus tubes) extending from an achene base surro unded by a tuft of bracteate papery scales or tufts of feathery hairs (Krassilov, 2009), analogous to that of modern Asteraceae (Taylor et al., 2009), and appear to be an adaptation to insect pollinators with long, narrow proboscises. The encir- cling appendages may have served as a pollinator lure. CAYTONIALES Caytoniales comprise a few genera of which — originally described from the early Middle c of Yorkshire, United Kingdom (Harris, 1933, 1940, 1957; Anderson et al., 2007), is best known urasian in distribution ie ian) to the . They are pre- or trees. ‘es. The lineage may be closely related or is the sister group to an (Crane, 1985; Doyle, 2008). The most notable specimens of Caytonia range from the lowermost Cretaceous (Berri sumed to be woody shrubs are ovulate organs from Bajocian to Bathonian in the Middle Jurassic of Yorkshire and are affiliated with distinctive *Sagen- opteris Presl foliage, TCaytonianthus pollen organs, +Amphorispermum dispersed seeds, and 1 Vitreisporites pollen (Harris, 1951a, 1957; Zavada & Crepet, 1986; Retallack & Dilcher, 1988; Ren et al., 2009). Th re an erect, thick, and edil fleshy recurved cupule that had several downwardly oriented seeds attached to placentation along the upper cupulate region. Each short micropyle ended in a tubule within the cupulate tissue that terminated in a surface opening under a distinctive lip adjacent to the subtending peduncle. The most intriguing ana- tomical feature of Caytonia are these tubular connections between the micropylar pollination drops and the lower lip, which are diachronously deployed, one at a time as each ovule reached maturation within the infructescence. The length of these integumental tubules ranges approximately from 2 to 6 mm and is consistent with similar measurements for the siphonal lengths of co-occurring long-proboscid insects (Ren et al., 2009). Annals of the Missouri Botanical Garden MODES VERSUS SYNDROMES The notion of pollination syndromes was estab- lished early in pollination ecology, but recently has been challenged (Ollerton, 1996; Waser et al., 1996; Fenster et al., 2004). As originally defined, with subsequent modification, a pollination syndrome consists of a group of functionally related floral characters and behaviors that collectively are con- sistent with pollination by a similarly distinctive functi taxonomic group of animals t ave convergent feeding strategies, functionally similar mouthpart types or foraging behaviors that access floral rewards in the same way. Floral rewards typically are nectar and pollen, but also include oils, resins, mating sites, warm resting places, and other less obvious attributes (Baker & Baker, 1979; Pellmyr & Thien, 1986; Haslett, 1989a; Thien et al., 1990; Bergstróm et al., 1991; Donaldson, 1992; Lopes & Machado, 1998; Azuma et al., 1999: Jürgens et al., 2000; Frame, 2003; Seymour & Matthews, 2006). Recently, the traditional notion of pollination syndromes, e.g., beetle-pollinated flowers (canthar- ophily), small fly-pollinated flowers (myiophily), and bee-pollinated flowers (melittophily), has been shown s k. x J^ I 1: ] į Poe es animals. They also were inconsistent with the ista of the pollinated flowers themselves when attributes of the animal pollinators were taken as predictable variables (see Ollerton et al., 2009, for an example). Such examinations frequently indicated that the suite ted h du £ = ] 11; t CHL of nharant JH lat Or t 4 SE FE was not bome out by post hoc confirmatory tests. Because the idea of a pollination syndrome has not been wed. and thos... E LI x £ s overwhelming generalization over specialization in pollinator or pollinated clade. A Brier History or Earuer POLLINATION- RELATED FEEDING proteins, and other substances sufficient for nutri- tional sustenance (Labandeira, 2000). PALYNOPHAGY The earliest palynophagy occurred during the latest Silurian and Early Devonian Periods and is repre- sented by coprolites containing either a single kind of plant spore or compositionally heterogeneous types of sporangial and vegetative tissues (Edwards et al., 1996). These coprolite assemblages indicate the targeting of early land-plant hosts by microarthropods, occasionally suggesting specialization on a single host (Edwards et al., 1996; Labandeira, 1998). The culprits were microarthropods, particularly wingless, phyloge- netically basal, hexa clades. Isolated reports of spore-bearing coprolites continue through the later Devonian and into the Mississippian, but palynophagy dramatically increased during the Pennsylvanian of Euramerica. Two lineages of insects, in particular the major extinct clade Palaeodictyopteroidea, included taxa that used modified piercing-and-sucking beaks for consumption of spores (Labandeira, 2006b). Also, distant mandibulate ancestors of Orthoptera (grass- hoppers and crickets) consumed spores and sporan- gial tissues. Evidence for palynophagy from both insect groups is based on mouthpart structure, gut contents, permineralized coprolites, and feeding damage to spore-bearing plants in coal balls and compression deposits (Labandeira, 1998, 006b). The spectrum of palynivores increased significantly during the Permian. The evidence is mostly d on part morphology consistent with pollen feeding (Rasnitsyn, 1977; Novokshonov, 1998), but also from fossil macerations of insect gut contents from Chekarda, Russia, that reveal an eclectic breadth of consumed pollen types (Krassilov et al., 2007). A broad representation of Permian insect lineages—the Gryllo- blattodea (rock crawlers), Psocoptera (booklice), ex- tinct Miomoptera, stem Hemipteroidea, and probably early thrips—were feeding on a diverse assortment of prepollen and pollen from host plants such as noeggerathialeans (tDiscinispora), cordaites (tFlori- nites), glossopterids (tProtohaploxypinus), medullosans (tPotoniesporites), early conifers (tLunatisporites), and gnetophytes (FVittatina) (Rasnitsyn & Krassilov, 1996; Krassilov et al., 2007 ; Wang et al., 2009 After the end-Permian extinction interval, the record of palynophagy resumes and expands toward the end of the Triassic and the Early Jurassic. During this interval, the emergence of modern lineages with known feeding habits occurs in both larvae and adults. During the Triassic and into the Jurassic, early ibulate lineag ly ptera, Coleoptera, Lepidoptera, and perhaps other holometabolous orders were likely palynophagous, colonizing cycadalean, Poner, pentoxylalean, and undoubtedly other plant Volume 97, Number 4 Labandeira Pollination of Mid Mesozoic Seed Plants NECTARIVORY The early fossil record of feeding on the external surface fluids of plants is E and appears later than palynophagy, probably beginning during the Late aan: me "nue Ae in contrast to pollen, i tent far fluid oh is more et a and ‘ies on reproductive morphologies of potential host plants and on the distinctive mouthparts of insects associated with nonpenetrative fluid feeding. The Pennsylvanian to Permian record for nectarivory suggests that the Palaeodictyopteroidea may have extended its sap- feeding mode of puncturing tissues to probing fructifications for access to fide secreted in deep Lx SET + T ; ee + {Th 2E 2002?) Additional evidence is provided by insects with specialized mandibulate mouthparts that could access san Pas produced Ht. sory hichanes, and much , evidence and weenie organs (Mamay, 1976; Taylor & ee Krings & Kerp, 1999; Labandeira, 2000). pem such Aegre products might ps antiberbi: might be seen as simply dee metabolic byproducts. om: is y small insects during the Permian. One late Early Pa neuropteran insect, from the Ural Mountains of Chekarda, Russia (Vilesov, 1995), had a distinctively extended siphonate proboscis consistent with flui ede but only had a reach of approximately 2 mm. arly Triassic to Early Jurassic, there is — evidence for insect fluid feeding tnn pollination. This comes mostly from seed plan reproductive structures rather than insect “massa (Labandeira, pers. obs.). Seed-fern taxa of this interval typically had a pollination-drop system for capture of but this could have been hening and widening of the internal rs of micropyles to attract long- probeacid necia as more dien. venim. The only evidence for siphonate mout "nd distinctive, oe insect sienta compress its from the Eurasian Middle E continuing into the Late Jurassic and into the late Early Cretaceous (Ren et al., 2009). PoLLINATION MopEs DURING THE MIDDLE JURASSIC TO Mip CRETACEOUS Figures 1 and 2 depict the global Mesozoic distribution of nine pollination modes and the related lati and nectarivory. Both plant-host (Fig. 1) and insect-pollinator (Fig. 2) perspectives are provided, with vertical patterns indicating the temporal duration of major pollination 4 ES ER E E i£ related feeding associations from major compression and amber localities. An emphasis is placed on the long-proboscid pollination mode and convergences in ovulate anatomy and coordinate — structure, unlike the predominant evidence o late insects that heretofore has sliced the fossil en major pollination modes are discussed. PUNCH-AND-SUCKING POLLINATION in certain cycad genera of Australia (Terry et al., 2004, 2005; also see Okajima, 2000) has spurred interest in finding related, cycad-specific taxa in the fossil record. The finding of TCycadothrips chadwicki Mound (Aeolo- thripidae: — and other related new species on modem cycads and in late Early Cretaceous Burmese amber (Mound, 1991; Grimaldi et al., 2004), indicates that this distinctive association extends to the mid Mesozoic. wa some e" v— — surpassed only by beetles (Terry et al. , 2005). Thrips also are common piens on pei sings attribut- able to their ig petal tissues and T polen grains by their distimetivé punch-and-suck feeding technique in extracting prot plasts (Grinfel'd, Mox Kirk, 1984). In modern ied thrips rarely exceed 4 mm in length and are frequently abundant in a wide variety of flowers (Momose et al., 1998; Williams et al., 2001). LARGE MANDIBULATE INSECTS The fossil history of large, externally feeding, mandibulate insects that are inferred as pollinators consists of insect lineages that have gut contents of o or certain pollen types on their head an thpart surfaces. These indicators of palynovory or S e often provide evidence for identifying both the insect consumer and the consumed host plant. Nevertheless, demonstration of palynovory is insuffi- cient for identifying a pollination mutualism. With the exception of the Coleoptera, large mandibulate insects currently are minor pollinators, and consist of the Blattodea (cockroaches), Orthoptera (katydids and crickets), Phasmatodea (stick and leaf insects), and — (caddisflies) (Porsch, 1958; Proctor et al., 1996). Mandibulate insects disproportionately char- acterize the fossil record of pollination when com- pared to evidence for haustellate forms, such as long- proboscid insects. Even so, they probably had greater participation in past palynovory and nectarivory than nt descendant their curre lineages would indicate. Annals of the Missouri Botanical Garden Modern Blattodea have been implicated in gener- alist pollination of angiosperms in the tropics (Billes, 1941; Proctor et al., 1996), although there are few specific cases of pollinator function. Examples include an undescribed species of Hemithyrsocera, an undetermined genus (both Blatellidae) on Uvaria elmeri Merr. (Annonaceae) from Sarawak, Malaysia (Nagamitsu & Inoue, 1997), Paratropes bilunata Saussure & Zehntner (Blattidae) on Dendropanax arboreus L. (Araliaceae) from Costa Rica (Perry, 1978), and Amazonina platystylata Hebard (Blatelli- dae) on Clusia L. sp. indet. aff. sellowiana (Clusia- ceae) from French Guiana (Vlasáková et al., 2008). Blattodea would be prime candidates for large- ibulate insect pollinators for the mid Mesozoic. Unlike the Blattodea, there is a fossil record of palynophagy that indicates katydids (Orthoptera) as pollinators during the Late Jurassic. Several species of the Haglidae, such as TAboilus amplus Gorochov, from the Karatau shales in Kazakhstan (Doludenko & Orlovskaya, 1976; Krassilov et al., 1997a), were umented as having Classopollis and other pollen types in their guts. Modern Haglidae apparently are not p HN: ; however, E A pt DA implicated in recent pollination (Grinfel'd, 1957; Schuster, 1974), including the related katydid lineage Tettigoniidae. The tettigoniid Anthophiloptera dryas Rentz & Clyne is a pollen and nectar feeder on Angophora floribunda (Sm.) Sweet (Myrtaceae) in eastern Australia (Rentz & Clyne, 1983). A more spectacular example is the Madagascan orchid Angraecum cadetii Bosser, which is pollinated by an unidentified, spinose cricket of the Gryllacrididae (Micheneau et al., 2009). There are no records of modern walkingsticks or leef insects f ds t ) pollen or acti as pollinators. However, there is a fossil i dean, tPhasmomimoides minutus Gorochov (Susma- niidae), from the Late Jurassic of Karatau that may have been palynophagous. Its diet contained princi- pally Classopollis pollen, but also a significant amount of foliar material from the same host plant (Krassiloy & Rasnitsyn, 1998). It is unclear if the species was a generalist feeder on varied tissues of a cheirolepidiac- eous host, or whether it was incidentally including conspecific pollen as a specialist folivore. The Trichoptera have long been known to be occasional nectarivores (Porsch, 1958; Nozaki & Shimada, 1997), with fluid being taken up by sponging of the Diptera (Crichton, 1957). Nevertheless, their importance in pollination is limited, consisting occurrences, Stenophylax permistus 3 Lachlan (Rhyacophilidae) can be a common cae the herb Adoxa moschatellina L. (Adoxaceae) in the United Kingdom (Holmes, 2005). Tinodes waeneri L. (Psychomyiidae) nectars various apiaceous plants in the United Kingdom (Petersson & Hasselrot, 1994), and Nothopsyche ruficollis Ulmer (Limnephilidae) is re- warded on a variety of herbaceous hosts in Japan (Nozaki & Shimada, 1997). These occurrences indicate opportunistic pollination. Overwhelmingly, the most diverse group of large mandibulate pollinators is Coleoptera. Pollen and nectar consumption, as well as pollination mutual- isms, have originated numerous times within the order (Crowson, 1981), particularly within lineages of the Polyphaga, such as the Elateridae (click beetles), Buprestidae (metallic wood-boring beetles), Cleridae (checkered beetles), Nitidulidae (sap beetles), Mor- dellidae (tumbling flower beetles), Oedemeridae (false blister beetles), Meloidae (blister beetles), Scarabae- idae (scarabs), Cerambycidae (longhorn beetles), and Chrysomelidae (leaf beetles). Some of these are known from fossils, and cladistic evidence suggests that they extend to the Middle and Late Jurassic, or earlier (Arnol'di et al., 1977; Farrell, 1998; Zhang, 2005; Hunt et al, 2007). This assemblage of palynivores, and subordinately nectarivores, that currently polli- nate large, showy flowers once was considered the ancestral syndrome for angiosperm pollination (Diels, 1916), later elaborated by Grinfel'd (1975) and Gottsberger (1989). Studies of the pollination biology within the Nymphaeaceae (Capperino & Schneider, 1985; Williamson & Schneider, 1994; Hirthe & Porembski, 2003; Seymour & Matthews, 2006), Calycanthaceae (Crepet et al., 2005), Magnoliaceae (Azuma et al, 1999: Dieringer et al., 1999), and Annonaceae (Gottsberger, 1989) all implicate these taxa and others with similar floral features in the attraction of larger-sized beetle pollinators—the cantharophily syndrome (Proctor et al., 1996). Spe- cializations for this type of pollen feeding include maxillary pollen brushes (Fuchs, 1974) and modified mandibular teeth (Grinfel'd, 1975), which should be retrievable from fossils, or perhaps digestive enzymes (Johnson & Nicholson, 2001). ADULT BEETLES WITH LARVAE IN INTERNAL PLANT TISSUES In some Mesozoic fossils, the internal tissues of large ovulate or bisexual organs occasionally contain analogs of these tunnel networks are associated with conspecific adult beetles that are pollinators of the same host plants (Norstog et al., 1992, 1995). As fossils, these networks most commonly occur in bennettitaleans (Crepet, 1974; Labandeira et al., 2007a). Limited destruction of ovulate and pollen Volume 97, Number 4 2010 Labandeira Pollination of Mid Mesozoic Seed Plants organs is indicated by tunneling in bisexual bennetti- talean strobili and in modem cycads, whereby vegetative and some seed me phytic ti sacrificed as a reward to larvae of the adult pollinators. Beetles responsible for these tunneling networks in modern unisexual cycad cones typically are Curculionidae (common weevils), although other related beetle pollinator taxa such as the Belidae (cycad weevils), Nemonychidae (pine flower snout weevils), and, more distantly, Aulacoscledidae and estelar (pleasing fungua beetles), could have -— Similar evidence for an endophytic, paly- agous beetle association occurs in a Middle Tisa eycad, TDelmaya spinulosa, described by Klavins and colleagues (2005), containing conspecific are pokin into P iia GO jio Meca il Hei PEDT contaid a un bean à in the inter- seminal parenchyma of a fleshy fructification (Nishida & Hayashi, 1996), indicating a conspecific adult pollinator. Endophytic beetle borings are common throughout the Late Triassic to Early Cretaceous, involving vegetative and frequently woody tissues of conifers and extinct seed-ferns (Labandeira, 2006a), suggesting pollination by medium-sized adult beetles. SMALL NONPROBOSCID INSECTS Small nonproboscid insects of approximately 3— 8 mm in total body length, minus appendages, have frequently been cited as the type of insect associated with the earliest flowering plant lineages. Most early angiosperm flowers were comparatively small in size (Dilcher, 1995; Crepet, 2008; Taylor et al., 2009 Thien et al., 2009) and may have developed from a preangiospermous ancestor possessing an ovulate we longitudinal slit with access to pseudostigmatic secretions Me 2010). This model is consistent with small, roboscid, fluid-feeding insects as the earliest cou of small-flowered, dull- colored, unscented angiosperms. This hypothesis contrasts strongly with the idea that large mandib- ulate insects (discussed above) were the insect native options, as both floral types probably reflect early angiosperm history. Nevertheless, small, non- proboscid insects apparently were more abundan and diverse in the initial pollinator angiosperms than the less diverse, large ma beetles (Thien, 1980; Thien et al., 2009). The major players of the small nonproboscid insect assemblage were flies (Diptera), representatives of which spanned ire order during the Early e of ndibulate Cretaceous, excluding derived cyclorrhaphous lineag- es that evolved later (Grimaldi & Cumming, 1999). An tional group was diverse, small, parasitoid wasps, a underwent a radiation during the Jurassic (Labandeira, 2002b; Rasnitsyn, 2002) and may have fed on gymnosperm pollination drops and subsequent- ly shifted to angiosperm nectar. Monotrysian and early ditrysian moths evolved during the Early Cretaceous eira et al., 1994; Grimaldi € Engel, 2005) and relatively short proboscises compared to those of later lepidopterans; extant members are pollinators on a variety of angiosperms (e.g., Kawakita & Kato, 2004). Another nonproboscid element was small beetles; several lineages were considerably smaller than large Gà 3-5 s owe eR 1. dz 4 above. Amid this diverse assortment of nectar-feeding, small nonproboscid insects were perhaps pollinators of extinct seed "ue eh as Clita mi inte, few millimeters, ie dad, to pa Gnetales that are pollinated by similarly small insects ENTRAPMENT POLLINATION Originating several times within angiosperms and possibly other seed plants is the entrapment of insects riod of time while the plant host is ed by their receptive to pollination, follow for a crucial release (Proctor et al., 1996). Lures and rewards enticing insect visitation include heat from host thermogenesis (Roemer et 2005), T of mating sites (Petersson & Hacen 1994), aroma produced by volatile compounds (Bergstróm et 4.1 1991), as well as the typical rewards of pollen and nectar. Entrapment is accomplished by a fascinating array of recurved trichomes at entry sites, initially allowing one-way es for an exit, or clos flexibly hinged lids. These modifications to floral structure occur in several basal angiosperm lineages, ment pollination represent been present at least since the latest Early Cretaceous (Ervik & Knudsen, 2003; Gandolfo et al., 2004). OIL AND RESIN POLLINATION The use of plant oils and resins as a reward extends to the Turonian of the early Late Cretaceous (Crepet & Nixon, 1998). This is based on specialized floral features of clusiaceous plant fossils from New Jersey, consistent with known floral biology of extant Brazilian Clusiaceae pollinated by euglossine bees (Lopes & Machado, 1998). This association may have Annals of the Missouri Botanical Garden occurred earlier, as there is now evidence that bees extend to the latest Early Cretaceous (ca. 105 Ma) based on tMelittosphex burmensis Poinar & Danforth (2006), a small but non-oil-collecting specimen. Mip Mesozoic Lonc-proposcip INSECTS AND THEIR SEED Piant Hosts The oldest studies of the pollination of modern flowers by long-proboscid insects involved morphological descriptions of pollinator mouthpart and head structure, and of receptive floral morphologies in pollinated plants (Heddergott, 1938; Takeuchi & Tokunaga, 1941; Schneider & Jeter, 1982; Zetter & Keri, 1987). Such studies historically have been done separately by entomologists and botanists and involved characterizations of insect mouthpart and plant floral structure without inference of function. More recently, there have been investi- gations of how insect feeding mechanisms work Examples include capillary fluid uptake at the terminal proboscis, fluid food transport through the proboscis and the effects of possible pollen inclusion, the — and valyular Sen ii tinge donhi, e or or is hese, and. ancillary structures that ai in the detection, uptake, and subsequent processing of food, such as palps, setae, and mechanosensillae and chemosensillae (Graham-Smith, 1930; Barth, 1985; Proctor et al, 1996; Faucheux, 1999: Szucsich & Krenn, 2000; Borrell & Krenn, 2005). Similar analyses were made for floral structure and function, including receptivity to and physiological responses from insect pollination (Szucsich & Krenn, 2000; Ollerton & Liede, 2003). Also addressed has been the allocation of i insect pollinator and plant host resources of pollinator feeding and host-plant receptivity, pollination efficiency indices, detection of host-plant morpholo; tionary of variously loose to iconically tight plant-pollinator relationships in time and space; for example, the study of how coevolutionary rela- 2005) or species (Armbruster & Baldwi 1998) levels. Finally, there is the didana d ) pollination in the insect and for insect pollination has been known in prominent Cenozoic pnt once, 1913; Bequaert & Carpenter, 1936), an understanding of Mesozoic insect pollination in seed plants has been developed only recently and remains poorly known. It is this last aspect—the early evolution of the pollination of plants, particularly by long-proboscid insects with siphonate mouthparts—that I will dwell on for the rest of this ek ese recent investigations involve modern clades of adult holometabolous insects and their angiosperm hosts (but see Terry, 2001), both of which experienced major turnover events during the mid Cretaceous to Paleogene. For plants, many clades originated uring or soon after a mid Cretaceous evolutionary turnover (Fig. 1; Niklas et al., 1985; Wing & Boucher, 1998). In insects, there was a major, earlier turnover in insect clades with the Permian-Triassic extinction, resulting in the origin of early, plesiomorphic representatives of modern clades during the earlier Mesozoic, in turn succeeded by more derived lineages that appeared later in the mid Cretaceous (Fig. 2; Grimaldi & Engel, 2005). This latter event is partly identified by a slackening of family-level insect diversification ( deira & Sepkoski, 1993) that corresponded temporally to the shift in potential host plants from gymnosperms to angiosperms for this global turnover is reflected by increased insect origination rates and, to a lesser extent, increased extinction rates demonstrated in family-level diversity studies (Labandeira & Sepkoski, 1993; Jarzembowski & Ross, 1996; Dmitriev & Ponomarenko, 2002; n 2005b), as well as saturation of mouthpart parity (Labandeira, 1997). In this context, Sepkoski ie Kendrick (1993) have used model-based analyses to validate the use of taxic diversity data and methodology for understanding major macroevolution- ary patterns (e.g., Crepet & Niklas, 2009). There is an approximate 90-mllioa-year overlap between these two intervals approximately spanning the early Aptian to latest Albian of the mid Cretaceous (120-100 Ma). Consequently, fossil occurrences of the long-proboscid condition are divided into two overlap- ping intervals: the Middle Jurassic to late Early Cretaceous (phase 1), Matig ca. pe million M Kis 165 to 100 Ma d = (phase 2), commencing at 120 Ma and lasting ca. = million years to the Recent (Figs. 1, 2, right margins). The long-proboscid s; did dades : stages, past or present (Table 1). Most un mental this is attributable to the embryologic genetics of mouthpart formation (Jürgens & Hartenstein, 1993). Mouthpart elements from the maxill e are developmentally available for co-optation wau S... : [PER VUE | Š e such d as the siphon (Handschin, 1929; Eastham & Eassa, . Evidence a -— mecs in a Volume 97, Number 4 0 Labandeira Pollination of Mid Mesozoic Seed Plants 1955; Nagatomi & Soroida, 1985), often with anatomical contribution from fon doge Booten regions a ce et al., 2005). Sipl a rec d occurs, perhaps in a eo as and developmentally homologous way, in the conversion a es pa ne piercing-a sekig (Rogers & Ksufman, 3 997). Examples of functionally convergent siphonate mouthpart structures have been found in seven of the 13 holometabolous clades, including representatives of the Lepidoptera, Diptera, Coleoptera, and Hymenop- tera, and the less diverse M Neuroptera, and Trichoptera (Table 1). The occurrence of siphonate — — D 5 99% of the species in the huge lepidopteran clade Glossata (Kristensen, 1997), to a few, major clades in the brachycerous Diptera (Labandeira, 2005a), where the condition may be plesiomorphically primitive, to a major extinct clade of the Mecoptera (Ren et al., 2009), two extinct lineages in the Neuroptera (Labandeira, pers. obs.), two minor, probably related clades within the Coleoptera (Rivnay, 1929; Bologna & Pinto, 2001), a few sporadic species in the Trichoptera (Ulmer, 1905; Cummings, 1913, 1914), and many originations across the Hymenoptera (Takeuchi & Tokunaga, 1941; Schedl, 1991; Krenn et al., 2005). These functional conver- gences have originated minimally 25 to 120 times in LI EE I hictary a 2 +L LI = occurrences are provided in Table 1. Other fossil and sedem ripe pa t dieere NN Baud by way of inediti, the long-proboseid clades of phases 1 and 2 are discussed below AT PROBOSCID CONDITION The permithonid TTschekardithonopsis ?oblivius Vilesov "N ilesov, from central Ural Mountains of Russia, exhibits a promi- nent, ca. l.7-mm-long proboscis (Fig. 3). The pre- served proboscis of this specimen apparently consists of conjoined maxillary palpal elements that still retain segmental divisions, including a thickened terminal region bearing fine setae. A comparatively narrow food tube is present, indicating a use for feeding on fluids, possibly secretions accessible from concealed, reproductive organs (Mamay, 1976). MECOPTERA (PHASE 1 OCCUPANT) Extant adult Mecoptera (scorpionflies) are detriti- vores or scavengers, occasionally predators, but rarely are associated with flowers (Piggott, 1958; Porsch, 1958). Modern scorpionfly mouthparts are fundamen- tally mandibulate, located terminally at the end of a long, downward, projecting extension of the head capsule (Heddergott, 1938). The labium, while elongate, consists of a medial structure basally Manka i. +k > k A 1 it t f, the medial glossae and laterally positioned para- glossae typical of the mandibulate condition. Mandi- bles are prolonged-triangular and functional, and are used in E for feeding on solid, often dead, food. By e proboscis of the early derived a Tanie & Kozlov, 1991), a clade consisting of the three Mesozoic families, Meso- psychidae (Figs. 4, 5), Aneuretopsychidae (Fig. 6), and pha gee og (Fig. 7), is consider- erent, consisting of siphonate mouthparts nice. 1997; Grimaldi et al., 2005; Ren et al., 2009). The proboscis structure of the Aneuretopsy- china is better known than any other clade of long- id insects in the Mesozoic fossil record, a consequence of superb preservation in the Middle Jurassic a (165 Ma) and the mid Early Cretaceous Yixian (125 Ma) Formations of China. The length of these proboscises varies considerably, from ca. 2 to ca. 11 mm; widths vary from ca. 0.2 to 0.6 mm, with proportional variation in their food canal widths (Figs. 4—7). The proboscises are generally long and gracile, and not thick and short. Among these t modestly diverse families, the proboscid surface can be smooth or ribbed, occasionally ornamented with transverse ridges, or clothed in fine or coarse setae of various densities. The tip of the proboscis may lack capillary uptake organs, or more commonly may be surmounted by three types of pseudolabellae, de- pending on the species. The proboscis is connected to a cibarial pump underlying the clypeus, providing a suction to assist the capillary-based uptake of fluids by pseudolabellae. There is some evidence for a second suction pump at the proboscis base in the O (Ren et al., 2009). Three-segmented, ial are present only in the Meso- n usata, taxa of the other families are palpless Relevant to the origin of the long-proboscid vlads is the Nannochoristidae, a plesiomorphic extant lineage whose fossil record extends to the early Mesozoic. Its distribution was once worldwide, though the c now is confined to the western Gondwanan region of eastern Australia, New Zealand, and southern South America. The phylogenetic position of the Nanno- choristidae has been highly debated, variously considered as the basalmost extant scorpionfly clade, a separate order, a sister-group to the Diptera, or even a clade within the Siphonaptera (fleas), due to its atypical mouthparts for extant mecopteran taxa (Ren Missouri Botanical Garden Annals of the 800 “TP 19 "itopugqe' :eco0z *e1ropueqe' ‘9007 eunf “wuwo *s1od *rsAo1sopy *200g "Te 19 e119pueqe'T ‘0007 *uruoury X O[OIeZZe]W 22007 “Te 19 varopueqeT ‘48661 ‘uy 22007 “8 19 eriəpueqr' *9s00Z “extopueqe] “UH “8661 alo `sqo `siəd Se 11661 '^ouousoov 6006 “`[# 19 Yay 6100 “PE 1 enopueqe] *1661 “A0[203 39 uásusey S661 'A0SO[IA ,899u2139]2H pere eqe Tee rqe mgen (jeop93;) Kreppixeur rqe rqe jeiqer (sdped) Arrow squouiopo stəsoqoid sofe essteg eisean ES :RBOLISUIY YINOG UBIXIA :PISEID'] UPIXIA “essirg *nejgiewv ¿BISBIN Y UBIXTA *nejeaewy eseng UPIXIA Inejpiew *nosingoe(q :erseansg Bury) ‘uvex g pue hosnyorg ‘erseany Joquie osounmg pue *ugiXrA Inejeew *nodnuoe(] :eiseiny Pury) ‘noĝnyoeq :pispiun;] vissny zupeoo| pus Áudvisdoosorg [|Pi191eur pequosopun (9-36 314) UILIQUIY X o[o1ezze[y DiouÁM049DUi. 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"peuodoz are syrediinour prosoqoud-Suo[ "suoneiro jugAo[ar 1aqyo pue *sorpnis Ago|oudiotu ueduinoui *səsK|eue ənəuəgo|Kud ‘suonduosap satoads Surpnyour ‘saounos amgeaoj[ [[e opn[our saoua13j23 , (ovursso¡8 Amy sepnopo) - 0007 uolsnojj :01ə1douəu]) “ISUSYINA tege *uoisnog sunodsorgur ` (Ied[ed) &xejprxeur eiperisny baafingn) Dusayng luəoəl[ viafimqni wusana G00Z “Te 19 uuary ‘0007 “*uəstu[əu[tA (swurümq :oeprlied — Y SIA[ *1661 ‘IPAS sunodso1due [eique enensny Aqury snpinu sting 1u999y ‘eroydouawAy) stung 0002 à 'uosuipouprA x stA1of (runisopopy :osprurpangiua, ‘GL6T ‘ONEN ‘TH6I Tequr nono :t1o1douaurkg 1) *eSeunyo Y IonoxeL, surrodsoidue pue Ármixeur uedef — smigpanu smyoukuyaouoddi 1u90ay snysudysouoddiyy ,899ue19Joq sisoy jutqd.- squouio[o ,Ali[eoo| pue uloloy saouasojod andy &Soouo142008 Japio yasut — ; pouojug stosoqoad aofepy KudeisooSotg pue o[durexe jsogr [9aa[-a3uyg pue uoxe] [6904 Tpenunuo) ^p eiger VECES PRESE set Qs IP Do omae Lar SPI eee ge Bea TOU Cds NOE E NM EIE EAST S I Ear rs ET eer et daa. cp ab ape EA m US ddl Volume 97, Number 4 Labandeira 491 Pollination of Mid Mesozoic Seed Plants The earliest vos long-proboscid siphonate insect, A gna ?oblivius Vig (Vilesov, 1995), fro € rien PUN hekarda, €— Pius Mountains, Russia, of Lower Permian T an) age. —A. Photograph of entire specimen. —B. O voi eim ng of A. —C. Photograph “of outlined area in A. iet ‘Ov iin) drawing of head, mouthparts, and horti in C. Scale = en 492 Annals of the Missouri Botanical Garden ); specimen CNU -M-NN200 imen modifi ified slightly - Photographic detail of siphon with Mesozoic Mecoptera t Shih, oe m } proboscis, 5-021-1; scale from Ren et al. ind. CNU- M- NN2005-024; scale bar = 1 m : Family Mesopsychidae. —A. pogo s, labial palps, and antennae, ann roboscis lengt othe mm. —b- ba setae (center), 3- -segmented labial palp (center cea A A ALA Ii e e ac Sky qa akka S se tives L eR SU. x Volume 97, Number 4 Labandeira 2010 Pollination of Mid Mesozoic Seed Plants Figure 5. Reconstruction of two mid Mesozoic associations €—— _mesopsychid piatti and their inferred. host plants. Courtesy of Smithsonian —— Painting by M. Parrish. —A. Lichnomesopsyche gloriae feeding on the pollen drops of Caytonia sewardi Harris through an ntegumental pus under "e cuales s lower lip. Nbocióted pellen; ,ohwiporites sp.. would have b btained fro rris pollen organs nearby. The affiliated foliage of Sagenopteris colpodes Harris is shown A ibis Eurasian, Mi ddle Jurassic cu assemblage (Ren et al., 2009). —B. The mesopsychid Vitimopsyche kozlovi Ren, Laban deira & Shih feeding on ira p funnel p of the cheirolepidiaceous ovulate cone Alvinia lobos ica Kvatek. Classopollis sp. pollen would have been vectored by this scorpionfly from — F renelopsis alsia diseno Knobloc h prre cones on tbe: same or diesque plans ae foliage, also termed F. a. Eurasian et al., 2009). The Nannochoristidae is characterized NEUROPTERA (PHASE 1 OCCUPANT) by a modified, projecting but short, tubular labium inferred to take up fluid food (Beutel & Baum, 2008), Adult and larval neuropterans are overwhelmingly an early mecopteran mouthpart type that likely was a — insectivorous. With the minor exceptions of the precursor to the long-proboscid condition of the proboscis bore by one species of Early Permian Aneuretopsychina (Ren et al., E Periodos (Fig. 3) and some modern Nemopter- SA t) of i in A (Ren et al., 2009); scale bar = 1 mm. Preserved proboscis length is 4.5 mm, um SEEN extended to ca. 9 mm. —D. Ove rlay drawing of a third — of L. gloriae showing head, mouthparts, palps, and antennae (proboscis truncated); CNU-M-NN2005-023; scale bar = 1 m ente Photo i image e dorsal br view xis a fourth specimen (Ren et al., 2009); CNU-M-027-2; scale bar — 5 mm. P I g —F. Phot of a complete specimen w whose mouthparts are detailed in A above; head and proboscis at lower right; scale bar = 5 mm. —G. Photo of a fifth specimen, with proboscis at top center (Ren et al., foot “ONU M-NN2005-020-1; scale bar = 1 mm. Proboscis length is ca. 10 mm. Note: in Figures 4 and 6-9, all head sizes are standardized to a scale bar that represents 1 m to establish a comparison of the relative sizes, shapes, aspect ratios, and e features of the long-proboscid specimens. Al specimens on this figure are L. gloriae from the Middle Jurassic — n Formation, Inner Mongolia, northeastern China. A-C, E, and G reprinted ‘vith permission from Ren et al. 494 Annals of the Missouri Botanical Garden ure 6. The long-proboscid i : opch E e liaoningersis me ME em in mid Mesozoic Mec 'optera: Family Aneuretopsyc hidae. —A. Photo of bar — 10 Proboscis len ngth is ca y ani mu owing head and proboscis at top center; CNU-M-NN2005-002-1; scale et al., 2009 09). Xn Ov drawing alos hd pecimen is from the Yixian Formation of Liaoning, northeastern China (Ren proboscis; scale bar — 1 mm. —C. Detail d sep of the head in A a we, — compound eyes, antennal bases, and A" an ellipsoidal mouth, =D 1 m MEE A and B, s showing transy ree ribbing and a terminal pseudolabellum at right, enlarged and — in E below; CNUA. OS QUI species of pr with head, antennae, and proboscis iid of an enlargeme t of head and proboscis in D l; scale bar — 5 mm. roboscis length is ca. 6 mm. —E. Overl: ei oto indicating detail oa m ac T > Compare to the head of a congeneric species in B; scale bar = = 0.1 m hee in s 4 and € A hoja sa other ornamentation on proboscis and leg in D and E above: scale bar mparison of the utm sizes, shapes, as aspect ratio are standardized to a scale bar that re presents ] mm to establish a pelao with permission from Ren et al. (2009). (S. and other features of the long-proboscid specimens. Parts A, B, D. and E “payaka rak (cathe ie Sec oa Ghatak T eae, | PER es rahe Bate Volume 97, Number 4 Labandeira Pollination of Mid Mesozoic Seed Plants 495 Figure 7. The long-proboscid siphonate condition in mid Mesozoic Mecoptera: — P hih Overlay drawing of head, antennal right; NU-M-N 2005-004; scale — ] mm. & Labandeira. (s dp ar = = mm. —C. Enlarge "S Figures 4 and 6— n d m. —D. Es of a pues specimen of P. janeanne, showing roboscis e indicating flexibility; CNU- M-NN2005-003; se e bar = 5 mm. Proboscis length is ca. 2 mm. Note: in t represent ] mm, to establish a comparison of the relative sizes, shapes, sD ratios, and other features of the long- a specimens. Parts A, B, and D reprinted with permission 009). from Ren et al. (2 idae (Tjeder, 1967; Krenn et al., 2008), there has been very little in e phylogeny or tnihi INOI phology t in palynophagy, nectarivory, or r polidi. However, one extinct lineage, the Um mid Mesozoic Kalligr: a major exception, assumed to have had tad associations with plants (Zherikhin, 2002; Engel, 2005b; Grimaldi & Engel, 2005). The Kalligrammatidae have considered as fundamentally mandibulate (Grimaldi Engel, 2005), like the mouthpart spectrum of m neuropteran lineages (e.g., Tjeder, 1967). Recent specimens from the same two mid Mesozoic deposits in China that produced siphonate mecopterans also have yielded impressively large igrammati europterans exhibiting siphonate mouthparts as sit (Fig. 8). Their known proboscises range in length from a slender 11 mm to a robust 20— 25 mm. Interestingly, the extant related lineage Nemopteridae (spoonwing lacewings) displays active morphological nectaring of herbaceous plants (Krenn et al., 2008), though it possesses elongate and modified, but basically mandibulate, mouthparts (Tjeder, 1967). Unlike the fundamentally labial proboscis structure in me ae era and pem, he kalligrammatid a siubal a that is aii rally aiie to that of the lepidopteran Glossata (Labandeira, pers. obs.). DIPTERA (PHASE 1 AND PHASE 2 OCCUPANTS) Diptera exhibit various modifications of the labium and supporting structures, with palps and labellae functionally transformed into ensembles for nectaring and occasional pollen ingestion. Several major clades of nematocerous and especially lower brachycerous flies have convergently resin long proboscises agatom roida, rrell & Kinds , 2005), often Sod in Er: io Proboscid lengths in Mesozoic taxa ranged from 4 to 9 mm, and 496 Annals of th Missouri hice Garden ition in m id Mesoz ZOIC Neuro ter f il > í : ing wing eyespots; CNU- r ptera: tamily ies campeggi intem Photo o illary : "d of the head NEU-NN2009-032-2; scale bar = 5 mm. —B. Overlay drawing ma m probably hogs ae leg; m = d. seu from top center in ^ showing antennae, compound eyes extended toca. mm, inferred fro S © bar = l mm. The p rved enn length is 14 mm, but i thei ir aspect ratios. Note: in Figures 4 an aspect rati hat re pe ios, pee the Ps of the a bus d — 1 mm to establish. a eotapunisoq of the relative sizes, shapes: Volume 97, Number 4 2010 Labandeira Pollination of Mid Mesozoic Seed Plants aspect ratios varied from gracile to robust, as in Early Cretaceous Nemestrinidae (tanglevein ies Fig. 9). Brachyceran taxa of ae, strinidae, Apioceridae, and others (Figs. 2, 9) are pa known from Middle Jurassic Eurasian deposits that reveal sp proboscises either for nectaring, as in the ase of the Nemestrinidae, or conceivably Moved in bifa mama om proboscises that would en. nectaring in males and joint nectaring and blood feeding in perdat: females, as pangioniine horseflies of the Tabanidae (Mostovski, 1998; Ren, 1998a; Mazzarolo & Amorim, 2000; Labandeira, ee ea mem nid Mee based on distinctive Mer Jpeoliquoises and associated mouthpart es (Mostovski, 1998; Ren, 1998b; a 3 052). clumps of gymno- spermous Classopollis pollen on their heads (Laban- so see Nicholson, 1994), and high Nepi M al., 2009» Aocodiony. these nega a and palynophag initially targeted gymnospermous seed pits during e Middle Jurassic and evidently transferred their diets to angiosperms during their initial radiation of the Early Cretaceous. Insect clades such as the Nemestrinidae, Apioceridae, an nidae continued through this transitional interval and persist to the present day on angiosperm nectar (Manni & Goldblatt, 1996; Morita, 2008), but with decreased diversity and relict distributions. TRICHOPTERA (PHASE 1? AND PHASE 2 OCCUPANTS) In adult Trichoptera the principal feeding organ consists of conjoined and expanded maxillary palps whose distal segment is expanded into a labellum-like spongi , the haustorium, for uptake of surface fluids (Crichton, 1957). At least two modern taxa have diverged independently from this condition and evolved an analog to the lepidopteran siphon. The closely adpressed galeae from the maxillary region orm a tubular structure that joins in a relatively loose arrangement, resulting in a tubular or near-tubular pro s for imbibation of nectar and other fluids. The ae origin of this siphon is similar in arrangement to that of the kalligrammatid Neuroptera, glossate Lepidoptera, and ripiphorid and nemog- nathine Coleoptera. This distinctive proboscis is associated with flower-feeding and occurs in the unrelated Dipseudopsis africana Ulmer (Dipseudopsi- rom southern Africa and Plectrotarsus graven- horstii Kolenati (Plectrotarsidae) from eastern Aus- tralia ( ia (Ulmer, 1905; Cummings, 1913, 1914). LEPIDOPTERA (PHASE 2 OCCUPANT) Constituting almost all of the lepidopteran taxa, the diverse clade Glossata is exemplified by a proboscis consisting of maxillary, paired galeal elements uniquely joined into a figure-8 configuration in arrangement tae (Kristensen, 1984 Fig. 10A). The lepidopteran proboscis is almost always distinctively coiled due to angled, intrinsic characteristic knee he nsen, 1984, 1997). The lepidopteran proboscis is derived from the same mouthparts region as the proboscis of kalligrammatids and meloid beetles. The origin of the lepidopteran proboscis occurred during the mid Early Cretaceous, contemporaneous with the angiosperm radiation, based on the earliest once Labandeira et al., 1994; Grimaldi & Engel, 2005). However, there is a distinct possibility that the Glossata, partly defined by the synapomorphy of a siphonate proboicis may have meo earlier, in association and they moved to iode pope hosts ione diminutive flowers ted probes by short-siphoned moths ix. see Powell et al., 1999). COLEOPTERA (PHASE 2 OCCUPANT) Coleoptera are the most speciose order of insects and exhibit dietary diversity and mouthpart variation that rival those of the inge and Hymenoptera (Crowson, 1981; Godfray , 1999; Skevington & Dang, 2002; Grimaldi & dis 2005). Although most Coleoptera possess mandibulate mouthparts an biting-and-chewing feeding habits, the clade is rife with mouthpart modifications. In phytophagous line- ages, herr are serra! paka mou tapan types, some of others that i inv ;iolve diverse ways of acta asiatica onim 1981). A a formed from conjoined g among acrosiagonini of de "Ripiphoridse (ri E beetles), and particularly the Meloidae (blister beetles), the latter in the subfamily Nemog- nathinae (Rivnay, 1929; Barth, 1985; Fig. 10B). The Nemognathinae are illustrated by the indir Pri Leptopalpus rostratus Fab. and Nemognatha punctu- lata Fab., which have conjoined maxillary galeae. although in some E - atia halves are is found incompletely connected, su channel rather than an enclosed tube RA. 1929; Barth, 1985; Borrell € Krenn, 2005). A larval meloid fossil has been found from the middle Eocene (Engel, 2005a) Annals of the Missouri Botanical Garden = j M el ——HEÓ E Le 5 mae = s os o VR E T re 9. The lon g-proboscid siphonate condition in mid —A. Overlay y deta: of do of he. Mesozoic Diptera: families Nemestrinidae and Cratomyiidae. aspect of head, is, and prothoracic legs of Protonemestrius Jurassicus Ren (Ren, 19982) (Nemestrinidae), from the iid Early Cretaceous of binis eqs enlarged from B at right; CNU-LB1 = ] mm. The comparativ: " thin and gracile ee ies ngth is ca. 5 mm. : and proboscis shown in A at left. Sc ale cimen with head . —C. Photo of eM rius pulcherrimus Ren (Ren, 1998) Volume 97, Number 4 2010 Labandeira Pollination of Mid Mesozoic Seed Plants and poorly known adult ripiphorids extend earlier to the latest Early Cretaceous (Perrichot et al., 2004), though it is unclear whether these taxa are associated with siphonate mouthparts. HYMENOPTERA (PHASE 2 OCCUPANT) The central mouthpart feature of Hymenoptera that projects into flowers for nectaring is the concealed nectar extraction apparatus (CNEA). As an integration f and labial elements, the CNEA can be deployed in ' leverlike fashion for projecting into flowers or structures for extraction of nec (Jervis et T 1993; Jervis, 1998). The CNEA is Si) typically parasitoid wasps and probably origi T duda the parasitoid revolution of the Early Jurassic (Lal sbdeira, 2002b), although it has been transformed into multielement siphonate mouth- parts of independent origin approximately 100 times, particularly in more recent lineages that have larger body size, such as vespid wasps, ants, and especially Krenn et al., 2005). The CNEA represents a distinctive mouth complex when compared to the comparatively simpler, long-proboscid mouthparts mm in other major holometabolous lineages. a few taxa from earlier, basal s of Pd Symphyta (sawflies)—w convergent with the long-proboscid condition he able Tp Some symphytans that have tubular elized proboscides the sawfly cai P de (Schedl, 1991), which includes pet proboscis labial components, and the common sawfly Nipponorhynchus of the Tenthredinidae (Takeuchi & Tokunaga, 1941), which includes both maxillary and labial elements. At the opposite end of the hymenopteran phylogenetic spen is ree iue e ere Po. y OL MaAtlital y palpal structures elias: 1983). DISCUSSION Several persistent themes characterize the evolu- tion of pollination modes between seed plants and insects during the mid Mesozoic. The first theme is the phenomenon of separate structural and functional convergence in insect mouthparts and in the receiving structures of seed plants. One remarkable aspect is the variety of ways mti cH. "e rd du. uced similar mou thpar from different "menia structures of the major segmental nsect head, especially the elaboration of maxillary d labial appendages. The same can be said for the various structural accommo- dations that have been used by gymnos plants, especially to facilitate pollination-drop pro ing and pollination by d long-proboscid insects. A second theme is plan turnover, reflecting te cd ee patterns as various gymnosperm lineages were extirpated while permous seed ost and insect pollinator angiosperms underwent a major radiation. A third theme addresses how the data in this contribution provide for an explanation in long-recogniz eso- zoic trends in the diversity records of fossil insects, fossil plants, and their associations FUNCTIONAL CONVERGENCE IN HOST AND POLLINATOR ATTRIBUTES BEFORE ANGIOSPERMS Similar genetic and developmental programs ac- count for the parallelisms between gymnosperms and angiosperms as well as between quite different lloc insects in achieving similar pollina- tion mechanisms. The efficiency of these mechanisms was presumably modulated by architectural and phylogenetic constraints that resulted initially in subopti u tedly reflected by tem- poral lags between the initiation of the association and its subsequent fine tuning. Nonetheless, there was generational continuity of both the pollinated plant and insect pollinator. solutions Plant ovulate structure If the hypothesis that certain mid Mesozoic pollination is correct, then an expected outcome would be multiple, independent, and varied solutions — E from the mid Early Cretaceous of China; head at M mdi inD below; CNU-LBI991-008; scale bar — = mm. "n of right lateral view of head * ea bas = The comparatively — and robust pat. proboscis “length is ca. 4 mm. E. Photo of Cratomyia macrorrhyncha Nonus mid A DBRP-0050; scale = 1 mm. —F. Overlay Pesca of the ventral pest Y tC. macrorrhyncha head in E, showing convergent c ron eyes, proboscis, antenna, and prothoracic legs; se mm. The pte decking proboscis is ca. T5 mm m long. —-G. Photo c pace idea sin abel obes eim CI Not: ote: : in Figures 4 and 6-9, t p shapes, aspect ratios, RUE ee ene 1 ue" Annals of th : f the Missouri Botanical Garden Figure 10. The lon bosci £-I 1 siph lition in Early Cretaceous Lepidoptera and modern Coleoptera. —A. F rontal and occipital views of the head and separated maxillary galeae of an un escribed glossate moth ( Lepidoptera: Glossata), from the early Late Cretaceous (Turonian) of New Jersey (Grimaldi & Engel, 2005: fig. 13.22). Reprinted with permission from Grimaldi, D. A. & M. Engel. 2005. Evolution of the Insects. Cambridge University Press, Cambri Head and mouthy g a proboscis of conjoined galeae, of the recem gnathine blister beetle Nemognatha sp. (Coleoptera: Meloidae) from central Europe (Barth, 1985: fig. 31). The proboscis length in A is estimated as 4 mm and in B 1t 18 approximately 10 mm. Reprinted with permission from Barth, F. C. 1995. Insects and Flowers: The Biology of a Partnership. Ist ed. Princeton University Press, Princeton, New Jersey. rts. includin to insect pollination mechanisms, some of which were less reliable than those of today (Campbell, 2008). The diverse structures and inferred in seed plant ovulate organs to fac are instructive. For example, in can by an integumental tube surrounded by cupulate tissue connecting each micropyle to a surface aperture mechanisms seen Harris, 1933, 1 ). For the bivalved Leptostrobus, pollination was accomplished by anatropous ovules idate insect- oriented adaxially, but with an abaxial entry point at pollinated lineages of gymnosperms, a wide variety of the exposed, opposite end of the ovulate organ, ovule-associated, elongate tubular structures received through which a 4- to T-mm-long interovular channel scises of various lengths, widths, and aspect was available to access deeply sequestered pollination ratios (Labandeira et al., 2007a; Ren et al., 2009). drops. For ovules reported in Pentoxylon and These tubular structures originate from various Umkomasia, structures consistent with wind pollina- ovulate and adjacent plant tissues, but share the — tion, an additional mode could have been insertion of function of accepting a proboscis for a reWard of a short insect proboscis into the micropyle, providing pollination drop fluids in return for depositing pollen. a simple reward of pollination fluid with minim In Caytonia, an inserted proboscis was likely received modification of surrounding extraovular tissue. Gne- A A eae ETTI TNT US T Volume 97, Number 4 2010 Labandeira 501 Pollination of Mid Mesozoic Seed Plants taleans such as Problematospermum were achenelike ovules that bore broad micropylar pappus tubes extending at least to 14 mm, at whose base originated enveloping, bracteate, papery structures and setose plumes (Krassilov, 2009; s et al., 2009), possibly attracting mobile, winged pollinai Undoubtedly, the most ebd construction for insect pollination in any plant is re m arborescent cheirolepidiaceous conifers (Alvin et al., 1994; Axsmith et al., 2004; Labandeira et al., 2007a), whose ovulate organs apparently were more compli- cated than that of any other Mesozoic gymnosperm or angiosperm. The morphology of Alvinia bohemica ovulate scales is consistent with entomophily through the provisioning of lures, such as the prominent abaxial lobes perhaps directed to indicate the funnel opening, and rewards such as secretions from deeper nectary-like structures at the funnel base and perhaps glandular trichomes near its opening. Smaller con- specific pollen cones accordingly supplied Classopol- lis pollen that would have been transported by long- proboscid or small nonproboscid insects. In addition, Classopollis pollen has been identified as intestinal boluses and smeared on the head capsules of several coeval mid Mesozoic insects (Krassilov et al., 1997a; Labandeira, 2005a). Insect mouthparts With the exception of siphonate mouthpart exper- imentation during the Early Permian, Mesozoic mandibulate and stylate mouthparts were transformed , based phase 1 and the earlier part of phase 2 (Table 1). These changes parallel the convergence mentioned above in seed plant ovules. Major, mid Mesozoic insect clades with this mouthpart mo are: E Mecoptera (Mesopsychidae, iia lycentropodidae); (2) Diptera (Nemestrinidae, Pana Mydidae, Thereviidae, pangioniine Ta- banidae, Vewsileonidaok sata); (4) Neuroptera (Kalligrammatidae); and pos- sibly (5) Trichoptera (descendants of Permian or ancestors of modern siphonate taxa); (6) Hymenoptera (parasitoid wasps or apoid bees and their wasp relatives); and conceivably (7) Coleoptera (macro- siagonine Ripiphoridae and nemognathine Meloidae) n Poent A Bein, = - Laband 2005 L. 2009). hi is instructive that two species of ¿anun Trichoptera | token three species of Hymenop- tera with karaii taxa lack a fossil record (Table 1). Extant and fossil long-proboscid mouthparts typically have a "- — of etin, panies on and frequently the proboscis itself. Other fontures slated to pollen, nectar e and pollination include a ridged or rib n bi in —M— and nd structures at the sse tip "m ied x of fluids, including the dipteran labellae, mecopteran pseudola- bellae, trichopteran haustorium, and flattened plates at the siphon tips of some glossate lepidopterans (Barth, 1985; Chaudonneret, 1990; Krenn et al., 2005) and alligrammatids. Often, such proboscises are accompanied by palps that are absent or significantly reduced (Chaudonneret, 1990; Ren et al., 2009). There also are convergent parallels between long- proboscid mouthpart features and gymnosperm ovulate features mentioned above, suggesting close associa- r imperfect. If these ovulate and insect mouthpart features evolved in tandem, a true coevolutionary relationship may have existed, although coevolution is demonstrated from s reciprocal feedback in modem o (Jan 1980) and is difficult to test in ii fossil iie besides, the congruence between ovulate organs and co-occurring insect mouthparts is more than fortuitous (Ren et al., 2009). First, both plants and insects with apparently linked structures co-occur in diat Second ik t Il z ] kak £ tions or even mutualisms, howeve tubelike features in ovulate organs tightly matches the coeval spectrum of insect mouthpart sizes and shapes that would fit into these tubes. Third, the pollen morphology is more consistent with insect than wind dispersal. Fourth, pollen grains from candidate ovulate organs presumed to be insect pollinated are the same grains found on mouthpart contact surfaces and in the nsect pollinators. Finally, the ed plants were bisexual and presumed to outcross with conspecific pollen organs. PALIERNS LN TO ANGIOSPERMOUS POLLINATION Not counting an Early Permian occurrence, the assemblage of gymnosperm-insect pollinator associa- tions (phase 1) lasted ca. 65 million years, from the Middle Jurassic (165 Ma) to approximately the late Early Cretaceous (100 Ma), well into the angiospe enn The m of phase 1 with mre 2 me when many earlier gymnosperm insect associations were rare, uncommon, or extirpat- ed (Figs. 1, 2). During the 20-million-year co- occurrence of phase 1 and phase 2 associations, and continuing into the Turonian Stage of the early Late Cretaceous, angiosperms expanded their initial evo- lutionary and ecological scope, accompanied by Annals of the Missouri Botanical Garden geographical shifting, decline, and demise of gymno- spermous groups. During the mid Cretaceous interval of mounting angiosperm dominance, there were three macroevolutionary patterns of plant hosts and insect pollinators. First was the extinction of many sperms and their insect pollinators. Second was the survival of other, older, mid Mesozoic insect-pollinat- ing lineages that transferred their host preferences from gymnosperms to angiosperms. Third was the origination of new angiosperm taxa and their new insect pollinators; this latter pattern has been dominant since the mid Cretaceous. Pattern 1: Extinction Several major seed plant lineages with pollinator associations either became extinct or were significant- ly diminished in diversity during or soon after the angiosperm radiati wskiales, Voltziales, Pentoxylales, and Caytoniales became extinct around this interval, whereas Corystospermales, Cheirolepidia- ceae. and nettaal úl ía l l rsity until the Cretaceous-Paleogene (K-Pg) boundary or shortly thereafter (Fig. 1). Insect pollinator lineages that underwent a similar extinction during the angiosperm radiation were Mesopsychidae, Aneuretopsychidae, and Pseudopolycentropodidae (Mecoptera), i i dae (Neuroptera), and Cratomyiidae (Diptera). Many other nonpollinating but nonetheless plant-associated insect lineages alsa h a O , such the Palaeotinidae (Hemiptera), Lophioneuridae hysa. noptera), and Eolepidopterygidae (Lepidoptera). Pattern 2: Lateral transfer One particular insect clade, Diptera, experienced limited pollinator extinction during the interval when angiosperms became ecologically dominant. Modern floricolous, long-proboscid dipteran lineages, such ds Nemestrinidae, pangioniine Tabanidae, Apioceridae Thereviidae, and Mydidae, had their origins in the Jurassic as associates of gymnosperms. This continu- ity indicates a shift from earlier fluid feeding on pollination drops of gymnosperms to subsequent nectaring on angiosperms. These transfers probably represent opportunistic cl ic events in the Plant and fly lineages, with an effect at higher taxonomic ranks, seen in family-level diversity data (Labandeira & Sepkoski, 1993; i 1996). It is unknown why, for pollinators, only the Diptera escaped the extinction blitz. Further ñ i may be gained in establishing which biological host shifts from gymnosperms onto angiosperms. Pattern 3: Origination Major clades of insects had their origins e pollinators and phytophages on angiosperms d their initial radiation, traceable through fossil oc during the early, formative period of angiosperm ` evolution, representing the 25-million-year interval 4 from the late Barremian (125 Ma) to the end of the Early Cretaceous (100 Ma), and probably continuing to the mid Turonian (90 Ma). Much of what has been documented for this crucial longer interval involves - angiosperms and their associated, | especially pollinating, insect clades and consequently focuses on the origins of much of the current land , biota (Crepet, 1983, 2008; Crepet & Friis, 1987; - the radiation of Grimaldi, 1999; Grimaldi & Engel, 2005; Crepet & Niklas, 2009). The remarkable co-radiation of insects 1 and angiosperms is better documented than earlier A associations between plants and insects, such as the Late Triassic event in Gondwana (Labandeira, 2006a, — b) or the Middle Jurassic origin of gymnosperm 8y l pollinating clades discussed here. Whether earlier, mostly Jurassic, associations, including pollinator associations between insects an gymnosperms, have a role in explaining the success and launching of perms remains an unexplored question. MACROEVOLUTIONARY AND MACROECOLOGICAL INTEGRATION One perspective for understanding the major patera, of insect pollination during early angiosperm diversification was provided by Grimaldi (1999), later updated in Grimaldi and Engel (2005). This has been ` supplemented by the accumulation of new data and a more comprehensive understanding of plant-insect - i long before, during, and soon after the k (Gorelick, (VU associatio diverfiscs 2001; Labandeira, 2005a, b; Labandeira et al . 20072; Crepet, 2008; Nepi et al., 2009: Ollerton & | thard, 2009; Ren et al., 2009). Recent associ- ics during the mid Mesozoic should (1) incorporate important information from older, Juras- . Volume 97, Number 4 2010 Labandeira Pollination of Mid Mesozoic Seed Plants sic and Early Cretaceous compression deposits; (2) encompass data from additional insect taxa that also emphasize mandibulate insects; (3) include knowl- edge of mouthpart structural details and feeding modes that reveal convergences; (4) add crucial plant associational evidence such as the reproduc- tive structure of plant ovulate organs and pollen consistent with entomophily; (5) assess the babam of endophytic larvae, perhaps immatures of conspecific pollinating adults in their consumption patterns of plant reproductive tissues; and (6) provide additional data of the later Mesozoic record of insect diversity for a broader synthesis of extinction and origination patterns. Although this list requires considerable interdisciplinary and atypical integration of paleobotanists, paleoentomol- ogists, and ecologists, there have been three areas of improvement in understanding the Mesozoic history of insect pollination. Two basic types of mid Mesozoic pollination The record of mid Mesozoic pollination is divided into two fundamental types of pollination and related associations. (1) Mandibulate palynop that interact with plant hosts bearing bes ped reproductive organs with rewards typically being pollen d ipea reproductive tissues. Larvae often are endophytic consumers of reproductive tissues from the same host plant used by eon adult pollinators. Inferred associations are p nantly those between beetles and plants with ed often bisexual strobili, such as Bennettitales, but also including the physiognomically similar cycads and probably pentoxylaleans. (2) Fluid-feeding insects ariety of insect clades access this type of pollination reward; they have long-proboscid mouth- parts with features consistent with penetration of various tubular devices in gymnospermous ovules and associated tissues. A detailed contrast of these two different types : ens is provided by Laban- deira et al. (200 The existence of a distinctive type of long-proboscid pollination on gymnosperms during the mid Mesozoic The mid Mesozoic long-proboscid insect pollination mode discussed in this and two other recent reports (Labandeira et al, 2007a; Ren et al, 2009) was predicted earlier by pollination biologists working on modern seed plants (Meeuse, 1978; Lloyd & Wells, 1992). However, earlier discussions did not propose any credible, co-occurring insect pollinators, and no functional interpretation was given for the various tubular structures in reproductively anomalous plants such as the Cheirolepidiaceae (Axsmith et al., 2004; Axsmith & Jacobs, 2005) and Caytoniaceae (Harris, 1957; Dilcher, 2000; Ren et al., ). — skepticism for the existence of a pre rmous pollination mode on — by fluid- a insects has been superseded by additional structural evidence for insect- e and plant- ovulate features indicating diverse pollination modes that preceded angiosperms. Whether these novel data impact theoretically or mechanistically on the origin of the angiosperm flower remains to be seen. But it would appear that criteria based on more efficient angiosperm pollination, particularly given the wide variety of disparate receptive structures found in gymnosperms, may provide a way forwa The impact of mid Mesozoic pollination data on understanding plant and insect diversity in the fossil record There is a significant drop-off in perm- pollinating clades during the Early oia (Niklas et al, 1985; Ren et al, 2009), and many more nonpollinating,. pariophsgoua. nega, such as pier- cer-and-su feeders, similarly became extinct. One hypothesis the this interval of insect extinction, supported by their preangiosper- mous occurrences and occasional knowledge of their biologies, is that their life cycles were closely connected to gymnosperm hosts that similarly became extinct or significantly reduced in diversity (Gotts- relick, 200l; Labandeira et al., 20072; Ren et al., 2009). Angiosperms and their newfound insect associates diversified considerably after an approximate 25-million-year lag after their origin (Grimaldi, 1999; Crepet, 2008), initially with a comparatively small number of clades but subse- quently increasing to the elevated levels during the Eocene, recorded in the Green River and Florissant formations, Baltic amber, and Messel Lake (Bequaert & Carpenter, 1936; Kusnezov, 1941; Melander, 1949; Lutz, 1993; Wilf et al., 2000; Weitschat & Wichard, 2002; Meyer, 2003; Engel, 2005a; Labandeira et al., 2007b; Michez et al., 2007; Wedmann et al., 2009). Although the family-level analyses of fossil insect diversity by katandan ani epi. us need ha be updated, t Sai 1996; Dmitriev & imei: 2002) indicate that the plateau in the earlier semilogarithmic rise of family-level insect diversity may be real, attributable to a biological event that transformed plant species dominance from gymnosperm to angiosperm. An alternative explanation is that this plateau tiim Annals of the Missouri Botanical Garden a lull in the recovery of insect taxa from earlier deposits with high numbers of insect species. y, taxic data analyses can capture fossil insect diversity data (Sepkoski & Kendrick, 1993), indicating that global biotic c resulted in major decreases in insect diversity. This diversity decrease is wedged between an earlier extinction episode and a subsequent diversification event in seed plants. From the plant fossil record we know that deep- throated flowers did not originate among the earliest lineages of angiosperms, which tend to be bowl- shaped, open, and accessible to a variety of small nonproboscid insects (Friis et al., 1987). The earliest angiosperm flowers indicate pollination predominant- ly by small nonproboscid, large mandibulate, and punch-and-sucking insects (Dilcher, 2000; Laban- deira, 2005a). The earliest deep-throated flowers specialized for long-proboscid insect pollination are of Turonian age (Crepet, 2008), occurring ca. 45 million years after the earliest angiosperm fossils. If iosperms are older, as some molecular phylogenies indicate (Magallón, 2010), it is highly unlikely that they presaged th hies found in deep-throated flowers, particularly given recent work in the different pattern would have occurred if early angiosperms originated from a Caytonia-like ancestor + 2008), in which a Jurassic origin involved long-proboscid pollination. SUMMARY AND CONCLUSIONS This study, partly informed by two related contri- butions that precede it (Labandeira et al., 2007a; Ren et al., 2009), provides the following seven conclu- ns. sio 1. Evidence for pollinator mutualisms. Six lines of evidence are used for establishment of pollinator mutualisms in the fossil record. They are: (1) the structure of insect mouthparts and related head features; (2) the structure of ovulate organs and especially features for Provisioning rewards for insects; (3) the structure of pollen and its placement on plant and insect contact surfaces; (4) palynivore gut contents and dispersed coprolites; (5) the host feeding patterns of insect particular relationshi ip between an insect pollinator and a host plant. 2. The past versus recent spectrum of insect plant associates. There now is more knowledge of . five major lineages brachyceran flies, kalligrammatid neuropterans, and perhaps glossate lepidopterans and caddisflies. Their ` / inferred host plants were corystosperms, pentoxyla- - leans, czekanowskialeans, cheirolepidiaceous coni- | fers, gnetaleans, and caytonialeans. The two major _ trajectories of pollination and related feeding associ- ations—mandibulate versus haustellate insects—de- fine gymnosperm hosts of the mid Mesozoic as wellas | angiosperm hosts of the mid Cretaceous to the present. 3. Opportunism as a key principle in the evolution of pollination and related associations. Recent tests of ` the pollination syndrome hypothesis have failed, 3 rendering use of the concept an uncertain enterprise. ` Instead, the term "pollination mode" is introduced, where the referent is to a common mechanism rather : than to a particular insect clade as the essential : identifier. This suggests an opportunistic pattern of — pollination associations for the Mesozoic fossil record. 4. The long-proboscid, siphonate condition originat- ` lan. ed during the Early Permian. The lesiomorphic, p i ; heuropteran clade, Permithonidae, — pe included a small, fluid-feeding species that bore siphonate mouth boscis of this taxon consisted of conjoined maxillary Palpi that retained segmental divisions and encom- passed a comparatively narrow food canal i > ion for major, mid Mesozoic pollina- "t des. Based on the fossil record, seven distinct pollination modes define the mid Mesozoic, al Parts. The primitive, elongate pro- a Volume 97, Number 4 2010 Labandeira Pollination of Mid Mesozoic Seed Plants mode from the Middle Jurassic to the Early Creta- ceous on a variety of gymnosperm hosts. Most clades of long-proboscid insects ane extinct during the Early Cretaceous, whereas some lineages survived and underwent a host-plant shift onto angios, p- proximately at . A third group of he proboscid insects m on emerging angiosperms during their evolutionary radiation. 7. The importance of the long-proboscid pollination mode for understanding mid Mesozoic fossil plant and insect diversity. First, there has been an expansion of knowledge about the biology of mid Mesozoic insect pollination. In particular, there is greater understand- ing of palynophagy and nectarivory for mandibulate insects and their inferred host plants that bear large unisexual or bisexual strobili. Also, long-proboscid, siphonate insects likely occu a variety of mnospermous hosts with receiving tubular struc- tures. Second, the replacement of the long-proboscid pollination mode, in existence for ca. 65 million years on gymnosperms, by a similar but simpler pollination mode on angiosperms may be related to the origin o the flower and its greater pollinator efficiency. Third, new Mesozoic pollinator data support previous studies on fossil insect diversity during this interval. 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First find of chrysomelids (Insecta: Coleopte era: Cheysonchidea from Callovian—Oxfordian : 865-871 insects. Pp. 33 n A. n “apuy of bns Kluwer Academiis Publishers, ASSEMBLING THE ANGIOSPERM Douglas E. Soltis, Michael J. Moore? TREE OF LIFE: PROGRESS AND J. Cordon ah Charles D. Bell? FUTURE PROSPECTS ME T omela 3. Soli; ABSTRACT th P L 7 TQ U* A +h L L L ] > T » E 3 1 £ Lo r t e o e I ECT o E: A Analyses of large, primarily plastid molecular data sets have revealed new insights into numerous historically contentious hl £ a L 1] 2 s M d E 1 E B Ls an gi rms” r o A +» e r O p I g (not members of either the eudicot lades), among clades of Mesangios; , and 1g maj ts. The same large data sets also have provided evidence for numerous rapid radiations throughout the evolution of angiosperms. The five lineages of Mesangiospermae, as well as most major core eudicot lineages, each likely arose within a narrow range of just a few million years. The rapid radiations i ids (Rosidae) gave rise t angiosperm-dominated fi » Which are also associated with the di ificati f beetles. hemipterans, amphibians. and t t Ongoi hyl i ] now I f going phylog yses now routinely construct phylogenetic hypotheses encompassing thousands of taxa. Such trees enable us to take a broad phylogenetic ive on character evolution, community assembly, and conservation. While the wealth of new sequence data continues to transform the study of angiosperm luti it al t i canada E ERR : acd iE the t and analysis of enormous data se » ts. i Key words: Angiosperm, Asteridae, Caryophyllales, eudicots, Mesangiospermae, monocots, Pentapetalae, phylogeny, A O no J r eo With perhaps 400,000 extant species, the angio- RESOLVING ANGIOSPERM PHYLOGENY sperms represent one of the largest terrestrial radiations. During the past 20 years, contributions Early studies using DNA sequences provided a from paleobotany, phylogenetics, developmental solid phylogenetic framework of angiosperms and biology, and developmental genetics have provided defined the major clades (e.g., Angiosperm Phylogeny new perspectives on the diversification of the Group, 1998; Angiosperm P. hylogeny Group II, 2003; angiosperms. Advances in large-scale genome Angiosperm Phylogeny Group III, 2009; reviewed in sequencing approaches, such as rapid whole-plastid Chase, 2004; Judd & Olmstead, 2004; Soltis & Soltis, genome sequencing via next-generation sequencing 2004; Leebens-Mack et al., 2005; Soltis et al., 2005, technology, have enabled particularly dramatic 2009; Chase et al, 2006; Graham et al., 2006). A progress in resolving plant relationships at deep complete review of this dynamic period is beyond levels. Here, we first highlight improvements in our the scope of this paper, but a few landmark rs understanding of deep-level angiosperm phylogeny. illustrate the rapid progress in angiosperm phyloge- W s robust phylogenetic netics. Ritland and Clegg (1987) first suggested that din de pi the plastid gene rbcL was useful for phylogeny ( n the angiosperms, as reconstruction in ane; — well as to improve estimates of the timing of the the routine use of Din cre iaa in — of the angiosperms and major subclades systematics and evolutionary biology, the first papers i I angiosperms. It is now clear, for example, appeared using rbcL to infer angiosperm phylogeny por A ha characterized by numer- (e.g. Doebley et al., 1990. Soltis e al., 1990). Shortly ae rapi lations, many of which are thereafter, advances in PCR technology enabled a associated with co-diversification events in diverse collaborative f scienti a 500- Essi. Finally, wa soqo. em ins a 1 group of scientists to generate a ; prospects and opportunities for angi : € i M I oe staan slosperm phylo- provided the first broad framework of angiosperm phylogeny. By the late 1990s, other large, collabora- i > epartment of Biology, University of Florida, Gainesville. i ` Biology Departme ment, Oberlin College, Oberlin, Ohio ao. partment of Biological Sci iversi ens es Depa logic: lences, University of New Orleans, New Orleans, Louisiana 70148, U.S.A. Museum of Natural Hi t i : : : doi: 10.3417/2009136 istory, University of Florida. Gainesville, Florida 32611, U.S.A. U.S.A. dsoltis@botany.ufl.edu. ANN. Missouri Bor. GARD. 97: 514-526. PUBLISHED oN 27 DECEMBER 2010 — Volume 97, Number 4 2010 Soltis et al. 515 Assembling the Angiosperm Tree of Life tive ventures ultimately produced 3-gene analyses of 560 oe plant species (Soltis et al., 1999, 2000). xamples illustrate well the central role of lcd collaboration in realizing rapid progress in angiosperm phylogenetics and provide a_ useful template for addressing large-scale questions in the future. Despite the rapid progress of these early studies in defining the major subclades and revealing the basal splits in angiosperm debes t am major subclades remained u . In the past few years, technological epic (o g., next-genera- tion sequencing) have dramatically accelerated the pace of DNA sequencing, permitting the construction of massive data sets involving thousands of nucleo- tides. This rapid and relatively inexpensive sequenc- ing has helped resolve most of the remaining problematic deep-level questions of relationships in flowering plants. Furthermore, these and other technological advances set the stage for t ever larger trees comprising thousands of termi PHYLOGENOMICS In less than four years, nde sequencing technologies (e.g, Roche 454 [Roche, Branford, Connecticut, U.S.A]; [lumina Solexa [Illumina, Inc., an Diego, California, U.S.A.]; and ABI SOLID [Applied Biosystems, Foster City, California, U.S.A. ] have introduced a genomic perspective to phyloge- netics. For example, some investigators are using these technologies for deep transeriptome sequencing, and ressed sequence tags (ESTs) have nuclear genome for deep-level phylogenetic inference (e.g., de la Torre et al., 2006; Sanderson & McMahon, 2007; de la Torre-Barcena et al., 2009). This approach is being employed by the 1KP project (an international pus that will pne Mie" pen for G. K. Wong, vmm ici [PT], Utüvensity of Alberta) as well as the monocot Assembling the Tree of Life project Dus T BA PI, vieni s n re to nd monocots respectively. Although EST sequences generated via next- generation transcriptome sequencing represent a wealth of potential phylogenetic ka this approach also presents challenges for phylogenetic inference. For example, sampling of orthologous gene copies among taxa is not guaranteed; thus, both contig assembly and shylopenetic inference may be ham- pered of ogs. Furthermore, the alignment of short EST fragments typically results in large amounts of missing data, which can complicate phylogenetic analyses (Hartmann & Vision, 2007; Lemmon et al., 2009). Also, high rates of nuclear gene duplication (neludins whole-genome duplications) and loss. as incomplete lineage sorting, can confound dheas inference, creating ee yad ence between € tree and species tree topol (e.g., Maddison, 1997). Despite these nil pitfalls, recent €: suggest that phylogenomic analyses employing EST data can be highly informa- tive in plants (de la Torre et al., 2006; Sanderson & McMahon, 2007; de la Torre-Bárcena et al., 2009; Burleigh et al., in press). Perhaps the biggest impact of next-generation sequencing in angiosperm phylogenetics has been rapid sequencing of complete plastid genomes. The plastid genome has long been the workhorse of plant systematics because of its ease of €— its relative lack of gene duplication an and its wealth of characters (ca. 150,000 bp) bi are m logenetically informative across many taxonomic ration sequencing has astid genome sequencing routine and relatively inexpensive. The — genome is ideally suited for next-generation sequenc ing because of its structural simplicity, highly conserved gene content and arrangement, rarity repeats, and small genomic size (Raubeson & de 2005; Jansen et al., 2005; Moore et al., 2006). Both the Roche 454 and Illumina Solexa sequencers have been successfully used to sequence s genomes (e.g., Moore et al., 2006, 2007; Cronn e ). With rapid technological aio the cost of sequencing a single plastid genome has dropped from o $5000 per plastid genome in initial studies (e.g., Moore et al., 2006) to the point at which $100 to $150 for a complete plastid genome sequence is near at hand. At such low cost, new avenues of research that employ complete plastid genome data are readily affordable, including analyses of phylogeography and deep-level phylogenetic problems. Early studies that employed complete plastid genome sequencing were, by necessity, limited in their taxonomic samp (e.g, Goremykin et al., , and e iha produced erroneous results ser Soltis et al., 2004; Leebens-Mack et e 2005). ee studies of 1 “A s o the methods and assumptions sa stoped nicus and an paid ña insight into many of the vexing deep-level problems in angiosperms. For example, Moore et al. (2007) and Jansen et al. (2007) used complete “awas genome data sets to resolve relati among the major clades of angiosperms, and Moore et al. (201 0) used 516 Annals of the Missouri Botanical Garden complete plastid genome sequencing to resolve relationships among Pentapetalae sensu Cantino et al. (2007); other formal names within angiosperms also follow Cantino et al. (2007). We review these studies below. Mesangiospermae (sensu Cantino et al, 200 consist of five major clades (Magnoliidae, Monocoty- ledoneae, Chloranthaceae, Ceratophyllaceae, and Eudicotyledoneae) and comprise all extant flowering plants other than Amborellaceae, Nym es, and Austrobaileyales. Within Mesangiospermae, Monocot (monocots) and Eudicotyledoneae (eudicots) contain approximately 20% and 75% of all flowering plant species, respectively. Relationships among the five clades of Mesangiospermae have been difficult to determine even with data sets of up to 11 genes (reviewed in Soltis et al., 2005). However, analyses of complete plastid genome sequence data have resolved relationships among clades of Mesan- giospermae and with generally high bootstrap support (Jansen et al., 2007; Moore et al., 2007). Significantly, complete plastid genome sequence data provided strong support for monocots as sister to Ceratophylla- ceae—eudicots (Jansen et al, 2007; Moore et al., 2007). Furthermore, Magnoliidae and Chloranthaceae form a clade (albeit with low support) that is sister to * monocot—Ceratophyllaceae—eudicot clade (Fig. 1). Moore et al. (2007) estimated that the Mesangiosper- mae lineages, which ultimately gave rise to 99% of all extant angiosperm species, appeared in as few as five million years. For perspective, this is comparable in geologic timing to the rapid radiation of species of the o (Baldwin & Sanderson, 1998). Complete plastid genome sequencing has clarified relationships at deep levels within the Pentapetalae, or core eudicots excludi (Moore et al earlier studies failed to resolve subsequent sisters to Asteridae; and Dilleni (Fig. 1). The splitting of these subclades also occurred "a rapidly, again perhaps within five million years. K e Acopio of two major clades of Pentapetalae for understanding patterns of morphological diversi fication. There appear to be morphological features that differ between these two clades that require examination within this new phylogenetic context. For example, perianth zygomorphy and inferior ovaries predominate in the superasterids, whereas actinomor- y an versely, a e n features in the superrosids than super- asterids. Complete sequencing of the slowly evolving plastid inverted repeat (IR) region has emerged as a Jian et al., 2008; Brockington can be easily sequenced using the near-universal angiosperm primers described by Dhingra and Folta (2005). This sequencing approach successfully re- ` solved relationships within Saxifragales (Jian et al., 1 2008) and Rosidae (Wang et al., 2009). For example, . analyses of the Rosidae using the complete IR region supported two large clades, each with 100% bootstrap support, following the divergence of Vitaceae. These clades correspond to (1) the Fabidae, which include the nitrogen-fixing clade, Celastrales, Huaceae, Mal- ` pighiales, Oxalidales, and Zygophyllales, and (2) the alvidae, which include Huerteales, Brassicales, Malvales, and Sapindales, as well as Geraniales, Myrtales, Crossosomatales, and Picramniales. Recently, Moore et al. (in press) constructed a large matrix of IR sequences for over 2 terminals. This tree, with far greater taxon sam ing compared to previous complete plastid genome analyses (above), reveals the same pattern of relation- ships among major clades of eudicots. At this point, the one remaining unresolved deep-level phylogenetic question within eudicots is the placement of Dille- niaceae. Whereas early studies employing one to four genes consistently placed Dilleniaceae with Caryo- Phyllales, albeit with low internal support, analyses of 83 plastid genes (Moore et al., 2010) and IR sequence à (Moore et al, in press) place Dilleniaceae as sister to all or most Pentapetalae (Fig. 2). While the recent abundance of plastid genome data has advanced our understanding of deep-level angio- Sperm relationships, genomic data from the nucleus 1 jeu mitochondria will be necessary to corroborate the E O ñ tic + lvees Because the plastid genome is a single, non-recombin- _ ing locus, evolutionary processes such as introgression d superior ovaries typify superrosids. Con- floral hypanthium and woodiness are more ick | and inexpensive alternative to full plastid genome ` sequencing for deep-level phylogenetic inference (see et al., 2009; Wang et 1 al., 2009; Moore et al., in press). The entire IR region zi XS HORAE Vp idea ode de o NN A A Sot Sol onde ah a quarc pi c e Eu ca eI ll hla Ber dca: gh OS A Rg RP a a Na D eir V t ai A ELA pi eias pce psi y? fue Pi Volume 97, Number 4 Soltis et al. 517 2010 Assembling the Angiosperm Tree of Life $ Fficum | Monocotyledoneae vif Is = @ = O > 5 ° e a o ° @ c Ke] ° 3 o O basal eudicots Crop Magnoliidae mae Chloranthaceae s; Ž 82 — saxifragales Dillenia — 0.01 substitutions/site INSET à F c E Phylogram of the best ML tre iated with branc are ML (seco ipe 1 the lowe rid A: i the phylogram. data to red the effects of h rror. Systematic errors may remain, potentially d in pidenin estimates of phylogeny (e.g., Phillips et al, 2004) Thus, in analyses of plastid genome iie sets, we are now challenged to identify potential biases that may produce error. IMPROVED ESTIMATES OF DIVERGENCE TIMES ng been an interest in using molecular data to date i origin of the angiosperms (reviewed in S) v es ML BS values for the basalmost branches of Pen e eco an analysis of all - pid po and four ribosomal RNA genes 0 dapted from Moore et al., 2010). values. Asterisks widest ML BS = 100%; the inset box in niapet talae, which are too short to visualize in Sanderson et al., 2004). Early cn to estimate the age of the angiosperms p ed highly variable values, ranging from ca. 195 to greater than 400 million years ago (Ma). Most of these early estimates also conflict with the fossil record (see Sanderson & Importantly, more recent efforts to date the origin of the angiosperms have converged on estimates that are between 180 and 140 Ma. Some of these recent estimates are only five to 10 million years older than 518 Annals of the Missouri Botanical Garden —>to superrosids (Fig. 2B) Frankenia Drosophyihix Ximenia a mna E [Dilleniaceae gi a: Ranunculus basal eudicots Limonium bago [Santalales His. : Trachelium 0.04 substitutions/site Figure 2. ML topology derived from genetic algorithm for rapid likelihood inference (GARLI) analysis of all available IR ledoneae. —A i i j sequences in Eudicoty - Overview of topology depicting relationships in basal eudicots relationships among Superrosids. the oldest angiosperm fossils (e.g., Sanderson et al., 2004; Bell et al., 2005; Magallón & Castillo, 2009), although other recent studies have yielded much older estimates, suggesting a possible Triassic or Permian origin of crown angiosperms (Magallón, 2010; Smith et al., 2010). Until recently, the most taxonomically comprehen- sive dating analysis for the angiosperms was per- formed by Wikstróm et al. (2001). These authors, using nonparametric data set of 560 an (inset) showing major clades of Eudicotyledoneae, an lo > Gunnerales, Dilleniaceae, an gr: superasterids. —B. Phylogram depicting provided new estimates of the age of the angiosperms as well as of the major clades of angiosperms. Using 22 calibration points or age constraints and 560-angiosperm data set of Soltis et al. (1999, 2000), Bell et al. (2010) conducted multiple analyses clock methodology that does not assume any correla- tion between rates, thus accounting for the potential of lineage-specific rate heterogeneity. In one set of BEAST analyses based on 36 fossil constraints, Bell et al. (2010) obtained an estimated f the angiosperms of 199-167 Ma, which is still older than the age of the oldest known fossils (132 Ma; Hughes, 1994). These results, as well as other recent dating studies, suggest a Late Jurassic to Early Cretaceous angiosperms (e.g., Sanderson al., 2005). However, other recent studies suggest an £ [2 . even ald IM cn lA o > — T seplLisjsy addas e a asa m Mi Volume 97, Number 4 2010 Soltis et al. 519 Assembling the Angiosperm Tree of Life aepisoy phn i : Eyasi | Vitaceae —> to remainder of tree (Fig. 2A) Figure 2. Continued. 2010; Smith et al., 2010). Hence, these molecular estimates indicate that angiosperm fossils older than those discovered to date may exist and are awaiting discovery. Bell et al. (2010) also obtained the following age estimates for major angiosperm clades: Mesangiospermae (156-139 Ma); Gunneridae (core eudicots; 139-109 Ma); Rosidae (132-118 Ma); Asteridae (119-101 Ma) (Fig. 3). A more complete set of divergence times is given in Table 1. Significantly, recent topologies (above) as well as these recent studies of divergence times also provide insights into Darwin's abominable mystery—the rapid rise and early diversification of the angiosperms. Both tree topologies and estimated dates of divergence suggest not just one or a few major radiations in the angiosperms, but many successive rapid radiations. For example, a series of recent studies, many based on complete plastid genome data sets, indicate rapid radiations ughout the diversification of major Eroups of angiosperms, including the lineages of — v— . o. +>ə . Dx n nT Mesangiospermae (Jansen et al., 2007; Moore et al., 2007), the lineages of Pentapetalae (Moore et al., 2010), and within subclades of core eudicots, such as Rosidae (Wang et al., 2009) and Saxifragales (Jian et al., 2008). ThE RISE OF ANGIOSPERM-DOMINATED FORESTS AND ASSOCIATED CODIVERSIFICATION EVENTS Plastid phylogenomics revealed that Rosidae are divided into the Malvidae and Fabidae clades and split rapidly into several major lineages over a period of less than 15 million years, perhaps as quickly as four to five million years (Wang et al, 2009) Estimates for the age of crown group Rosidae ranged from 115-93 Ma (Late Aptian to Early Turonian), in the Early to Late Cretaceous, followed by rapid diversification into the Fabidae and Malvidae crown ups around 112-91 Ma (Albian to Coniacian) and 109-83 Ma (Cenomanian to Santonian), respectively Annals of the Missouri Botanical Garden ÓN Figure 3. Summary ch g lepicting di g 567-taxon data set from Bell et al. (2010). Node d pth estimated with BEAST. (Wang et al., 2009). These estimates of the timing of the rapid diversification of these rosid lineages are comparable to published values based estimates from broad angiosperm surveys (Wikstróm et al., 2001; Davies et al., 2004; Magallón & Castillo, 2009; Bell et al., 2010). For example, Wikstrém et al. (2001) provided an estimate of 117-108 Ma (their node 15), and Davies et al. (2004) estimated ca. 115- 110 Ma. Wang et al. (2009) proposed that the bursts in diversification within the rosids correspond to the d ated E ra a f. C 1987; Upchurch & Wolfe, 1993). In fact, woodiness i. particularly prevalent within the rosid clade. Families timated by BEAST using the 3-gene, IE L 95% : r A ity in the Fabidae include most of our temperate, as well as many tropical, trees (e.g., Betulaceae, Casuarina- ceae, Clusiaceae, Euphorbiaceae, Fabaceae, Faga- ceae, Juglandaceae, Moraceae, Ochnaceae, Rhizo- Phoraceae, Rosaceae, Salicaceae, and Ulmaceae). The Malvidae include a number of subclades with important forest trees, such as subclades representing Malvales, Sapindales, Brassicales, and Myrtales. Malvales and Sapindales comprise key tropical forest elements, including Rutaceae, Meliaceae, Sapinda- ceae, Simaroubaceae (Sapindales), and Malvaceae and Dipterocarpaceae (Malvales). Myrtales also — comprise important forest elements in the families Myrtaceae, Melastomataceae, and Combretaceae. i i i | | Volume 97, Number 4 Soltis et al. 521 Assembling the Angiosperm Tree of Life Table 1. Estimat lad Clade numbers ref bered nodes in fi rom Bell al. me P fien clades that ha have been — we have pace clade names tas cuba Cantino « “ 2 par or 36 Jail epusirsinas (ses Bell et sl e model and Clade Wikstróm et al. (2001) BEAST 1 Angiospermae 158-179 183 (167-199) 2 153-171 173 (160-187) 3 Mesangiospermae . 146 (139-156) 4 E 140 (128-140) 5 Magnoliidae 122-132 122 (108-138) 6 127-134 119 (100-138) 7 108-113 118 (107-133) 8 140-155 156 (146-168) 9 Eudicotyledoneae 131-147 130 (123-139) 10 130-144 129 (116-143) 11 128-140 125 (110-138) 12 124-137 134 (120-145) 13 23-1 127 (109-139) 14 nneri 116-127 127 (109-139) 15 Pentapetalae 114-124 121 (111-124) 16 104-111 120 (112-131) 17 106-114 121 (113-129) 18 * 114 (107-122) 19 Asteridae 102-112 110 (101-119) 20 14-1 108 (99-116) 21 Core asterids 107-117 100 (92-109) 22 Superrosids 111-121 128 (120-135) 23 Rosidae 108-117 125 (118-132) 24 95-101 116 (108-121) * Node not compatible with inferred tree. The diversification of rosids is closely congruent in geologic time with a number of other major diversi- fication events. For example, the diversification of major ant lineages is attributed to the “rise in angiosperm-dominated forests" (Moreau et al., 2006: 103) and corresponds to the time period estimated here for the rosid radiation. This time period also corresponds to the radiation of other major herbivores, such as beetles and hemipterans (Farrell, 1998; Wilf et al, 2000). Diversification in amphibians is estimated to have occurred slightly later (85-80 Ma), although it is similarly attributed to the rise of — forests (Roelants et al., 2007)—in fact, 82% oe species live in forests. The mta of living ferns similarly resulted from a Cretaceous divenifeaióoá (initiated ca. 100 Ma) coupled with the rise of angiosperm forests; diver- gence time estimates eet that ferns diversified "in wo rms” (Schneider et al., arly, dies sija splits underlying the deron of the extant lineages of placental occurred in a id time frame, from 1 85 Ma (Bininds-Emonds et al., 2007). The rise of all of these lineages appears to have closely tracked the .. fise of angiosperm-dominated forests. Most of these key forest lineages occur within the n Hence, the radiations detected in Rosidae largely represent the rapid rise of angiosperm-dominated uk and associated codiversification events that have pro- foundly shaped much of the current terrestrial biodiversity (Wang et al., 2009). ROUTINE SEQUENCING OF COMPLETE NUCLEAR GENOMES Next-generation sequencing has made it possible to sequence the entire nuclear genome much more rapidly and inexpensively than just a few years ago. pe such comprehensive sequencing of angiosperm omes has been limited mostly to crops and model ane (e.g., Arabidopsis thaliana (L.) Heynh. [Arabi- is Genome Initiative, 2000], Oryza sativa L. [International Genome Sequencing Project, 2005], Vitis vinifera L. [Jaillon et al., 2007; Ve lasco et al., 2007], Carica papaya L. [Ming et al, 2008]. However, as nuclear genome sequenc ing becomes increasingly routine and cost-effective, ae is important to consider which nuclear genomes to sequence. A broad phylogenetic perspective is crucial in the study of genome evolution, and this can best be obtained via the acquisition and analysis of a phylogenetically a Annals of the Missouri Botanical Garden diverse sampling of genomes. Thus, we should identify un patterns of genome evolution in plants (see Pryer et al., 2002; Soltis et al., 2008). One such phylogenetically pivotal angiosperm is Amborella trichopoda Baill, the sister to all other extant angiosperms (e.g. Soltis et al, 1999, 2000; Leebens-Mack et al., 2005; Jansen et al., 2007; Moore et al., 2007). B ll angiosp lear g sequenced to date have been either monocots or eudicots, obtaining the nuclear genome sequence of Amborella will be crucial for providing a better understanding of the processes shaping genome and gene evolution on a broad scale across the flowering plants, as well as a better understanding of the many similarities and differences between model monocot and eudicot plants. A complete nuclear genome sequence of A. trichopoda will therefore be an exceptional resource for plant genomics (Soltis et al., 2008) in much the same way as the nuclear genome sequence of the platypus (as sister to other mammals) was a crucial resource for mammals (Warren et al., 2008). Ultimately, complete nuclear genome sequences of other “basal angiosperms” will also be important. Comparing the nuclear genomes of Amborella with those of other “basal angiosperms,” monocots, and eudicots would be of enormous value in helping to reconstruct genome and morphological evolution in early angiosperms. For example, many y angiosperm features, such as the flower and accompanying diverse pollination systems, double fertilization, vessel elements, diverse biochemical pathways, and many of the specific genes that regulate key growth and developmental processes, first ap- among the descendants of the first splits in angiosperm phylogeny (e.g., Soltis et al., 2005, 2008). or similar reasons, the nuclear genome of Aquilegia formosa Fisch. ex DC. (Ranunculaceae) is being sequenced. Aquilegia L. is a member of Ranunculales, a clade that is sister to all other eudicots; consequently, this genome sequence will be an important evolutionary reference for all eudicots. Aquilegia has also been used in studies of pollination, mating system evolution, floral development, and adaptive radiation (Kramer, 2009), so a complete nuclear genome sequence will provide a wealth of "oda t the genomes of taxa that are sister to all other liuesqes within each major clade of angiosperms, for example, in idae, superrosids, superasterids, as well as Rosidae, Asteridae, and Caryophyllales. Perhaps one of the most important nuclear genomes to sequence based on its phylogenetic position is that of Gunnera L. (Gunneraceae), a member of Gunnerales, the clade that is sister to all other Gunneridae. Ultimately, a nuclear genome sequence for at least one represen- 1 tative of each of the major angiosperm clades (perhaps using the 59 orders sensu Angiosperm Phylogeny Group III as a guide) would provide a broad suite of informative reference genomes for phylogenetically use in plant biology TowarD A GREEN PLANT TREE OF LIFE The availability of DNA sequences from thousands of taxa across a broad phylogenetic spectrum has it dios t truct phylogenet that encompass much of the species diversity of green life. During just the past three years, phylogenetic analyses that include thousands or tens of thousands of species have become increasingly common (e.g., Bininda-Emonds et al., 2007; Goloboff et al., 2009; | Smith et al., 2009). Establishing such a broad framework of evolutionary relationships across not only green plants, but all of life, will have profound implications for how we study many areas of biology. . Considering just the green plants, a phylogenetic inni new insights for underpinning can yield important comparative genomics and molecular evolution, developmental genetics, the study of adaptation, speciation, community asse ly, and even ecosystem structure and function that are not possible with smaller trees. A series of recent studies has demonstrated the plants in relationship to plant life history (Smith € Donoghue, 2008) and have helped elucidate patterns ` of biodiversity in the flora of South Africa (Forest et 2 g. - 2007). Large trees may also help predict responses success of potential biological invasions (e.g., Strauss et al., 2006; Proches et al., 2008). Several studies also. illustrate an important new trend in tree-building studies. Although systematists typically think in terms of building trees for a particular clade, this research — illustrates the value of building big trees for all of the t taxa in a given geographic area (e.g., Webb et — ; Kraft al, 2002; et al., 2007; Wright et al., 2007; Cavender-Bares et al., 2009; Vamosi et al., 2009). Several approaches have been used to build these comprehensive trees, including supertree methods, — ined smaller phylogenetic trees into a which combined single, compreh p. ds, 2004); a supermatrix approach, which infers trees from con- ic hypotheses Volume 97, Number 4 2010 Soltis et al. Assembling the Angiosperm Tree of Life catenated alignments of genes with partial taxonomic overlap (de Queiroz & Gatesy, 2007; Smith & ) and a hybrid megaphylogeny of approach included up to 4600 species (e.g., Kallersjé et al., 1999; McMahon & Sanderson, 2006; Smith & Donoghue, 2008). Howev- er, more recent studies have analyzed supermatrices with more than 10 times as many taxa. Illustrating the recent trend to build much larger trees, a parsimony analysis of 73,000 eukaryote taxa was recently qu (Goloboff et al., 2009), and ML analyses 3,000 (Smith et x. 2009) and ca. 19,000 uiid. in ee plant sequences have also been n larger plant trees are on the ei Seas et ont n prep.) are analyzing a 50,000-tax data set for green plants. Still, while the size of e trees is impressive, ultimately the use of these trees — on race quality. In large part, this has yet to be ass po the funding of the iPlant Tree of Life (iPToL) project through the National Science Foun- dation (NSF)-funded iPlant Collaborative affords the opportunity to address the grand challenge of constructing, analyzing, and navigating the green plant tree of life. The project will provide tools for the systematics community and a cyberinfrastructure to construct, navigate, and employ big trees. For example, character-state reconstruction and gene- tree/species-tree reconciliation methods cannot now be implemented on large trees; earl will be to scale up and build these and other tools that can be employed on large trees. Such tools will be of broad benefit to the plant biology community. The systematics community is now in position to take a true “moon shot”: iPToL will attempt to build the infrastructure for reconstructing a comprehensive phylogeny of green plants, first for 100,000 species in phylogenetic studies resulted directly from coopera- tion of many plant systematists, this new scale of plant phylogenetic inference is a direct result of the coordinated and collaborative efforts of plant system- atists with computer scientists and computational biologists. However, tools alone will not be enough to complete challenge successfully. Only ca. 75,000 plant taxa are now represented in GenBank, and many of these sequences are fragmentary. To realize a complete green tree of life will consequently require a vast amount of additional sequence data, as well as ment on a set of gene regions to be sequenced for all plants and/or genomic approaches that make it possible to sari sequence large numbers of gene regions on a large phylogenetic scale. Literature Cited Angiosperm Phylogeny Group. 1998. An ordinal classifica- +: f, aL £ spe £f s 1] Ann Mi " . Gard. 85: 53 : rem ind Group II. 2003. An update of the Angiosperm Phylogeny Group classification for the orders and families of flowering plants. Bot. J. Linn. Soc. 141: 399-436. Angiosperm Phylogeny Group III. 2009. An update of the Angiosperm Phylogeny Group classification for the orders and families , eren plants: APGIII. Bot. J. Linn. Soc. , 16k: 105-12 l 2 sequence of the ew plant C thaliana. Nature 408: 796-8 Baldwin, B. G. & ee 1998. Age and rate of diversification of the Hawaiian silversword alliance Proc. Natl. Acad. Sci. U.S.A. 95: Bell, C. D., D. E. Soltis & P. S. 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Ti I radiations of leaf beetles: Hispines on gingers from Wright, Lk D. D. Ackeily, F. Bongers, K. E Harms, Ibarra-Manriquez, M. Martinez-Ramos, S. J. Mazer, H. C. | Muller-Landau, H. Paz, N. C. A. Pitman, L. Poorter, M. Silman, C. F. Vriesendorp, C. O. Webb, M. Westoby & S. J. Wright. 2007. Relationships among ecologically impor- tant dimensions of plant trait variation in seven neotrop- ical forests. Ann. Bot. (Oxford) 99: 1003-1015. ANGIOSPERMS HELPED PUT THE C. Kevin Boyce,? Jung-Eun Lee,? Taylor S. Feild,? RAIN IN THE RAINFORESTS: THE. Zim J. Brodribb,* and Maciej A. Zwieniecki> IMPACT OF PLANT PHYSIOLOGICAL EVOLUTION ON TROPICAL BIODIVERSITY! ABSTRACT The recycling of € water is well known to be an important source of rainfall, particularly in the tropics, angios ve transpira! and rise to ecological y caco of flow wering plants closely correlated with leaf vein density other and capacities higher than any other plants throughout evolutionary history. Thus, the evolution MPO to have strongly altered climate. n n cal] pacity is ity plants, esa: h. or extinct. A rapid Trónisition w n vein densities occurred | separately i in three. or more flowering plant TS a ago. lineages about 100 would be hotter, duck in more seasonal in the ab decline substantially. Because angiosperm diversity i is influenced. by rainforest area and by simis partially a produ evenness, the ne TA of angiosperms is initiated by anon eo Tuta sn in the wake of the angiosperm radiation may be tied ë "he unprecedented im on climate RESUMEN Í +h , and the overall ical rainforest would ertebrate and invertebrate animals and pact of angiosperms u ee de agua transpirada es bien , conocida por ser una importante fuente de precipitscwoen, especialmente en el , y los p p g , se propone que la evolución ye el de angiosp p ón de d ecológica ha alterado fuert te el clima. La a£ à t£ "n 1 » 3 1 ] 2 2 8 1 2 7 | J f 4 d 1 d Se de las h hojas angiospérmicas es es cuatro veces mayor que - resto de plantas, vivas o cing Haoe unos 100 iiem ie id afios tuvo "our de f. rápida ón hacia altas dens idades v. en tres o más linajes de angiospermas. La tela el dioi del impacto e esta revolución fisiológica Ls que los p serían más ee secos, y más estacionales sin los angi Aa, con una aoe reducción sustancial de las á áreas de selva -e angiospermas, peere a que ‘la Seeded de ae. y regularidad vertebrados e invertebrados y paraa no IE en pos de la radiación angiospérmi impacto sin precedentes de los angios el clima. ialment te los jospermas es facilitada por el área de selva lluviosa y por la de precipitaciones. La diversificación de un número significativo de linajes entre animales ca podría ser el resultado del as sobre Climate, hydraulics, bud precipitation, transpiration, venation. The geographic extent of the moist tropics has varied considerably (Ziegler et al, 2003) over the approximately 380 million years since vascular plants the first forests (Algeo & Scheckler, 1998; Stein et al, 2007). During the Carboniferous, vast areas of tropical Euramerica were covered with wet, peat-forming forests, although they were subject to rapid contractions and expansions with replacement millennial-scale glacial cycling (Montafiez et al., 2007; Falcon-Lang et al., 2009). With the transition to a hothouse climatic regime during the Permian, seasonally dry conditions spread throughout the nah-like Panini and everwet conditions were limited to isl an areas of continents enm with tropics to produce more savan narrow coastal significant maritime precipitation (Ziegler et al., ). Predominance of rainfall seasonality and by more seasonally dry vegetation in association with 1 We thank Peter Stevens for his encouragement of this work and invitation to contribute to this symposium. This study is supported in part by the the Australian Research Council (T.J. * Departme School of Biological Sciences, Monash University, x ‘Departmen t of Plant Sciences, University "of Tasman ` Arnold Arboretum of Harvard doi: 10.3417/2009143 National Science Foundation (J.E.L., T.S.F.), Canadian Institute for Advanced Research (J.E.L.), and nt of the Geophysical Sinus: i of pv Chicago, gp = U.S.A. ckboyce@uchicago.edu. e, Victoria 3800, A ae. Tasmania 7001, Rocce University, Jamaica Plain, Massachusetts 02130, U.S.A. Ann. Missouri Bor. GArD. 97: 527-540. PUBLISHED ON 27 DECEMBER 2010. 528 Annals of the Missouri Botanical Garden tropical aridity persisted through most of the M modern tropical rainforests provide further support for. I until the expansion of high precipitation conditions beginning in the early Late Cretaceous and reaching a maximum extent in the Eocene (Parrish et al., 1982; Parrish, 1987; Upchurch & Wolfe, 1987; Vakhra- meev, 1991; Morley, 2000; Beerling & Woodward, 2001; Ziegler et al., 2003; Ufnar et al., 2008). The early diversification of angiosperms accompa- nied the expansion of tropical wet climates during the Cretaceous and Paleogene (Bumham & Johnson, 2004; Crepet, 2008; Feild et al., 2009). However, the exact timing of the origin of angiosperm-dominated tropical rainforests of modern aspect is debated (Upchurch & Wolfe, 1987; Morley, 2000; Burnham & Johnson, 2004; Davis et al., 2005; Wing et al., 2009). Evidence for megathermal angiosperm rainforests in the Paleocene (Johnson & Ellis, 2002; Wing et al., 2009), but Cretaceous evidence is mixed. This problem persists, in part, because macrofossil records are extremely scarce in the modern tropics (Burnham & Johnson, 2004; Wing et al., 2009). Furthermore, interpretation can be ambiguous for the more frequently available evidence from microfossils, climate-sensitive sedi- ments, geochemistry, climate modeling, and inference from living plants. However, climate-sensitive sedi- ments and modeling support at least local persistence of environmental conditions compatible with growth of megathermal rainforests at tropical and/or temperate latitudes during the Cretaceous (Parrish et al., 1982; Barron & Washington, 1985; Parrish, 1987; Upchurch et al., 1999; Beerling & Woodward, 2001; Ziegler et al., 2003; Ufnar et al., 2008). Nonetheless, most paleobo- tanical macrofossil studies suggest that the establish- ment of angiosperm rainforests was delayed until the oiy Tertiary, based on the paucity of wood indicative closed-canopy environments in the Cosiaccaue (Tiff- ney, 1984; Wheeler & Baas, 1991; Wing & Boucher, 1998). This paleobotanical evidence i licated b the leaf physi . EA localities suggesting warm, wet forests as early as the Cenomanian about 100 million years ago (Upchurch & Wolfe, 1987) and by recent arguments that large seed size is an advantage for germination in deep shade rather than a requirement (reviewed in Feild et al. 2004; Davis et al., 2005). Palynofloras indicate highly diverse tropical forests by the Eocene (Jarami limited to that envir í - 1 I ( in Morley, 2000) have been questioned (reviewed in Wing et d: Molecular clock estimates for the antiquity of 9). Sperm lineages found in the shaded understory of a mid-Cretaceous origin (Davis et al., 2005), although concerns over molecular calibrations persist among paleontologists (Burnham & Johnson, 2004; Wing al . On positive evidence for angiosperm rainforests in the taceous, but neither is there evidence for their complete absence. As discussed below, perhaps the 1989) and basal extant angios are highly ` intolerant of drought (Sperry et al., 2007; Feild et al, — 2009). Tropical rainforests have the highest biodiversity of — any ecosystem, housing more than half of all species, despite occupying less than 7% of Earth's surface (Bierregaard et al., 1992; Wilson, 1994). The niche specialization necessary for such high diversity is | promoted by the high productivity of tropical rain- forests, the dense stratification of their vegetation, and m their coverage of a large and heterogeneous area (Grubb, 1977; Ricklefs, 1977, 2004; Leigh et al, 2004). The stability of rainforest climate then allows | E that potential for specialization to be reached, and ` specialist herbivores and pathogens further promote — diversity by suppressing the emergence of dominant — species (Janzen, 1970; Givnish, 1999). Alternatively, if trophically similar species are considered inter- 2 they promote tropical diversity through the creation of a cradle of high species origination rates or a museum of low extinction rates (Givnish, 1999; Hubbell, 2001; Condit et al., 2002: Leigh et al., 2004; Ricklefs, 2004; will emphasize that, just as tropical climate has strongly influenced biotic evolution, the opposite is So true—evolution, of angiosperms in particular, has strongly influenced tropical climate. Tur EvoLurion or Lear HYDRAULICS THE SIGNIFICANCE OF LEAF VEIN DENSITY As vascular plants absorb carbon dioxide (CO) from the | for photosynthesis, they lose water to the atmosphere through transpiration. If leaf Volume 97, Number 4 2010 ce et al. Plant Physiological Evolution and Tropical Biodiversity water is lost faster than it can be replaced by the vascular system, then leaf tissues desiccate. The development of a water deficit in the leaf triggers the closure of the stomatal pores through which leaf gas e occurs in order to limit further water loss and a plant's ability to conduct photosynthesis is dependent on its ability to transport water to the stomata for transpirational loss (Davidoff € Hanks, 1989; B 5 ). Replacing transpired water in leaves requires xylem to transport water efficiently from the soil to the sites of evaporation. Xylem allows mass flow of water through conduits composed of the walls of dead cells, avoiding the slower diffusion through living cells. However, leaf tissue retains a non-xylem hydraulic pathway from the ends of veins to the sites of evaporation, and this short pathway involving living tissue constitutes a major resistance to hydraulic flow. Indeed, a third or more of the total resistance from root to stem to leaf to atmosphere is concentrated in the last few centimeters of that transport pathway represented by the leaf (Sack & Holbrook, 2006; Brodribb et al., 2007). Thus, any anatomical change that decreases the transportation path length through the leaf mesophyll tissue will have a substantial impact on the hydraulic resistance of the entire plant. The most direct way to shorten the distance between leaf xylem and stomata through the meso- phyll is to increase the density of leaf veins. As a result, plants with higher leaf vein density iid have higher assimilation and transpiration rates—a expectation that has been demonstrated across an ecologically and phylogenetically diverse array of ascular plants (Brodribb et al., 2007; Boyce et al., 2009; Brodribb & Feild, 2010; Fig. 1A). In addition to the functional significance of leaf vein density, there is a practical application for the study of physiological evolution. Vein density is rom many traits that would otherwise be unavailable from fossil organisms. For example, assuming that fossil cycads had low assimilation rates to match the slow growth of extant cycads would be dangerous because the modern taxa have been marginalized by the ecological expansion of angi rms. Hence, extinct cycads may have had a greater diversity of ecologies, growth habits, and growth rates (Wing & Sues, 1992). However, all leaf vein density measurements in fossil cycads haye been equally as low as the extant forms, thereby providing a functional basis for the interpre- tation of low primary productivity throughout their evolutionary history (Boyce, 2008). EVOLUTION OF LEAF VEIN DENSITY Paleozoic origins and later history of nonangiosperms Laminate leaves are common among euphyl- ophyte vascular eem but are not all ladies cdot Kenrick & Crane, 1997; emote 2008; Days; 2010). Leaf laminae evolved Emp at least four times within the seed pt archaeopterid progymnosperms, ferns, and horsetail- chia Simca ad the number could be significantly higher given the possibility of separate origins in ophioglossoid, marattioid, and leptosporan- giate ferns and in minor fossil a of enigmatic a inis the Noeggerathiales (Boyce & Knoll, 002). te multiple origins, e densities of veins in E lon are nearly uniform (Fig. 1B). The vein density of the db Devonian and Carboniferous leaf fossils averages between 2 and 3 mm mm ? and rarely ranges beyond 1—4 mm mm ? (leaf vein density is measured as the length of vein [mm] per area of leaf [mm?] [Boyce et al., 2009]. The leaf vein density of nonangiosperms has remained extremely consistent, with the mean value for any time interval never reaching higher than the 2.8 mm mm ? of the Pennsylvanian or lower than the 1.8 mm mm? of the modern world (Fig. 2). This uniformity is in itself remarkable given the extreme variations in climate regime, paleogeography, and atmospheric composition over the same time period. Finer ‘ilies and stratigraphic sampling is need there are no hias vein — — hothouse diisi nn earth history (Fig. 2), as might be expected from the presence of both high and low vein Bear in a PME ud modern dii regim and ibus CO, ¿onecritration (Uhl & Mite ger, 1999; es a is more pees. CO» concentra- and a grea ter "n" US SU sensitivity w vein au win has n predicted low ° ^ decisio rate on stomatal donde (Brodribb & Feild, 2010). A CO; driver has been suggested for me vein density fluctuations at a fine stratigraphic eii (Retallack, 2005), but average vein density among nonangiosperms has remained re ly flat through longer time scales even as CO, concentrations have fluctuated over an order of magnitude and stomatal densities have responded with fluctuations over almost three orders of magnitude (Fig. 2). z Angiosperms Averaging near 2 mm mm ° and almost never reaching above 6 mm mm °, the uniformity of vein 530 Annals of the 1 Missouri Botanical Garden A = 08 š s: 52 0.4 $ B *Fems" 3g o 43) ake ar um ar (n ELI ü n am m am ee Í um abe ace t EL im a ARE LLL Ü dm E ae ee d Figure l. Leaf vein densi i. b 1 maximum onde d d n — Empirically derived relationship between leaf vein density and (Boyce et al., 2009). —B. Distribution of leaf vem dense are s ri te Piaton under standard atmospheric conditions — ~ im tw ¿Ë Leu: a i pr lies among seed plants, one or more independent evolutions among imum t 3 : E N hial ivocal) hi ds "o e vein density (white line) and median 50% of values (d ike Mad. es de p: values compiled from Boyce et al (2000) en lineage indicating the number of tne mle) Vein density liekana A De E n Brodribb and Feild (2010) with some supplementation (Retallack, 2005; density among nonangi ORG years and multiple leaf originations would men bee, ol extant angiosperm phylogeny, including single hydraulic optimum for leaf c K emo Amborella Baill, Nymphaeales, Austrobaileyales, which all early lineages converged and to which all - he common ancestor of the Chloranthales, later generations adhered. Such a conclusi magnoliids, and eudicots, possess vein densities that nable based on all plant life as oe can be moderately high (4-5 mm mm-?), but within Early Cretaceous, but since then = the range of ferns and nonangiospermous seed plants lished a mean above 8 mm mm”? and ° (Boyce et al., 2009; Brodribb & Feild, 2010). High | reached densities higher than 24 dn have vein densities greater than 9 mm mm? ins ar to have © et al., 2009). O. ieved by some derived magnoliids (e.g. — High vein density is not a characteristic Nees at 152 ° e à; i ' : i mm mm 2), monocots angiosperms as a whole (Fig. 1B). Lineages a the (eg, Hyparrhenia Andersson ex F. Fourn. at 113 Me 85 E and eudicots (e.g., species of Populus L. i ; i i I ———— ————— see ————————" Volume 97, Number 4 2010 Boyce e Plant Physiological Evolution and Tropical Biodiversity Pangea Coldintervals HS EN | 6000 8 pa 58 Š 2000 š oo, > | ; es” 100 . me. Fit Ti «EH 101 > E 1 23 ii * 0.1 >— it 10 cE $E 5 bodies l 0 400 300 200 100 0 Millions of years ago pte : M leaf vein asiy through time among rms (c ipis circles) and angiosperms (open 208 s with stomatal uri ties and extrinsic run that could poten atially influence leaf evolution and h lies, including ro G (Scotese, 2004), cold bine (Royer et al., 2004), and the range of potential atmospheric C0; Ob Soma des through time (Berner & Kothavala, i à Wolf, 1 1975; Reena & Schabsliow; 1978; Batenburg, 1981; anner & Kapos, 1982; Sugden, 1985; Pigg, 1990; Rolleri et al., 1991; Knapp, 1993; Pigg & Taylor, 1993; McElwain & Woodward, 1997; , 1998; McElwain et al., 1999; Chen et al., 2001; Liu & Yao, 2002; Hesselbo et al., 2003; Yao & Liu, 2004; Krings et al., 2005). ranging from 9.0 to 23.3 mm mm 2) independently (Boyce et al., 2009; Brodribb & Feild, 2010). These evolutionary transitions to high vein densities appear to have occurred around ibb & Feild, 2010), coinciding with the explosive radiation of the rosids (Wang e ich possess many of the highest vein deis: Even among derived eudicots, angiosperm evolution represents an increase in the upper bound of leaf vein densities, not a wholesale departure from low values (Fig. 1B). mao, low idee in the range of 1- mm ? are found among derived angiosperms only in thick-leaved, drought-adapted succulents (e.g., Crassula L. at 0.4 mm mm ° or — aa at 0.7 mm mm *; Noblin et al., 2008), p radically different morphology than the hile ferns for which such values are also commo IMPACT OF ANGIOSPERMS ON CLIMATE The contribution of re-evaporated moisture, also termed “recycling,” is important in feeding precipi- tation in forested regions (Salati et al., 1979; Eltahir & Bras, 1996). Recycled water moistens the atmospheric boundary layer—typically from the surface to a height of 1 km—and can decrease atmospheric stability (Fu et al., 1999), causing convective rainfall. Soil moisture status, which is determinant of evapotranspiration rates in DREAS terrestrial environments, has been studied as a possible indicator for forecasting precipitation. Summer precipitation has been shown to be sensitive to late spring to early summer soil moisture content from studies using a unique network of soil mo nts Illinois, U.S.A. (Findell & Ehtshir, 1997; 7; D'Odorico & Porporato, 2004). Doc increases have also been observed in response to the increased evapo transpiration associated with crop Ln (Stidd, 1975). The changes in plant physiology heralded by greatly increased leaf vein density suggest that the radiation of angiosperms was accompan ied by more than a doubling of photosynthetic capacity (Brodribb & Feild, 2010) and approximately a fourfold increase in transpirational capacity (Boyce et al., 2009) on a leaf area basis. The impact of these changes on the global carbon and hydrologic cycles is likely to have been profound. Because the recycling of rainfall through evapotranspiration can be an important contributor to precipitation, any increase in transpi- ration capacities that accompanied angiosperm evo- lution should strongly influence climate, particularly in the tropics and during the growing season at higher latitudes. Of course, the Intertropical Convergence least seasonally high precipitation, orographic rainfall can be significant on the win ndward side of mountain proximity to large bodies of water can also feed jtih However, transpiration represents an important addition to these physical processes. use direct quantification of recycling requires the irc task of distinguishing different water sources (Salati et al., 1979), climate models have long Annals of the > Missouri Botanical Garden Figure 3. Climate modeli g of the diff i rld with angiosp lative to a world without them (Boyce & Lee, 2010; Lee & Boyce, in press). Absence of angiosperms was simulated by a 75% reduction in tran factors were held as fixed at modern values, includi day is defined as one with at least 3 mm of precipi been used to estimate the influence of land evapo- transpiration on precipitation. These studies show that recycling is greater during the growing season e.g., Koster et al., 1986; Lee, 2005) and that the observed precipitation response to soil moisture is indeed related to the atmospheric response to the added evapotranspiration (Findell & Eltahir, 2003). Regions where precipitation is dependent on soil-moisture status coincide with areas with a large recycling ratio (Koster et al., 2004; Dirmeyer et al., 2009). How important the evolution of angi transpiration capacities might have been can be similarly con- strained with climate modeling. CASE STUDY OF THE MODERN WORLD coupling atmospheric and land models, biomass was held constant and the only change imposed on the piration rates. All other ng sea surface temperatures, geography, and vegetative biomass. A rainy tation. modern system was a drop of maximum transpiration rate by a factor of four (Boyce & Lee, 2010; Lee Boyce, in press). In these simulations, the impact of angiosperm transpiration is large and widespread (Boyce & Lee, 2010; Fig. 3. The most dramatic effects are seen in the tropies, which are drier, hotter, and more seasonal in the absence of angiosperms. Although higher-latitude precipitation effects are dwarfed by the tropics in absolute terms, they can still be proportionally large (Boyce & Lee, 2010). The influence of transpiration on climate is largest in South America (Boyce & Lee, 2010; Lee & Boyce, in press) where the projected loss in annual rainfall in the absence of angiosperms can be greater than 1500 mm per year. This decline involves both less Precipitation every month of the year and greater seasonality, with the dry season extending 80 days longer over the eastern Amazon Basin. This is significant given the high sensitivity of rainforest and lianas to drought (van Nieuwstadt & Sheil, Volume 97, Number 4 2010 Boyce et al. Plant Physiological Evolution and Tropical odian Together, these effects result in a reduction to one fifth in total everwet rainforest area without angio- sperm transpiration, as defined as areas with 240 wet days or more per year (Boyce & Lee, 2010). Because evaporation entails the transfer of large amounts of energy from sensible to latent heat (Lee et al., 2005), angiosperm transpiration also exerts a strong cooling effect with temperatures seasonally up to 5°C warmer in their absence. The lesser impact on precipitation seen in South- east Asia and Malesia and in Africa (Fig. 3) highlights that elevated transpiration is an addition to a system that is still largely governed by physical parameters. ximity to the sea that precipitati i abundant throughout much of Southeast Asia and Malesia regardless of transpiration rates. Conversely, unusually high topography keeps Africa drier and more seasonal and confines rainforest development to the west (Ziegler et al., 2003). These effects are dependent on orogeny and continental configurations that are in constant flux—the East African Plateau, for example, did not exist 10 million years ago (Partridge, 1997). Thus, the larger influence of transpiration on climate exhibited in South America may well have been more widespread in the geologic past, including other areas of the tropics and perhaps extratropical latitudes during the warmer periods of the Cretaceous and Paleogene. Ë ANGIOSPERMS AND DEEP-TIME CLIMATE How many leaves? Vegetative biomass and leaf area were held constant in the above climate modeling in order to isolate the impact of changes in transpiration rate. Over the geological record, changes in transpiration rate per unit leaf area conceivably could be offset by changes in total leaf area. Such a possibility must be treated with particular caution because the leaf area index (LAI; total leaf surface area divided by the land Surface area) can never be measured directly from fossils, and some living conifers can have an LAI three to four times that of typical angiosperms. However, several lines of evidence indicate that the Compensation of increasing transpiration rates by decreasing leaf area is unlikely. First, conifer LAI also can be quite low and extremely high LAI values are found primarily in the Pinaceae (Oren et al., 2001; DeLucia et al., 2003; Fetene & Beck, 2004; Teske & Thistle, 2004), but the Pinaceae have never been an Important element in the lowland tropics (Brenner, 1976; Rees et al., 2000; Brodribb & Feild, 2008). Second, the LAI of other plants aside from angio- SPerms and conifers is often quite low: the LAI of Ginkgo L. is below the angiosperm average, and tree ferns, which are representative of a rosette architec- ture common in the geological past with groups such as cycads, medullosans, and Bennettitales, can approach LAI values as low as 1 (Harrington et al., 2001). Third, plants with high LAI values are found in open, often semi-arid environments because they require high levels of light, i.e., high LAI individuals tend to be found in low LAI landscapes. Given the high leaf area and deep shading already present in tropical rainforests (Clark et al, 2008), simply quadrupling the number of nonangiospermous leaves does not seem like a compelling mechanism to offset increased angiosperm transpiration rates. Thus, LAI values may have been somewhat higher or lower in a pre-angiosperm world, but they are unlikely to have been dramatically higher. Finally, because biomass is dependent on precipitation, a negative feedback loop can be expected in a world without angiosperms whereby the lack of elevated angiosperm transpiration rates results in less precipitation, which results in less biomass, which results in even less transpiration and precipitation. As a result, the overall impact of angiosperm transpiration may actually be larger than indicated by changes in vein density alone. Angiosperm radiation and rainforests If tropical rainforest angiosperms are both depen- dent on and partially responsible for the high rainfall of their environment, then how could modem angiosperm lowland tropical rainforests have become established? A possible solution lies with the long entertained (Axelrod, 1959), but since discarded (Doyle & Hickey, 1976), possibility that angiosperms originated in tropical cloud forest sites in coastal uplands (Feild et al., 2009). Early-diverging clades encompassing the first five or six major n angiosperm phylogeny are extremely drought-intoler- ant and are characterized by a profound loss of xylem water transport ability at very modest water potentials (Sperry et al., 2007; Feild et al., 2009). These lineages are today largely confined either to low insolation, upland tropical cloud forests with high and daily precipitation or to freshwater aquatic zones (Feild & Arens, 2007). The high rainfall expected for oro- graphic reasons on the wi ard side of mountain belts close to oceans during the Early Cretaceous continuation of Pangea fragmentation could have allowed for the initial viability of higher vein density and transpiration rates among early, drought-intoler- ant angiosperms. The potential for positive feedback between increasing vein density and rainfall then could have permitted a gradual expansion of angio- sperms into environments that were increasingly Annals of the Missouri Botanical Garden Gupta et al., 2001; Beerling et al., 2002; Schulte et - al., 2010). In addition to these relatively immediate effects, the destruction of angiosperm tree canopies’ wherever their dominance had been already estab- ished in the Cretaceous would have resulted in heating and drying unique to those terrestrial | environments because of the loss of angiosperm | transpiration. If these climate changes slowed the | distant from maritime and orographic precipitation sources as transpiration-fed hydrological cycles were established. Early Cenozoic warmth At their Eocene apogee, warm high precipitation forests blanketed the tropics and extended past the subtropic desert belts well into the temperate zone (Morley, 2000). Although this expansion clearly related to the unusually warm conditions of the time period, i warm periods in earth history resulted in the spread of conditions that were at least seasonally dry (Ziegler et al., 2003). Direct compar- isons between the later and earlier hothouse climates of the Early Cenozoic versus the Permian and Triassic are difficult because the extreme size of the supercontinent Pangea promoted seasonality and aridity in its interior. However, Pangea fragmentation had already in the Early Cretaceous, and high xcd E a s Į lat would have further disrupted continental aridity (Ziegler et al., 2003; Ufnar et al., 2008). The widespread development f cok 1 t£ : E. Se de š Barty Cenozolc and modifying potential of angiosperm ecological domi- nance. Simulations of the absence of angiosperms indicate a 50% reduction in precipitation in modern eastern North America (Boyce & Lee, 2010), and this impact would be considerably greater in warmer climates that would allow high transpiration in the temperate latitudes to continue through a year-round growing season (J.-E. Lee, unpublished). Environmental perturbations With angiosperm dominance, tropical forests are cooler, wetter, and less seasonal. As with modem tropical deforestation (Shukla et al., 1990; Eltahir & Bras, 1996; Laurance & Williamson, 2001), disrup- tion of thi } : © or COEM angiosperm ecosystems by destructive environmental events in the geologi logic increased risks of amplified environmental response (Boyce & Lee, 2010). For example, the Cretaceous/ and dust into the upper atmosphere, followed by further global warming from the release of gravitationa] energy as heat as the enormous quantity of fine particulates settled from the atmosphere (O'Keefe & Ahrens, 1989; reestablishment of angiosperm forests, this effect would have lasted at least decades to centuries, : although such short timescales are difficult to resolve - directly from the fossil record. The loss of forest canopies during earlier events that caused widespread | disruption of terrestrial ecosystems but predated the angiosperms, such as the end-Permian (Looy et al., 4 1999) or Triassic/Jurassic extinctions (McElwain et ` al., 2009), would have resulted in much smaller 1 climate effects because of the smaller transpiration capacities of the plants involved. As a more complicated example, the Paleocene/ 3 Eocene Thermal Maximum (PETM) was a rapid global | | warming event lasting approximately 50,000 years in ` which sea temperatures increased by 5°C. Warming _ was triggered by the injection of greenhouse gases into ` the atmosphere from widely debated sources perhaps ` including the disassociation of methane hydrates from ` continental slope sediments (Katz et al., 1999; Zachos et al., 2003, 2005; Panchuk et al., 2008). In response, terrestrial plant populations migrated 1000 km or more to higher latitudes (Wing et al., 2005; Smith et al., 2007). Immediately before the PETM, angiosperm 1 canopies, then terrestrial temperature changes would 1 have involved both the gain of abiotic heating from atmospheric changes and the loss of biotic cooling . from transpiration. This cooling is seasonally as large as 5°C in the modem angiosperm-dominated world during the dry months when transpiration has the largest climatic effect (Boyce & Lee, 2010). Thus, the 1 magnitude of temperature increases on land could have been significantly larger than in the oceans because the terrestrial temperature increases expect- ed from the marine record would have been reached 4 from a transpirationally depressed pre-PETM baseline 1 temperature. However, if the PETM onset was slow ` enough to allow species migrations within a contin- uously existing canopy, then terrestrial temperature 3 be no more than expected from the increases would later during the Eocene Thermal Optimum, but were reached gradually - rather than as a discrete event, | Volume 97, Number 4 2010 Boyce et al. Plant Physiological Evolution and Tropical Biodiversity giving ample time for gradual plant migrations in continuously existing forests. Thus, comparing terres trial climate indicators from and n ne could constrain the rapidity of PETM onset and the extent ii initial environmental degradation. EcortoGy AND EVOLUTION IN AN ANGIOSPERM- DOMINATED WORLD TROPICAL DIVERSITY While temperature increases can be a positive stimulus for diversity in colder climates, the greatest correlates of plant diversity within the tropics are overall precipitation abundance and the evenness of precipitation as measured by the annual number of wet days (Kreft & Jetz, 2007). Beyond the precipita- tion at Er one spot, the size of contiguous rainforest has also been considered an important additional ^ (Reed & Fleagle, 1995; Leigh et al., 2004; Jaramillo et al, 2006). Because these factors promoting biodiversity— precipitation evenness, and rainforest area—are all pies igo angiosperm transpiration, angiosperm diversity is largely a result of the ecosystem modifications initiated by the angiosperms themselves. When viewed in this climatic context, the evolution of angiosperm le siology stands out as an intriguing key innovation for their success. Other angiosperm characteristics, such as their co-evolution with insects, reproductive barriers that promote out- crossing, and shortened generation times, may have revolutionized intrinsic plant biology, but the in- creased transpiration capacity that angiosperm vena- tion represents likely initiated a series of positive feedbacks at the ecosystem level that re-engineered climate in a way that increasingly favored angiosperm productivity as the angiosperms transitioned from a eet but Frdiopicaliy secondary grup (Wing etal, 1992 IE )t tU UCI m minanee He fostering of diversity initiated by the gos has not been limited to the a growing list of lineages that diversified ¿luc foli the angiosperm radiation includes ferns, bryophytes es, ants, bees, es, ma * am- Phibians (Farrell, 1998; Wilf et al., 2000; Schneider et » 2004; Moreau et al., 2006; Bininda-Emonds et al.. ec CN an aul 2007; Wilson et al, 2 Wahlberg et al., 2009; Wang et al., 2009). Ree Ss. for how angiosperm evolution might have driven the evolutionary pattems in other lineages often rely on generalized evocations of increased ecological com- a (ei, Schneider et al., 2004; Schuetipelz & te is consistent with a concrete mechanism driven by the rainfall increases initiated by flowering plants. Ferns and other sa have passively benefited from the ncreased precipitation that accompanied angi dierdiñostien: while animal radiations have been in response to the increased productivity and diversity of the vegetation that flourished in the new climate regimes that the angiosperms helped engender. The impact of angiosperm evolution on tropical environments may be recorded in the changing ecological opportunities available in tropical forests throu, d time. Epiphytes lack contact with soil water and dependent on reliably frequent precipitation for endi Warm, high precipitation environments have existed n n history of vascular plants, but epiphytes have arbonif- erous fern interpreted as an epiphyte dick 1991) suggests epiphytism has long been a possibility if conditions are suitable, yet other fossil examples are lacking before the evolution of angiosperms 200 million years later. In contrast, vines and lianas, which can make use of groundwater, have been abundant in non-arid environments throughout the fossil record ee et al., 2005; DiMichele et al., 2006; Burnham, 2009). True epiphytes radiated in i in the ferns, lycopods, bryophytes, and angiosperms (Wikstrom & Kenrick, 1997; Givnish et al., 2007; Heinrichs et al., 2007; Schuettpelz & Pryer, 2009; Silvera et al., 2009) only after the evolution of iosperm forests, suggesting epiphytism was a less viable strategy before the buffering of precipitation regularity by angiosperms. BIOGEOCHEMICAL CYCLING The environmental impact of angiosperms may extend beyond climate to modifying the exchange of important elements between soil, ocean, and atmo- sphere. First, the expansion of environments with abundant rainfall has shifted checks to tropical productivity in many areas from water limitation to nutrient limitation. We posit that the efficiency of nutrient scavenging strategies by rainforest vegetation in order to maintain high productivity on low fertility angiosperm-modified the chemical weathering of silicate minerals is a principal sink for the drawdown of CO» from the — fines 19 and the deeper veaimering the ;hydrologie cycle may have contributed (along with other biological and geological factors) to the steady decline of global atmospheric CO» concentrations since the Cretaceous. 536 Annals of the Missouri Botanical Garden CONCLUSIONS Bierregaard, R. O., T. E. Lovejoy, V. Kapos, A. A. dos Santos i The first order limitation on Photosynthesis i in low energy influx. The ae qupasity. of (pese to ire water L led to the spread of eh rainfall POM. particularly in the tropics. This angiosperm = has raised the diversity of other organismal grou including both the consumers ndent on the angiosperm bounty and other producers that have benefited from angiosperm-driven increases in cipitation. Discussions of the hyperdiversity of angios d ivity into a greater number of species (Doyle & Hickey, 1976). Such mechanisms et v» important, but we e angue angiosperms have tivity available for such subdivision through thelr pain of high rainfall environments. Literature Cited Ee TCI & S. E. Scheckler. 1998, T Terrestrial-marine the an: Links between the and marine leaf anatomy h to x environment in the tree fern Cyathea car acasana i ) ed ferns ley D. I. 1959. Poleward migration of early angiosperm flora. Science 130: 203: Barron, E. J. & W. M. Washington. 1985. Warm Cretaceous — High atmospheric CO, as a e explana- . 946—553 in E. T. Su Sundquist & S. Broecker ad The Carbon Bises and [aei dean CO»: Natural Variations, Archean to Present. American Geophysical Union, Washi E p. c. Batenburg, L. H. 1981. Vegetative m and A of Sphenophyllum zwickaviense, S. emar, compression species" of rus Ray. EE Palynol. 32: 275-313. Beerling, D. J. & F. L Woodward. 1997. Changes i land plant function over the Phanerozoic: R; a the fi Reconstructions based on record. Bot. J. Linn. Soc. 124: Ist- ye — —— 2001. Vegetation and the T, Terrestrial iE iode d Modeling the Fi rst 400 Million Years, Cambridge Univ niversity Press, + B. H. Lomax, D. L. Royer, G. R. J. Upchurch & L. R. Kump. 2002. 2002. An atmospheric pCO. ross the Cretaceous-T Tertiary from leaf mega- fossils. ie pees Acad. U.S. cc Berner, R. . The carbon e and CO, over d The role of land ts. Phil en mn €: os. Trans., & Z. Kothavala. 2001. GEOCARB of atmospheric CO. over Sci. 301: 182-204. IH: A revised over Phanerozoic time. Amer. J. Beck, R. Grenyer, S. A. Price, R. A. Vos, J. L. sega & A. Purvis. 2007. The delayed rise of present-day mammals. Nature 446; 507-51 Boyce, C. K. 2008. The fossil record of plant physiology and so erat te a leaves can tell us. Paleontol. Soc. Pap. a 0. The evolution of p development in a deleitó context. Curr. Opin. Pl. Biol. 13: 1-6. —— — & A. H Kn oll. 2002. Evolution of developmental potential eaves in Paleozoic mm plants. EE 28: 70-100. versity. Proc. Roy - Lond., Ser. B, Biol. Sci. 277: 3437-3443. » T. Brodribb, T. S. Feild & M. A. Zwieniecki. Teo anda leaf vein evolution was airs s p environmentally transformative. Proc. London, Ser. B, Biol. Sci. 276: 1771-1776. Brenner, G. den 1976. Middle n 2 provinces and y migrations of angiosperms. Pp. in C. B. Beck (editor), oem gin and Farly Evolution T Angiosperms. Columbia nives] Penh New York. iari T. J. 2009. Xylem hydraulic physiology: The onal backbone of terrestrial plant productivity. 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Angiosperm a ; and paleolatitudinal retaceous flori nal gradients in Cret diversity. Science 246: 675-678, Crepet, W. L. 2008. The fossi of angiosperms: row renaissance? Ann. Missouri Bot. Gard. 95: Devidelf, B. & R. J. Hanks. 1989. Sugar beet production by limited irrigation. Irrig. Sci. 10: 1-17. u C Aaa EE E cae M CLA Qui ii A Lr ML A SRA AQ ras, lianas, cipós, and - 160. th American n i š AEN EM " š O dM EE cer Ar: x. mede ; "pup ATL AER RA tU PL RA n has. yy pro em . Losos & S. P. 1 A < Ë WOES EI a PS TIT EE RRA PERO Ed eG eae em ur PACA NOCHE STIEG MEC mitt od IR che EY CI T Ut d ERES enter t Volume 97, Number 4 2010 Boyce et al. Plant Physiological Evolution and Tropical Biodiversity Davis, C- C, C. EE Webb, K. J. Wurdack, C. A. Jaramillo & M.J. e. 2005. Explosive radiation of Malpighiales supports a dicus origin of modern tropical rain i 36—65. es e carbon e rec tempe obal Change Biol. 9: 1158-1170. DiMichele, W. A., T. L. Phillips & H. W. 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Endress? TRENDS OF EVOLUTION IN EUDICOTS AND THEIR MAJOR SUBCLADES' ABSTRACT udicots and their currently recognized bs: subclades are characterized as to floral structure (including some “embryological” features) based on ca. 3000 o ginal publie ations. A new classification of nucelli i is y presented. In particular, + f larger subclades. Tenuinucellar ovules characterize Contisnales, and largely La Te CM lamiids, and Asteraceae of —ÜÁ thus all of the moet diversiipd subclades of asterids. In contrast enuinucellar ovules are sme in basal asterids and the | des of lamiids and campanuli E Ting n talales and Caryophyllales, hich h terid lineage s.l., have iiir thin nucelli. Also, the presence of endosperm haustoria or the particular ‘differentiation of the embryo suspensor characterizes some larger subclades such as Fabales and Lamiales or core Saxifragales, respectively. The expanded malvids (rih inclusion of. Cr Crossosomatales, Geraniales, and Ur i are sppored by cu features. F or several features that are potential k ey in innovations, because g — it is shown t ies ate also sporadically present in ne clades m more to the base of the phylogenetic tree. This indicates that what appear as key innovations in certain groups ma innovation. Thus, it is possible that such key innovations are 1 t ys ap hies in a strict (e.g. i -— T conforms with results of evo-d esearch, in which genetic struct | with floral f which the floral features are not prese od Key words: Asterids, basal ine: core eudicots, eudicots, evolutionary trends, floral diversity, floral structure, ovules, perianth, rosids. The extant angiosperms are composed of a basal of which, in turn, is associated with a basal grade. grade of three small clades: Amborella Baill., Thus, the phylogenetic tree, not only of the angio- Nymphaeales, and Apsirhellegeiet. s and three large sperms as a whole but also the part of the eudicots, is , monocots, and eudicots (Qiu et al., highly asymmetri c, reflecting unequal diversification 1999. Sd et a 1999). Eudicots have been (or unequal extinction or both) (Fig. 1). recognized as a clade since the structural phyloge- This is a first attempt to characterize the major netic studies by Donoghue and Doyle (1989) and are — subclades of eudicots in their floral structures, most inclusive clades, the = well supported in molecular phylogenetic analyses beginning wi t (Judd $ & Olmstead, 2004; Hilu et al., 2008; Burleigh — supraordinal level, and going down to the level of et al., 2009; Moore et al., 2009). Eudicots are the the orders. Many of these major subclades have been largest clade of the angiosperms with over 200,000 newly recognized or have substantially changed in species, over 300 families, and over 30 orders their circumscription over the past 15 to 20 years, yet (Magallón et al., 1999; APG, 2009). Triaperturate have not been agpi as to their floral pollen was recognized as a good synapomorphy for structure, apart eudicots Dae & Doyle, «. 1909) and, in particular, (Bremer et al., 2001; Stevens, 2001 à nos pollen with an aperture configuration according to Olmstead, 2004; Soltis et al., 2005; J : e aa Fischers rule, i.e., apertures originating in the Takhtajan, 2009). The ae era - e ` tetrahedral tetrad at each of the six sites where two m scis _ h mapa pore T However laa are not always ciao tures of high incidence in a ake ead they may disappear again within the of the four pollen grains are closest together (Doyle & Hotton, 1991), Like angiosperms as a whole, eudicots also exhibit a basal grade, and the core eudicots have two especially large clades, rosids and asterids, each aia Al E E: H would li oa thank M A A. x Brigitte t Y Ren, and Rudolf Schmid for noia "€ Else Marie Friis, Victoria C. . Hollowell, Cdi i bd T Stevens are acknowledged for rovienine e manuscript. v. “i on y, University of Zuric ae 10.3417/2009139 Ann. Missouri Bor. Garp. 97: 541-583. PUBLISHED ON 27 DECEMBER 2010. Annals of the Missouri Botanical Garden Sears H9HMeuNne clade and in an extreme case may not be present in the majority of its representatives. Furthermore, apomorphies can only be determined with certainty in those parts of the phylogenetic tree that are robust, and this is still not the case for many branches. Thus, it is not always practical or feasible to characterize clades, with unless they are key innovations with a dominant representation and the branches are well supported. However, larger clades are often simply characterized by certain features that have a higher incidence than in related larger clades. Such apomorphic or homo- plastic tendencies (Cantino, 1985; Sanderson, 1991) are a main topic of this study. A feature may seem to be an apomorphy of clade A within a more inclusive clade A + B, but it may have disappeared in clade B, thus technically being a plesiomorphy of clade A, or it may seem to be an apomorphy of clade A but is an apomorphy only of a large subclade of clade A or separately in more than one of its subclades. Such tendencies are quite common and deserve interest in their own right. They appear to be the result of i icular fi ir the evolution and the history of their establishment (see Figure 1. Cladogram of major subclades of eudicots (simplified after APG, 2009) (numbers in bold) and the occ h (n i theses). Asterids with 10 potential key innovations urrence of some of these features in other subclades where they were not key innovations also Endress, 2005b; Shubin et al., 2009). An example of a group with a prominent tendency is the nitrogen- fixing clade consisting of the four orders Fabales, Fagales, Cucurbitales, and Rosales. All angiosperms distributed in these four orders. However, only a small proportion of genera in these orders (except Fabales) exhibit this symbiosis. It has been assumed that the feature evolved independently several times in this clade because of a predisposition for the evolution of this feature (see, e.g., Soltis et al., 2005). Thus, a prediposition of a yet unknown nature for the symbiosis may be a synapomorphy in this clade, but not the presence of the symbiosis as such. plant groups at the level of alpha taxonomy, which I call here alpha morphology, is of course necessary. However, this is insufficient to understand patterns of evolution at all levels of angiosperms. A more comprehensive kind of morphology is needed based on the advances of evolutionary biology (Endress et al., 2000; Endress, 2003, 2005b, in prep.). The present contribution on floral structure of eudicots is based on the published work of a great number of systematists and morphologists. Condensed o de ax Volume 97, Number 4 2010 Endress Evolution in Eudicots and Their Major Subclades results on rosids based on information from over 1400 original publications were published by Endress and Matthews (2006b). For the present study, ca. 1500 additional publications on core eudicots were consid- ered, plus literature on basal eudicots (partly cited in Endress & Doyle, 2009). This literature was searched for structural features of interest for a characterization of the major subclades of eudicots. NOTES ON CONCEPTS AND Use OF TERMS PHYLLOTAXIS OF FLORAL ORGANS Phyllotaxis of floral organs is defined by the divergence angles between successively initiated floral organs (e.g., Endress, 1987). It should be emphasized that the mere developmental sequence of organs is not decisive for a certain phyllotaxis pattern (which has often caused confusion in the literature). Whorled versus spiral phyllotaxis can be best distinguished by equal versus different steepness of antidromous parastichy sets and presence versus absence of orthostichies (Endress, 2006). All flowers with regularly arranged organs, regardless of whether their phyllotaxis is spiral or whorled, exhibit conspic- uous patterns of spiral lines (parastichies) formed by the contiguous organs, as seen from above in young stages. These parastichies occur in several sets of certain numbers, which run in both directions (antidromous). In whorled flowers, the degree of steepness of the parastichies of two consecutive antidromous sets is equal, but in spiral flowers the degree of steepness is different. Orthostichies are straight radial lines created in the same way, but they are present exclusively in whorled flowers. Whorled patterns are either simple (with the same number of organs in all whorls, and the organs of consecutive whorls alternating) or complex (with organ number increasing or decreasing in consecutive whorls by collaterally double or multiple organ positions instead of a single organ (discussion in Staedler & Endress, ; see also Ronse De Craene & Smets, 1993, 1996). In irregular phyllotaxis there is no obvious pattern. It is generated in flowers with exceedingly numerous organs, especially in polymerous androecia. - Floral phyllotaxis is practically always whorled in Core eudicots and also predominantly in basal eudicots, but it is spiral in some core Ranunculales, in the polymerous perianth of Nelumbonaceae and some Buxales, and sometimes in the androecium of Trochodendrales. Complex whorled patterns are present in a number of basal eudicots and some rosids but less so in asterids. Irregular phyllotaxis in the androecium occurs scattered in various groups, 1 1 NE l1 exicdieots. a Figure 2. Diagram of outer organs in a typical 5-merous flower of eudicots. The unnumbered organ at the bottom itio Prophylls and sepals form in a spiral sequence, which leads i > E : E £ L Es dfe. band one organ in between, two organs inside). The prophylls are : bp: 4a so 4d 1 k: ‘+ oll th £ ,L counted as floral organs. of rosids, and some mainly basal asterids (see also section “Merism of Floral Organ Whorls or Series” below). MERISM OF FLORAL ORGAN WHORLS OR SERIES Merism in flowers is defined by organ number of whorls (in whorled phyllotaxis) or series (in spiral phyllotaxis) (for a closer explanation of series, see the illustrated examples in Staedler et al., 2007). Successive whorls in a flower commonly have equal numbers of organs and their organs alternate in position (see also Ronse De Craene & Smets, 1994). Determination of merism is mostly easy because of this alternation of positions. However, in some cases it is not trivial (see section Sabiaceae). In cases with ighly synorganized floral organs, alternation may be lost, probably by loss of one whorl (e.g., ante s stamens in subclade [III] of Ericales). Pentamerous flowers are a prominent feature of = eudicots, pentamery is common i polysymmetric flowers as well as in clades wi monos ic flowers. In basal eudicots, pentamer- ous flowers also occur but are not common (see notes for Ranunculales, Sabiaceae, Proteales, and Buxales). re is a common pattern in these pentamerous flowers (Fig. 2). Flower development is commonly initiated with two lateral prophylls. It continues with the sepals (1 to 5), all in a spiral sequence. It is not a Annals of the Missouri Botanical Garden spiral phyllotaxis (Endress, 1987, 1994, 2006). Phyllotaxis is defined by the angles between subse- quent organs, as explained above, and the angles of correspond to those in a whorled phyllotaxis (perhaps except in the outermost two or three organs [the prophylls included]. The consequence of the spiral sequence is that sepals 1 and 2 are positioned outside, sepals 4 and 5 are inside, and sepal 3 is in between (with one margin outside and one inside) This is a characteristic disposition of sepals in core eudicots and is “quincuncial” aestivation (Fig. 2) (Reinsch, 1926). The five young petals and the five young stamens, in contrast to th pals, arise almost simul ly and are in two neat whorls. Because of this, petals in eudicots are not commonly quincuncial, but often all petals h gi putada mt s.s. L: E contort aestivation. Petal aestivation is often incon- stant if petals are late growing, a situation that is common in many eudicots. perianth organs in a whorl. In the calyx, this is often associated with a reduction in size and change of function (e.g., Asteraceae, Valerianaceae) (Semple, ) or loss of function (e.g., Thunbergioideae) (Schónenberger & Endress, 1998; Schénenberger, 1999; Borg et al., 2008; Endress, 2008). Polystemony is prominent in many eudicots, especially in basal eudicots, and among core eudicots in rosids (especially malvids) and some clades of the asterid lineage s.l. (Caryophyllales, Cornales, Eri- cales). then develop from five primary primordia or a ring meristem. polystemony based on a simple increase of floral or androecial radii (Apiales, Sokoloff et al, 2007a) or presence of several stamen whorls (Ranunculaceae, Schóffel, 1932: Ren et al, 2010; Rosaceae, Kania, 1973; Lindenhofer & Weber, 1999), Multicarpelly is also quite common in various groups. But in contrast to polystemony, it is mostly based on more than five carpels in a whorl (Endress, 2002, 2006; Doyle & Endress, 2010). The presence of carpels in several whorls (or series) is rare and is, as a rule, correlated with apocarpy (in a few Ranunculales and Rosaceae). i PERIANTH One of the ongoing problems in interpreting structure is the concept of sepals defined by their specific male and female such a clear distinction is not possible for sepals and petals (Endress, 2005a, 2006). The function of bud protection and optical attraction of pollinators are commonly carried out by sepals and petals, respec- tively. However, both functions can be fulfilled by any floral organ type and even by organs outside of the flowers, such as bracts. Conversely, both sepals and petals may also have other functions than just bud protection and optical attraction at anthesis. Specif- ically, petals are not always “petaloid,” a term often used in the literature simply for a colored, optically conspicuous organ. The question of homology of sepals and petals has long been recently by molecular develop- mental genetics and an evo-devo approach (e.g., Kramer & Irish, 2000; Irish, 2008, 2009; Di Stilio et al., 2009; Hileman & Irish, 2009; Kramer, 2009a, b; Rasmussen et al., 2009; P. S. Soltis et al., 2009) and also from a comparative point of view (Ronse De Craene, 2007, 2008), but a simple answer is not in sight. For the time being, I use a practicable concept for eudicot perianth organs. Because most core eudicot groups have two whorls or series of perianth organs, I call the organs of the outer whorl or series sepals and those of the inner outer whorl or series petals, irrespective of their differentiation. In cases in which there are fewer or more whorls or series than two, the ocal phylogenetic situation is considered for an interpretation. In basal eudicots, the number of perianth organ whorls or series is often higher than two and a delimitation is sometimes more difficult. However, for problematic cases, the specific local phylogenetic neighborhood may also include cases that are easier to interpret, and from there tentative conclusions may be drawn — OVULES Ovules are ovular feat diverse in angiosperms, but several have b hown to be stable at higher systematic levels and can be used to characterize major subclades. Of special interest are the differen- tiation of the nucellus at the time of the beginning of meiosis, the number and relative thickness of the integuments and their differential participation in micropyle formation, and the direction and amount of curvature of the ovules at the time of fertilization (Endress, 2003, 2005a; Endress & Matthews, 2006b). The two types of ovules, crassinucellar and tenuinu- cellar, which are conventionally distinguished in the embryological literature and have been widely used in systematics (e.g., Philipson, 1977), cover a relatively broad array of forms. This and the need for a finer- grained ovule classification have been repeatedly addressed (e.g., Hamann, 1977; Tobe, 1989: Shamrov, Volume 97, Number 4 Endress 2010 Evolution in Eudicots and v Their Major Subclades Figure 3. Classification of ovules used here (meiocyte gray). —A. Crassinucellar (wit th several cell layers above Seen. —B. W Weakly ose (with. two Pm layers above meiocyte). —C Pseudocraesinucellar (with mn vel layer ncompletely te e ome at its flanks d at the nuecllus SUR £. Tenuinucellar cg one = layer above meiocyte and no sterile ts flanks or at the base of the nucellus). — F. Reduced tenuinucellar (as in E, but meiocyte longer than the sancti, on). ead iz p a partly "inferior" positio 1998; Endress, 2003). An extensive survey of the original literature (P.K. Endress, in prep.) shows that the diversity of forms can be compartmentalized into additional subtypes that are of interest because of r relatively stable occurrence in certain larger clades of angiosperms. These subtypes are shown in Figure 3: crassinucellar (nucellus with more than two cell layers above the meiocyte at the time of the first division) (Fig. 3A), weakly crassinucellar (nucellus With two cell layers above the meiocyte at the time of the first division, and the second cell layer not derived from the epidermis) (Fig. 3B). pseudocrassinucellar (nucellus with two cell layers above the meiocyte, the second derived from the epidermis by periclinal division; term introduced by Davis, 1964) (Fig. 3C). incompletely tenuinucellar (nucellus with only the xm (Fig. 3D), tenuinucellar (nucellus with only epidermis above the meiocyte and at its flanks, and nucellus without sterile tissue behind the Meiocyte) (Fig. 3E), reduced tenuinucellar (nucellus very short, with only the epidermis above the meiocyte e the meiocyte "inferior," i.e., situated partly below Sei (Fig. 3F). An endothelium, a physiolog- oS is y active layer of cylindrical, cytoplasm-rich cells, oe he i present in ovules with a thin nucellus, especially in the states depicted in Figure 3B-*. As the survey progresses, this classification may be further modified, but the present state is useful to discuss the distribution of ovule diversity in larger clades of eudicots. Crassinucellar ovules are predominant in basal eudicots and most rosids; incompletely tenuinucellar ovules are predominant in asterids. Tenuinucellar ovules occur especially in some species-ric clades of asterids (Gentianales, Lamiales, and Asteraceae). FLORAL NECTARIES Nectaries are originally not independent - organs but merely histological regions that secret nectar and may be located on any of the floral organs. However, in derived clades they may also form more independent structures (disc nectaries) that cannot easily be relegated to one of the floral organs. In basal eudicots, nectaries are as associated with stamens (some -— drales, Buxales). In core eudicots, disc nectaries are — de metes o occur in some a Sabiaceae ai (coll the gynoecium base). Disc incl are sometimes difficult to distinguish from other nectaries. I tentatively use this term for nectaries that form a ring around the gynoecium at the fl floral base and are Annals of the Missouri Botanical Garden elevated above the floral base in a disclike manner, thus they are of some thickness; they may be lobed between the stamen bases but characteristically form dello, 2007). An exploration of the evolutionary origin of disc nectaries is beyond the scope of this paper. MAJOR SUBCLADES OF EUDICOTS GRADE OF BASAL EUDICOTS The basal eudicots are a grade of three to six main clades (Hilu et al., 2003, 2008; Worberg et al., 2007; Qiu & Estabrook, 2008; APG, 2009; Burleigh et al., 2009: D. E. Soltis et al, 2009) Ranunculales, Sabiaceae, Proteales, Buxales and Trochodendrales (topology unresolved), and Gunnerales. The position of Ceratophyllales as sister to eudicots as found in a number of analyses is not sufficiently supported (see Qiu et al, in press), and they further here. The uppermost step of the grade, Gunnerales, which are sister to core eudicots, can also be treated as part of the core eudicots, as proposed by Soltis et al. (2003), because of high molecular phylogenetic support of their sister rela- tionship. However, from a floral morphological point of view, treatment as part of the basal eudicots is more practical. Drinnan et al. (1994) recognized that in basal eudicots there is a i In addition, Sabiaceae, with complex, somewhat puzzling monosymmetric flowers in Meliosma Blume, can be regarded as basically trimerous (see discussion under Sabiaceae). In three of the six orders of the basal grade of eudicots, there are genera without a perianth. Although this is only a very small fraction of the group, it is much more than in other orders of ' an interesting evolutionary tendency. Perianthless flowers are pres- in eudicots (cf. Doyle & Endress, E Doyle, 2009). The repeated loss of the entire p, may have possible because of only weak synorganization of floral parts (Endress, 1990). In some other genera, partly of the same families, the perianth is only weakly differentiated and bractlike: among Ranunculales in Circaeasteraceae (Circaeaster Maxim., Tian et al., ), among Trochodendrales in Trochodendraceae (Tetracentron Oliv., Endress, 1986; Ren et al., 2007), and among Buxales in Buxaceae (von Balthazar & Endress, 2002a, b). Concomitant with the weak differentiation of the perianth, wind pollination is relatively common, beginning with Eupteleaceae in Ranunculales, but then especially in the upper steps of the grade (Platanaceae, Buxaceae, Gunnerales). Pollen is basically tricolpate, although tricolporate in some Menispermaceae (Ra- nunculales), Sabiaceae, and Buxaceae (Furness et al., The gynoecium is commonly more or less apocarpous, which has been retained from the basal angiosperms (Endress & Doyle, 2009). The ovules are mostly crassinucellar and bitegmic, with the outer integument commonly thicker than the inner (Endress & Igersheim, 1999). Nectaries may be present on floral organs (petals, staminodes, stamens, or carpels), as in Ranunculales, Buxales, and Trochodendrales. In some Sabiaceae and Proteaceae, nectaries form collars around the gynoecium base. However, disc- shaped nectaries, as characteristic for many core eudicots, do not occur. RANUNCULALES Ranunculales comprise seven families. Euptelea- ceae and Papaveraceae are successive sisters to the core Ranunculales, consisting of the five families Lardizabalaceae, Circaeasteraceae, Menispermaceae, Berberidaceae, and Ranunculaceae (Hoot & Crane, 1995; Hoot et al., 1999; Qiu et al., 2006; Worberg et al., 2007; W. Wang et al., 2009). Floral merism is most commonly two and three, but five, eight, and more also occur (Hiepko, 1965b; Endress, 1987). Spiral phyllotaxis in the perianth is less common than whorled phyllotaxis (Schöffel, 1932; Hiepko, 1965b; Ren et al., 2009, 2010). Whorled perianth phyllotaxis 1s primitive in R hir: 4 ntire eudicots) (Endress & Doyle, 2007). Elaborate monosymmetric flowers evolved in two families of Ranunculales, in Papaveraceae and in Ranunculales; in some Meni- spermaceae there is monosymmetry by reduction (Endress, 1999; Jabbour et al., 2009). Valvate anther i e is common in Berberidaceae and rarely present in ulaceae (Endress & Hufford, 1989; Endress, 1995). Nectaries, if present at all, are on the Stamens, staminodes, or petals. Carpels are mostly free but fused up to the top in Papaveraceae (Endress & Igersheim, 1999). Ovules are basically crassinu- cellar, bitegmic, and anatropous, with a trend to in volume 97, Numbe Endress 2010 ion i Evolution in Eudicots and Their Major Subclades "d E ETT G I tan a tire al A—E. A fly-pollination syndrome is present in ast one genus in each family of the core owers small, flat, S dull-colored, ra brown, green, or crean short. cuneate, often He) i m RP f. & -w ws eee (Sinofra tia chinensis (Franch.) Hemsl. rdonia Berberic à .) (phato by Yi Ren). —C. Me rmaceae (: enium sU a bee eae n Mi wr d ust thalictroides (L). Mic hx. : » licissima Marsl petals, and d syndrome is amet in three families of Ranunculales (flowers with caducous or lacking sey Pe d Eu stam th long, pollen-rich anthers). —F, G. Eu uptelea polyandra 5 d & Zucc.) acleaya i. (Willd.) R. Br.). —J. Ranunculaceae (Thalictrum J foetidum L.). -J. ways s without H.I n syndrome occurs in representatives « dtm mainly greenish nted on the tips pollinatio five families: small, brown flowers with open nectar p í are homologous to se derived Papaveraceae, Circaeasteraceae, and ost Ranunculaceae, to unitegmic in Ranune -ulaceae, Menispermaceae, and Circaeasteraceae, and to cam of staminodes (Fig. 4A— E) wh the nectariferous petals in other peces of two of these families (Berberidac eae and Ranunculaceae) ; n et al., 2004). A wind- also noteworthy because it is eos (commonly associated with a zigzag e in some Papaveraceae, Jerberidaceae, Th spermaceae (Endress & Igersheim, 1999). cim (see also Endress y L3 pollination syndrome Is Ran interesting aspect of floral biolo unc iq . ulales is hat in the core group a fly- Annals of the Missouri Botanical Garden present in Eupteleaceae, the basalmost family of the order, and also rarely occurs in Papaveraceae and Ranunculaceae (Fig. 4F—J) (see also Endress, 2002). In these flowers, the perianth is caducous or lacking altogether, 4: ab. ie f g Iob I 1 The presence of wind pollination in a few Ranuncu- lales and other orders of basal eudicots (see above) is noteworthy because it is very rare in basal angio- sperms (Endress, 2010). SABIACEAE ch: t the n 4 ok ts Mk basal of eudicots or may form a clade with Proteales (Qiu et al., 2005). Relatively elaborate floral monosymmetry, perhaps with an explosive anther opening, is present in Meliosma (Ronse De Craene & Wanntorp, 2008). The lowers of Meliosma have been described as pentamer- ane with th, is 1 ë L uk opposite organs partly fused with each other (Stevens, 2001 onwards). However, the flowers can be easily mimada : It n de + } J. 19 whoris NEIN d š L v > 1 of floral monosymmetry. In this way, the floral organization would be as in trimerous Ranunculales (e.g, Berberidaceae, Menispermaceae) or dimerous Proteaceae. In these groups, there is a tendency that stamens are basally fused with the next outer petals of the same radius. However, as the floral organs are in regar ahetoating trimerous whorls, these next outer floral whorl, but only to the second next outer whorl. The same is true for the dimerous whorls in Proteaceae, in which the stamens are fused ( i i I 20) with he senal 1 are lacking). In Berberidaceae, this synorganization between petals and stamens may be so intimate that + Lg i is shown in exceptionally 5-merous terminal flowers of an inflorescence, in which five stamens remain congenitally connected with the five petals in the same radii (Endress, 1987). In this case, the alternation of organs between whorls appears no longer present. The flowers of Sabiaceae with seemingly supe: organs can be interpreted in the same way. In the floral diagram of Meliosma by Wanntorp and Ronse De Craene (2007), although they i | in gd DE the flowers differently, the followed by three wh a (lo 1 : propnytis ieeesbnale Eh U L l ¿À a pee (1) * whorl of with the sepals, (3) a whorl of two small petals (one missing in the symmetry plane) alternating with the larger petals, (4) a whorl of three stamens alternating with the small petals, and (5) two stamens mati with the outer stamens (one missing in the symmetry s as a unit. This plane, in the radius of the missing small petal). In contrast. the fl f Sabia Colel I ly y tric and pentamerous (van de Water, 1980), analogous to the 5-merous terminal flowers of Berberis L. The two (or three) carpels are at least basally congenitally united, and in Sabia postgenitally united on top (van de Water, 1980; Endress & Igersheim, 1999). The two ovules per carpel are unitegmic, hemianatropous or orthotropous, and probably weakly crassinucellar in Meliosma and erassinucellar in Sabia (Mauritzon, 1936). However, more detailed research is needed. A collar-shaped nectary around the gynoecium base is present in Sabia (van de Water, 1980). PROTEALES Proteales, the third clade of basal eudicots (found by Chase et al., 1993), has three seemingly unrelated ble with the giant-flowered waterlilies among Nym- phaeales, which are also primitively small flowered. Of the three families, only Proteaceae are diverse and they have a wide array of pollination adaptations, including insects, birds, mammals, and wind. How- ever, their floral organization is uniform with consistently four sepals (with valvate aestivation), no petals, four stamens (fused with the sepals of the same radius), and one carpel, and secondary pollen presentation on the stylar head (Yeo, 1993). All Proteaceae have flowers with dimerous whorls (Doug- las & Tucker, 1996, see also preceding section), modern Platanaceae have flowers with trimerous to tetramerous whorls (von Balthazar & Schénenberger, 2009). and in Mak n p ly Pis with a spiral perianth, and stamens and probably the free carpels in irregular position, the stamens arising from a ring primordium in centripetal sequence (Hayes et al., 2000). Interestingly, some fossil Platanaceae are pentamerous, so that the seemingly primitive trimery in modern representatives may be derived (Friis et al., 1988; Crane et al., 1993; Pedersen et al., 1994; von Balthazar & Schónenber- ger, 2009; Doyle & Endress, 2010), but dimerous flowers are also known from Cretaceous members (Magallón-Puebla et al., 1997). Modem Platanaceae are wind pollinated and have decurrent stigmas. Ovules are orthotropous in Platanaceae and many Proteaceae (as in Sabiaceae, see above), and the inner integument is thicker than the outer in Platanaceae and Proteaceae, but the other way around in Nelumbonaceae (Endress & Igersheim, 1999). Some have a collar- neetary around the gynoecium base (Rao, 1971). volume 97, Number 4 2010 Endress Evolution in Eudicots and Their Major Subclades gure 5. Proteales, Lacan aia m" Buxales. A—E. Proteales. A. Proteac ee Cerne levis (Cav.) : P atus (A. Cunn.) Endl.). E Proteaceae m scidendro 3r. sp., male pop le [yellow] and fe male [red i fi infloresc ences, wind poll —F. Tabak Trochodendraceae (Trochoe lendron aralioid. (S Beds es. Sarci infl ococea hookeriana Baill. male inflores 1 cence). —I. Buxaceae (Styloceras brokawii A. H. Gentry & R B. rescence, wind pollinated). MOCHODENDRALES AND BUXALES (Endress. 1986; Chen et aL. Domin), - —B. scene d Bid: —F es Siebold & uxaceae > (Bun s sempervirens L., a fe male flower surrounded } by male flowers). —H. Buxaceae L ( B Foster. male and some Buxaceae (von Balthazar & Endress. 2002a, b). In f E so Si In in the next two clades, Trochodendrales (with both orders, polymerous flowers are ah o present. Troc I es. Trochodendron 1i poly i hodendraceae inc luding Trochodendron and Tet- Trochodendrales, Trochoder - I à € Sr s K pu and Buxales (with Buxaceae and Didyme- androecium and gynoecium and shows ss, 1990); also, ©ae), dimerous flowers are present in Tetracentron and spiral flowers (Endress, 1 merous in th whorled 1 ts fossil Annals of the Missouri Botanical Garden relative, Nordenskioldia, is multicarpellate (Manches- ter et al., 1991; H. C. Wang et al., 2009). In Buxales, St and Buxus natalensis (Oliv.) Hutch. are polystemonous, the latter by double and multiple positions of stamens in two whorls (von Balthazar & Endress, 20022). The perianth is simple and incon- rochodendron (Endres, 1986; Wu et al., 2007), Styloceras (von Balthazar & Endress, 2002a, b), and Didymeles (Sutton, 1989; von Balthazar et al., 2003). Interestingly, in the Creta- ceous (early Cenomanian) Spanomera Drinnan, Crane, Friis € Pedersen, the male flowers have been reconstructed as pentamerous with the five stamens > aL nern toast e superposed to the five p gans ( , 1991). The male flowers of Spanomera are somewhat monosymmetric and may be interpreted in the same way as those of Meliosma (see under Sabiales), whereas the female flowers consist of dimerous whorls (Drinnan et al., 1991). Modern Trochodendrales and Buxales have predominantly decurrent stigmas, al- though the presence of nectaries in at least half of the genera, always associated with the gynoecium, indicates that wind pollination does not dominate (Endress, 1986; Vogel, 1998; von Balthazar & End- ress, 2002a, b). The carpels are united only at the base. The ovules are crassinucellar, bitegmic, anatro- pous, with the inner integument thicker than the outer (Endress & Igersheim, 1999). + Mart CL GUNNERALES Gunnerales, with Gunneraceae and Myrothamna- - ceae, represent the uppermost step in the basal eudicots and are sister to the core eudicots. Because this sister relationship is molecularly strongly sup- inflorescence, and they à wind-pollination syndrome. The two carpels of the (pseudomonomerous) gynoecium in G ited in the with mostly one locule. A single crassinucellar, itus hemitropous ovule is present, with both integuments two cell layers thick (Endress & Igersheim, 1999), u CORE EUDICOTS Core eudicots are the largest named clade in the hierarchical classification of eudicots. They are characterized by a predominance of 5-merous flowers (in contrast to the 2- and 3-merous flowers that dominate in basal eudicots). Pollen is mainly tricolporate or derived therefrom (in contrast to the simpler tricolpate forms that dominate in basal eudicots), although in basal clades of core eudicots, tricolpate pollen is still present and often coexists with tricolporate pollen in orders or families (Dilleniaceae, Saxifragales, Zygophyllales, Berberi- dopsidales, Santalales, Caryophyllales, Cornales, n, 1952). Some of the basal groups in core eudicots have spirally arranged perianth organs of an unfixed number, such as some condition is derived at this level and not primitive (Endress & Doyle, 2007), in contrast to Ronse De Craene (2004). Rosids and asterids are two especially large and diverse groups of the core eudicots. There are several classical floral characters that roughly distinguish rosids and asterids: (1) petals free versus united, (2) stamens in two whorls and not fused with petals versus a single whorl and fused with petals, (3) ovules bitegmic, crassinucellar, and without endo- thelium versus unitegmic, tenuinucellar, and with endothelium, and (4) endosperm haustoria rare absence of special mucilage cells in flowers (Matthews & Daa 2006). A previously unreported difference is that a L oi d — ae unvascularized ovules, whereas this does not appear to be the case in rosids. This needs more comparative study A surprisi gf +n Acer in behavior in those groups of rosids and asterids that have contort petal aestivation. In asterids, the direction of contortion is always fixed in a species, genus, or even family. In contrast, in most rosids both directions are Present in the same individual (Endress, 1999, 20014). re are two common contrasting alternative strategies that repeatedly evolved in both rosids and asterids but with different distribution in the subelades: (1) small simple flowers, often function- ally unisexual, the petals often with both protective and attractive functions (many rosids, some aster- ids; e.g., many Celastrales, Sapindales, Apiales), — and (2) elaborate, complex flowers with dichogamy/ ` E Volume 97, Number 4 Endress Evolution in Eudicots and Their Major Subclades 551 herkogamy mechanisms, often monosymmetric (some rosids, many asterids; e.g., Fabales, La- miales, Asterales), in part with secondary pollen presentation. DILLENIACEAE Dilleniaceae have an unresolved position at the base of core eudicots (APG, 2009). The flowers of 4 i T (u 2009). There are most often five petals, but three are not uncommon. These numbers and developmental observations in Dillenia L. (Endress, 1997b) indicate that perianth phyllotaxis may be spiral. In Dillenia, flower size is conspicuously increased, associated with a further increase in stamen number and an increase in carpel number and carpel fusion (Endress, 1997b; Horn, 2009). Androecial asymmetry occurs in two unrelated clades (Schumacheria Vahl and Hibbertia Andrews, p.p; Horn, 2009). Ovules are bitegmic, pronouncedly crassinucellar, somewhat campylotro- pous, with a zigzag micropyle, and the inner integument thicker than the outer (Sastri, 1958). The entire family appears to have short-lived pollen flowers without nectaries and is bee pollinated (Endress, 1997b). ROSIDS Rosids are systematically relatively well circum- scribed (H. C. Wang et al., ) and represent the largest subclade of core eudicots in terms of number of orders and families. However, there are still many unresolved topologies between larger subclades of rosids, which may reflect their rapid early radiation in the Cretaceous (H. C. Wang et al, 2009) A comparison of floral structures in the major subclades Was attempted by Endress and Matthews (2006b), and Comparison with fossils was discussed by Endress and Friis (2006) and Schénenberger and von Balthazar (2006). See also general notes on rosids under Core Eudicots. SAXIFRAGALES Saxifragales, the basalmost clade in rosids s.l. (not x included in rosids in APG, 2009), appear to consist of three main clades: (1) Paeoniaceae plus Peridiscaceae _ (not strongly supported), (2) the so-called woody families veia nm Daphni- Phyllaceae, Hamamelidaceae), and (3) the core Saxifragales ( (Aphanopetalaceae, kuspa wh Cras- sulaceae, Iteaceae, Penthoraceae, Pterostemonaceae, eae, Grossulariaceae) (Jian et al., 2008). Woody families have a poorly differentiated Ç Perianth or no perianth at all, and are completely or partly wind pollinated. In these families (except for a few Hamamelidaceae), floral nectaries are absent. In petaliferous families, the petals have a narrow base and are commonly retarded in bud. Another extreme are Paeoniaceae with much enlarged flowers, and mainly pollen as a reward for pollinators. Paeoniaceae and Peridiscaceae share the absence of petals (the seeming petals in Paeoniaceae are sepals, Hiepko, 1965b) and ao (Davis & Chase, 2004; Bayer, 2007) wi initiation in Paeonia- ceae (Hiepko, oe Moderate polystemony also occurs in a few Hamamelidaceae, and notably with both centripetal and centrifugal initiation patterns n 1976). If nectaries are M they form a ng (shallow, not disclike) arou ovary base peto S asifragscoue) (Bensel k Piles 1975), or scales (disc lobes) between the stamens (some Hamamelidaceae, Endress 1989b) or at the back of the carpels (Crassulaceae) (Wassmer, 1955); in some other Hamamelidaceae, nectaries are on stami or d bap 1989b). Elaborate disc nectaries, many eurosids, do not occur in MR mattis anthers are common (in contrast to dorsifixed anthers as in many other rosids; Hufford & Endress, 1989; Endress & Stumpf, 1991; Hermsen et al., 2006). Some families have largely or completely free carpels (Altingiaceae, Cercidiphylla- ceae, Fleece. llegaste Crassulaceae). arp gynoecia are isomerous with the outer fel whorls in Crassulaceae, Haloragaceae, Aphanopetalaceae, and Penthoraceae, or there are at least more than two carpels in Paeoniaceae and Peridiscaceae. Ovary position is conspicuously labile, fluctuating between -o semi-inferior, and superior at = level, metimes even within a genus (Hamamelidaceae, aku, 1967, 1989d; Corylopsis Siebold & Zucc., Endress, 1989d; Saxifragaceae, Morf, 1950; Soltis & Hufford, 2002; Lithophragma (Nutt.) Torr. & A. Gray, Kuzoff et al., 1999). The ovules are anatropous and apo! crassinucellar, but weakly crassinucellar in eae, Crassulaceae, and Haloragaceae ol 1928; Mauritzon, 1933); they are bitegmic (except for a few unitegmic Saxifragaceae, Mauritzon, 1933). In the taxa of several families, the presence of more than two meiocytes in the nucellus has been wasimi (Aphanopetalaceae, Mauritzon, 1939; Cras- sulaceae, Mauritzon, 1933; Hamamelidaceae, End- ress, 1977; Paeoniaceae, Walters, 1962). Commonly, the outer integument is thicker than the inner or both are equally thick, and the micropyle is formed by both integuments es are not yet mature at anthesis in Beason Cercidiphyllaceae, and some Hamame- idaceae, a feature ed with flowering in early spring (Endress, 1967, 1977, unpublished). Endo- = Annals of the Missouri Botanical Garden sperm toria are reported from Crassulaceae (Mauritzon, 1933). More strikingly, embryo suspenso haustoria are formed by the greatly enlarged terminal cells in members of core Saxifragales (Crassulaceae and Saxifragaceae, Vignon-Fétré, 1968; Haloraga- ceae, Bawa, 1969). A unique feature within rosids is valvate anther dehiscence in Hamamelidaceae. The state reappeared here in isolation after it had been Endress, 1989; Magallón, 2007). In the unusually rich Cretaceous fossil record of the family, valvate dehiscence is well represented (Friis & Endress, 1990; Endress & Friis, 1991; Magallón-Puebla et al., 1996; Magallón et al., 2001; Magallón, 2007). VITALES Flowers of the only family in the order, Vitaceae, are remarkably uniform. are tetramerous or erous, haplostemonous, and have a mostly dimerous gynoecium. Sepals are united and form a short rim. Petals are induplicative valvate and postgenitall y united in bud and form a massive protective cover (e.g., Gerrath € Posluszny, 1989). Stamens are addition, they together form a basal tube (Nair & Nambisan, 1957). The carpels are congenitally united up to the stigma (Gerrath & Posluszny, 1989). The ovary fluctuates between superior and semi-inferior (Kashyap, 1957). The two ovules per carpel are on an axile placenta (Gerrath & Posluszny, 1989). Ovules are anatropous and pronouncedly crassinucellar, with a nucellar cap (Berlese, 1892). The outer integument is thicker than the inner, and both or only the inner form the micropyle. A well-developed nectary disc is present between androecium and gynoecium. EUROSIDS Eurosids contain two major groups: fabids and malvids. Fabids again contain two major subgroups: the nitrogen-fixing clade and the es—Oxali- dales—Malpighiales (COM) clade. Two or three additional clades form again a basal so the order cannot yet be structurally characterized. Tapiscia Oliv. and Huertea Ruiz & Pay. were seen as a somewhat aberrant sub f Staphyl i Crossosomatales) for > long tiae (Riiie; 1942). Perrottetia Kunth and Di Dunn were previ- present in Balanites ously placed in Celastraceae, but floral structure of Perrottetia showed it to be clearly out of place there (Matthews & Endress, 2005a), and Gerrardina Oliv. was placed in Flacourtiaceae (Malpighiales) before it was recognized as constituting a separate family (Alford, 2006). The position of Myrtales and Gera- niales in the malvid clade is new (Burleigh et al., 2009). Furthermore, in analyses based on mitochon- drial genes (Zhu et al., 2007; Qiu et al., in press), the COM clade appeared to come with the malvids instead of the fabids. Interestingly, this relationship had been tentatively suggested earlier by Endress and Matthews based on floral structural data. It is important to emphasize that, although the different orders are relatively strongly supported by molecular systematic analyses, this is not always the case for the relationships between the orders. Therefore, details of the topology will most probably change in the future with denser taxon sampling. FABIDS (EUROSIDS D In APG (2009), core fabids have two large subclades that are sister to each other, the nitrogen- fixing clade and the COM clade. Zygophyllales are sister to them. However, fabids are structurally not easily characterized, especially as the position of the COM clade is uncertain (see above), and thus the circumscription of fabids is uncertain. ZYGOPHYLLALES Zygophyllales contain two families, Zygophyllaceae and Krameriaceae (APG, 2009). Flowers of Zygophylla- ceae are polysymmetric; those of Krameriaceae, elab- orate oil flowers, are monosymmetric (Vogel, 1974). Flowers are basically pentamerous, diplostemonous or (rarely) haplostemonous, with five or three carpels (Nair & Nathawat, 1958; Narayana & Rao, 1963); however, in iibi: tóm S E oca s RE gynoecium is pseudomonomerous (Leinfellner, 1971; Simpson, 1982). The re in early development (Ronse De Craene €: Smets, 1995). The carpels are congenitally united up to the stigma. Ovules are weakly crassinucellar in Balanites Delile (Nair & Jain, 1956; Boesewinkel, 1994), Fagonia L. (Nair & Gupta, 1961), Zygophyllum L. (Masand, 1963), and Krameriaceae (Verkerke, 1985a); those of Zygophylla- Ceae are associated with an endothelium. The micropyle A ns eu 1934; Kamelina, 1985), but a nome micropyle is ites (Boesewinkel, 1994), The outer integument is thicker than the inner in both families — (Verkerke, 1985a; Boesewinkel, 1994), volume 97, Number 4 2010 Endress Evolution in Eudicots and Their Major Subclades gure 6. e S, [ subgroups of t iii gales. A- 6. P; sal etic a L.). D, E. Polygalaceae Cuc gprs , and F oe 1 = a E-G. Polygalaceae and Fabaceae with conspic mb T e etric Midi: rneby (photo by Brigitte Marazzi). —G. x ifolia T s s Manas, gonia > i (rh sp., male and female ies: —K. Cu a inflorc gus ban (Colenso) Cockayne, male infos scence, wind pollinated). NITROGEN-F : zm EN-FIXING CLADE (FABALES, ROSALES, -UCURBITALES, FAGALES) oe clade is made up of all four cot ne nitrogen-fixing bacteria occur in the i k some re presentatives. To date, it is not features. la Pepe e the clade by floral struc tural "pig e orders there are groups with reduced, $, wind-pollinated, structurally unisexual Fabales. Ca eesalpisioide ( (C aesalpinia pulcherrima (L.) Sw. Vigna carac alla (L. Datiscaceae n cannabina e urbitaceae (Marah ddnde poses LN scence, wind pollinated). —M. Fagaceae (Fagus e L. in flower — in ar A-C. Fabace ae. Diversity y —B. Mimosoideae ne feuillei DC.). —C. D. X m octandrum (F. Muell.) Domin. oe Polygala LS flowers. —F. € —Ó (H lerb.) I E K. Cucurbitales. —H. Coriari: j e flower, wind vallisased). ix Beg Fagales. —L. female flowers with uniovulate carpels or gynoecia ( (least in Fabales) (Endress & Matthews, 2006b). Synsepaly is relatively common. In both | (Fagales and the subclade e former Urticales), the presence of he inflorescences is noteworthy (i.e. that form compact bodies). Fagales (Fagaceae erhaps Myricaceae) arger groups w ith reduced flowers of Rosales consisting of th coenosomes in t cymose branching systems They are present as the cupules in [Fig. 6M]. Nothofagaceae, and per Annals of the Missouri Botanical Garden (Macdonald, 1980; Fey & Endress, 1983; Rozefelds & Drinnan, 2002) and as the congested, sometimes flat or urceolate, inflorescences of Moraceae and Urtica- better, non-porogamy) associated with delayed ovule maturation is known from several Fagales (Sogo & Tobe, 2008) and from single Rosaceae and Ulmaceae (Nawaschin, 1898; Murbeck, 1901; Shattuck, 1905). us ovules occur in Juglandaceae and Myricaceae (Fagales) and Urticaceae (Rosales). Uni- tegmic ovules and ovules with vascular bundles in the integument(s) are known from representatives of all four orders. In bitegmic ovules, the outer integument is usually thicker than the inner. In addition, in some taxa the inner integument is retarded compared to the outer and does not contribute to the micropyle (many Fabaceae from all major subgroups, Prakash, 1987; Polygalaceae p.p., Verkerke, 1985b; Rhamnaceae (Rosales), Arora, 1953; Begoniaceae, Datiscaceae (Cucurbitales), Matthews & Endress, 2004). FABALES Fabales are one of those completely new orders derived from recent molecular phylogenetic studies (Bello et al., 2009). It consists of four families (Fabaceae, Polygalaceae, Quillajaceae, Surianaceae) that have not been together in earlier classifications (the relationship of the two larger families Fabaceae and Polygalaceae was first recognized by Chase et al., 1993). Fabaceae and Polygalaceae are characterized by monosymmetric flowers, in many cases complex keel flowers with the reproductive organs hidden in the lower petals, but with different organization (Fig. 6C-G) (Endress, 1994; Westerkamp & Weber, 1999: McMahon & Hufford, 2002, 2005; Prenner, 2004a; Lewis et al., 2005; Tucker, 2006; Sokoloff et al., 2007b; Bello et al., 2010) and secondary pollen presentation at the tip of the keel. Fabaceae are one of the most species-rich and most diverse angiosperm families. In addition to keel flowers (Papilionoideae), brush flowers with long stamens and short petals (Mimosoideae) and more open flowers with expanded petals are present (caesalpinioids, not monophyletic) (Fig. 6A-C) (Polhill & Raven, 1981; Tucker, 1987, 2003; Herendeen et al., 2003). In both families of Fabales with monosymmetric flowers, Fabaceae and Polygalaceae, asymmetric flowers occur as a further elaboration (Fig. 6E-G) (Westerkamp, 1993; Wester- kamp & Weber, 1999: Prenner, 2004a, b; Marazzi et al, 2006; Marazzi & Endress, 2008). Synsepaly is present in many Fabaceae and in Stylobasium : (Surianaceae) (Carlquist, 1978). Petals have narrow bases and tend to be conspicuously delayed in early development (Polygalaceae, Prenner, 2004a; Faba- ceae, Tucker, 2006; Quillajaceae and Surianaceae, Bello et al., 2007). Free carpels are common, except for Polygalaceae (Bello et al., 2007); a single carpel occurs in almost all Fabaceae and in three of the five genera of Surianaceae (Schneider, 2007). Ovules are commonly crassinucellar, bitegmic, and often anatro- pous, but in Surianaceae (Heo & Tobe, 1994) and many Fabaceae, they are campylotropous (Prakash, 1987). A chalazal endosperm haustorium is common in Fabaceae (Prakash, 1987) and also occurs in some Polygalaceae (Rao & Roy, 1981) and Surianaceae (Heo & Tobe, 1994). Zigzag micropyles are present in many Fabaceae (Prakash, 1987) and Polygalaceae (Verkerke, 1985b). Seeds with arils occur in a number of Fabaceae and Polygalaceae. ROSALES The major phylogenetic split in Rosales is between (currently four families) and a clade of Barbeyaceae, Dirachmaceae, Elaeagnaceae, and the perhaps poly- phyletic Rhamnaceae (Sytsma et al., 2002). Petals, if present, have a narrow base. However, there are relatively many Rosales that lack petals, such as all families of the former Urticales, Barbeyaceae, Elaeagnaceae, and some Rhamnaceae and Rosaceae; many of these have completely unisexual flowers and are wind pollinated. Haplostemony is predominant (all families of the former Urticales, Barbeyaceae, Di- rachmaceae, Rhamnaceae, most Elaeagnaceae, and some Rosaceae). However, in Rosaceae, polystemony including several stamen whorls and beginning with a complex whorl by double stamen positions is predominant (Murbeck, 1941; Kania, 1973; Linden- hofer & Weber, 1999). Presence of a single crassinucellar, anatropous ovule per carpel or per gynoecium is common (former Urticales, Shattuck, 1905; Fagerlind, 1944; S. P. Singh, 1954; Barbeya- ceae, Dirachmaceae, and Elaeagnaceae, Ronse De Craene & Miller, 2004; Rhamnaceae, Prichard, 1955: Rosaceae, Juel, 1918). The largest family, Rosaceae, has a considerable diversity of floral forms, with or without petals, with a varying number of stamen whorls, with carpel number ranging from one to several hundred (and then in several whorls), carpels ee or united in the ovary, and ovary varying from superior to inferior. : Volume 97, Number 4 2010 Endress Evolution in Eudicots and Their Major Subclades CUCURBITALES AND FAGALES In Cucurbitales and Fagales there is a trend toward trimerous and dimerous flowers in some families that is sometimes associated with the absence of petals, completely unisexual flowers, and wind pollination (Fig. 6H—M). Trimerous and dimerous flowers occur in Nothofagaceae, Fagaceae, and Betulaceae among Fagales, and in Datiscaceae, Begoniaceae, and Cucurbitaceae among Cucurbitales. Petals are absent ae, Begoniaceae, and some Anisophylleaceae and Ce nene (Matthews et al., 2001; Matthews & Endress, 2004). If petals are present, they are always pointed (Matthews & Endress, 2004). Unisexual flowers uniformly occur in all Fagales and consistently or partly in each family of Cucurbitales (Matthews & Endress, 2004; Garnock-Jones et al., 2007). However, Cretaceous Fagales and Cucurbitales may have had bisexual flowers (Friis et al, 2006b) and thus unisexual flowers may not be a synapomorphy for this subclade, and wind pollination may have evolved separately several times (Manos et al., 2001; Oh & Manos, 2008). Inferior ovaries are predominant in both orders. In addition, sometimes the flowers have a neck, a long intercalated zone between the base of the outer floral organs and the inferior ovary (Cucurbita- ceae, Fagaceae). A tendency to form long, unifacial stigmatic branches occurs in both orders e families in Cucurbitales, Matthews & Endress ; Betulaceae, Endress, 1967). In addition, misis lobes are bifurcate in several families of Cucurbitales and in some Juglandaceae of Fagales (Manning, 1940; Matthews & Endress, 2004). In the ovules, there is a trend to unitegmy (most Fagales, partly in Coriar- iaceae and Anisophylleaceae of Cucurbitales) (Mat- thews € Endress, 2004). Fagales have a rich Cretaceous floral fossil record indicating a high diversification of flowers at that time (Herendeen et - 1995; Sims et al., 1999; Schónenberger et al., 2001; Friis et al., 2003, 2006a, b; Takahashi et al., 2008) COM CLADE (CELASTRALES, OXALIDALES, AND MALPIGHIALES) The COM clade (informal name introduced by Endress & Matthews, 2006b) is a well-supported “aoa (Soltis et al., 2000; Wurdack & Davis. 2009). There is a tendeney to form fringed or lobed petals or staminodes (Endress & Matthews, 20062). In three orders, there are some instances with the petals Postgenitally united at the base (in some by eae and Connaraceae, Matthews & hooks) (Celastraceae, Matthews & Endress, 2002; Euphorbiaceae, Kapil. 1956; Lina- ceae, McDill et al., 2009). Heterostyly is present in two families of Oxalidales (Connaraceae, Lenza et al., 2008; Oxalidaceae, Luo et al, 2006) and in four families of Malpighiales (Clusiaceae, Lloyd & Webb, 1992; Linaceae, McDill et al., 2009; Erythroxylaceae, Del Carlo & Buzato, 2006; Tureraceac, Shore et al» 2006), n tristyly occurs in both orders (Canders, 19, A tendency of ie a TW to is MS suni d EDU IUE QC adi tenuinucellar (or weakly crassinucellar) with an endothelium, while such ovules are largely lacking in other rosids (also present in some Brassicales) (for more details of their distribution, see Endress & Matthews, 2006b). Even if the ovules are crassinu- cellar, they are relatively narrow and often have an endothelium (Endress & Matthews, 2006b). Equally interesting is that the inner integument is mostly thicker than the outer (see also below). Ovules are mostly anatropous. Seeds with arils are relatively common (Endress & Matthews, 2006b). For a discussion of additional features, see Matthews and Endress (2005a). CELASTRALES Parnassiaceae are close to Celastraceae in floral morphology (Matthews & Endress, 2005a) and have been incorporated into them (APG, 2009). The third family, Lepidobotryaceae, is more distinct. Flowers y small. In Lepidobotryaceae and many are not retarded in n and they become the protective organs in floral bud (Matthews & Endress, 2005a). Stamens form a single antesepalous whorl, but not in Lepidobotryaceae. There š are p inantly three carpels. Stigmas are commi ssural, but not in Lepidobotryaceae. The ventral slit of the carpels is p connected by long, interlocking epider- cells, and the pollen me tract is cell verse section iub & layers as seen in transv y form conspic- Endress, 2005a). Nectaries uous discs. OXALIDALES The order consists of six families and is well edominantly isomerous supported. The flowers have pr whorls (thus more than three carpels). Sepal aestiva- tion is commonly valvate. and the sepals are Annals of the Missouri Botanical Garden postgenitally connected (but quincuncial imbricate in Oxalidaceae and Connaraceae) (Matthews & Endress, 2002). Obdiplostemony is common. The pollen tube- transmitting tract is commonly restricted to a single cell layer around an open canal (Matthews & Endress 2002). Placentation is always axile. Most commonly there are two or slightly more ovules per carpel. Ovules are commonly bitegmic and anatropous, but hemitropous or orthotropous ovules occur (however scarcely) in some Oxalidaceae, Connara- ceae, Cunoniaceae, and Elaeocarpaceae (Matthews & . The micropyle is commonly formed by both integuments (Matthews & Endress, 2002). MALPIGHIALES Malpighiales are the 1 Ear f 1 i terms of families (36 in APG, 2009, 40 in Wurdack & Davis, 2009). The families are more or less well supported; however, the topology of families within the order is poorly resolved, except for a few small groups of families (Davis et al, 2005; Tokuoka & Tobe, 2006; Korotkova et al, 2009: Wurdack & Davis, 2009). Two of these subclades, Chrysobalana- ceae sl. with five families and Rhizophoraceae s.l. with ca. six families, were the first to be comparatively studied in floral structure (Merino Sutter & Endress, 2003; ews & Endress, 2008, in prep.. The realization of the position of the giant-flowered esiaceae within Malpighiales, close to the small-flowered Euphorbiaceae (Davis et al, 2007, 2008; B al, 2008; Davis, 2008), was surprising, and comparative studies on the floral structure will be necessary to understand the evolution of Rafflesiaceae. ora! monosymmetry is present in at least 11 families (e.g., do Carmo E. Amaral, 1991; Matthews & Endress, ; Zhang et al., 2010). Glands on the outer sepal surface are known from several families. They are probably mainly nectaries, but in the South American Malpighiaceae they are oil glands essential in pollination biology (Vogel, 1974). occurs in several families. It can be centrifugal or bidirectional, which, e.g. allows distinction of Salicaceae from Achariaceae, both former components of the defunct Flacourtiaceae (Bernhard & Endress, 1999). Synandry occurs in representatives of more than 10 families (Matthews & Endress, 2008). A trend to form stamen fascicles is present in several families (Fig. 7A-C) (Euphorbiaceae, Prenner et al., 2008; Clusiaceae, Leins & Erbar, 1991; Stevens, 2007; eeney, 2008; Hypericaceae, Leins, 1964; Rhizo- phoraceae, Breteler, 2008). Although incompletely tenuinucellar or weakly crassinucellar ovules with an endothelium are reported from at least 19 families, Polystemony crassinucellar ovules without an endothelium also occur in at least 15 families. Antitropous ovules (Endress, 1994), usually combined with an obturator, are recorded from at least 17 families (e.g., Merino Sutter et al., 2006). A nucellar beak is common in the earlier Euphorbiaceae s.1., which are now distributed to several families (present in Euphorbiaceae and Phyllanthaceae, Sutter & Endress, 1995, and Picro- 006 vascularization of the integument(s) (present in taxa of Euphorbiaceae, Phyllanthaceae, Picrodendraceae, and Putranjivaceae; Merino Sutter et al., 2006). Arils pear to occur, especially in combination with crassinucellar ovules. MALVIDS (EUROSIDS ID Core malvids are made up of Brassicales, Malvales, Sapindales, and the recently recognized Huerteales (Worberg et al., 2009). Huerteales are very poorly known in terms of floral structure. The recent additio of Geraniales, Myrtales, Crossosomatales, and Pi- ang et al., 2009) is still not well supported molecularly. Nevertheless, malvids are easier to characterize in floral structure than fabids, even with the addition of the four non- core orders. Furthermore, mitochondrial DNA sup- ports a relationship of the COM clade with malvids Zhu et al, 2007; Qiu et al., in press), which was earlier suggested based on floral structure (Endress & Matthews, 2006b). However, this relationship was not found in Burleigh et al. (2009) and H. C. Wang et al. (2009) — In Pieramniales, Sapindales, Huerteales, and many Brassicales, small flowers are predominant. Function- ally unisexual flowers are also common. Multiple evolution of monosymmetric flowers (but commonly not very elaborate monosymmetry) occured in core malvids and again in Myrtales and Geraniales (Fig. 8A—L). Except for Fabales which have elabo the trend to monosymmetry is restricted to malvids, including the newly extended malvids and some Malpighiales (Endress, 1992, in prep.; Zhang et al., 2010). Monosymmetry tends to be oblique (i.e., not in the median plane) in some Sapindales and Brassicales (Ronse De Craene & Haston, 2006), as well as in Malpighiales (Matthews & Endress, 2008). Contorted petal aestivation is relatively common in core malvids and in Geraniales, Myrtales, and Malpighiales (Endress & Matthews, 2006b). A trend to form polystemony is conspicuous, not only in core malvids, but also in Myrtales and Malpighiales (Fig. 7). In addition, polystemony with stamen fascicles is present in ` Malvales (Malvaceae, Nyffeler & Baum, 2001; von — Volume 97, Number 4 2010 Endress Evolution in Eudicots and Their Major Subclades igure T. gabriellae Bail EI orbiace:z re . caeca ( ; . Euphorbiaceae (Ricinus communis L.). ce Lophostemon confertus (R. Br.) M ot m chrysantherus F. Muell.). G-I. Malv E A (Pachira aquatica Aub rales. —G. l pe ss 2008, 2006), Myrtales (Myrtaceae, Rey oophore oe 2005), plus Mal pighiales (see above). Es " Kodkpaynaphore (e. a stipe below the D aa s Nm is preferentially found in fiin: i Ë the malvids (Fig. 8M-Q), but is also Miel nc rossosomatales. Gynoecia with three s eu common, but there is also a trend to core sr. - ith more than five carpels in a whorl in al., 2008) a ee Heel, 1995; Endress, 2006; Janka et Malpighial ^ this is also represented in Myrtales and ghiales (Endress & Matthews, 2006b). In several BN a. apindales) plus Crossosoma- ea ke e mr are largely free, but as a compensa- Meal y Hue internal compitum they become sg E used at the tip, which allows the a secondary compitum (Endress et al., 1983: : Matthews & Endress, 2005b; Bachelier & Malvids and potentially related groups. Stamen fa Peter G. Wilson & J. T. Wat .). —L Malvaceae-Bombacoideae (Fremont A—C. Malpighiales. —A, B. Clusiaceae ( Montr D-F. Myrtales. —D. Myrtaceae (Beaufortia sparsa R. Br S ] ascicles. ouziera ). —E mid). —F. My rtaceae ^D e r. calife erh.) (photo by Rudolf Sc Malvaceae—Bombacoideae (Bombax v.) > )uonopozens eau xlendron yrnicum Endress, 2008, 2009). Many groups of core malvids and some Geraniales, Myrtales, and Crossosomatales share campylotropous ovules with (Endress & Matthews, 2006b). An especially interest- is the relative thickness of the two of the ovules. In malvids and the COM the inner integument is commonly thicker than it is the other way around (Endress & a zigzag micropyle ing feature integuments clade, the outer; in the other rosids or both integuments are equally thick Matthews, 2006b). The rare and striking Penaea type of four quartet modules, in 2003) is. among embryo sac development (with the sense of Friedman & Williams. nown from malvids, such as Kamelina & Konnova, Stephens, 1909), and angiosperms, only k Sapindales (Biebersteiniaceae, 1990) and Myrtales (Penaeaceae, from Malpighiales (Euphorbiaceae, Johri & Kapil, 1953; Malpighiaceae, Singh, 1961). = 557 558 Annals of the Missouri Botanical Garden Figure 8. (Aesculus carnea Zeyher). —B. S Sapindaceae pte pinnata Comm. ex Rutaceae ii cda eius (Lindl.) Planch e eb.). — Lam.). gey eae (Moringa e. tam: a Zu Capp violacea L.). —I-L. Malvales. —] dada. pentadactyln La arreat). —K. Malva (Hibisc "n ed dis Bis “ee e M-Q. f thr order t hauc — + —). ue 'aceae (Lunaria redivi -). —P. Sapindales: Malvales: bass (Firmiana lips * Wight). GERANIALES Geraniales consist of three to six families, of which Geraniaceae and Melianthaceae are the most prom- inent ones. Petals are commonly retarded in develop- ment up to anthesis. There are as many carpels as sepals (mostly five or four) (Ronse De Craene & Smets, 1999; Ronse De Craene et al., 2001). Ovules are crassinucellar and anatropous (Melianthaceae. Mauritzon, 1936; Ledoc 'arpaceae, Boesewinkel, 1997 or M (mostly Geraniaceae, Boesewinkel & Been, 9; Vivianiaceae, Boesewinkel. 1997). The two Miser: tend to be equally thick (three cell layers each) (Boesewinkel & Been, 197° 9: Boesewin- kel, 1988 1997). Nectaries are on staminode-like = Malvids. A-L. Monosymmetric flowers in families —H. Brassicales. alvac ae-Byttnerioideae (Kleinhovia hospita L.). Rutaceae M e albiflora (Hook) Meisn.). — of three orders. —A-D. Sapindales. —A. DM eae Ln —C. Ruta —D. ceae (Dictamnus albus . Tropaeolaceae ( Troy govern vatum eae (Capparis micracantha DG). v Cleomaceae (Cleome —J. Mist Bombacoideae eae—Helicteroideae (Helicteres sp.). —L. Malvaceae—Malvoideae Flo owers or young fruits w m pm ed ey nophores i in families Cleomaceae (Cleome gynandra L .). —N aradoxum E ndl.) m ). organs (Melianthaceae: Greyia Hook. & Harv. and Francoa Cav.) or on the outer base of stamens (Geraniaceae) (Ronse De Craene et al., 2001) MYRTALES yrtales comprise nine to 13 families, with Cube eae basal (Sytsma et al., 2004). Sepals are valvate (in at least six families). Petals are sometimes extremely retarded in bud and have a narrow base. Often there is an extensive floral cup, with the result that the insertion areas of the narrow petals are far apart from each other (e. £.. Schónenberger & Conti, 2003). Stamens tend to be incurved in bud (Dahlgren Volume 97, Number 4 2010 Endress Evolution in Eudicots and Their Major S & Thorne, 1984). Polystemony is common (Fig. 7D—F) and is based on centripetal stamen initiation (Mayr, 1969; Leins, 1988; Bohte & Drinnan, 2005; Kadereit, 2005; Leins & Erbar, 2008). Carpels are united up to the stigma; stigmatic lobes are commissural in Onagraceae (Mayr, 1969) and Penaeaceae (Rao & Dahlgren, 1968; Schónenberger & Conti, 2003). The ovary is mostly inferior, and, in addition, there is a neck (a long intercalated zone between the base of the outer floral organs and the inferior ovary) in some Combretaceae (Tiagi, 1969) and Onagraceae (Carl- quist & Raven, 1966). Ovules are crassinucellar, often campylotropous, and the two integuments are regu- larly equally thick (two cell layers each) (e.g.. Tobe & Raven, 1987, 1990, 1996). CROSSOSOMATALES Crossosomatales contain seven or eight families that were scattered in very different orders before it was recognized that they formed a clade (Nandi et al., 1998; Savolainen et al., 2000; Cameron, 2003; Sosa & Chase, 2003; Oh & Potter, 2006). In contrast to Geraniales and Myrtales, petals tend to be protective in bud (Matthews & Endress, 2005b). Sepals are imbricate, with the outer smaller than the inner. Flowers tend to have a floral cup. So-called pollen buds (intine protrusions at the apertures) are common (Matthews & Endress, 2005b; Oh & Potter, 2006). above the ovary (except Stachyuraceae), but most fuse postgenitally toward the tip, forming an extragynoecial compitum (Matthews & Endress, 2005b; Oh & Potter, 2006). Th : EJES 1 aah DC st ea stalked (gynophore or stipe). Ovules are crassinucellar and tend to have relatively long integuments forming a l the inner (Matthews $ Endress, 2 present in several families (Matthews $ Endress, 2005b) PICRAMNIALES Picramniales are a new order (APG, 2009) based on a single family erected by Fernando and Quinn (1995). Detailed floral morphological studies are Ñ lacking. Flowers are minute and unisexual. Perianth and androecium comprise 3- to 5-merous whorls. The &ynoecium is 2- or 3-carpellate, syncarpous. with two ovules per locule (Fernando & Quinn, 1995). E SAPINDALES x A indales consist of nine families, including E _ basal grade of Biebersteiniaceae and Nitrariaceae and a poorly resolved core clade (Muellner et al., 2007). Functionally unisexual flowers appear to be common (e.g., Harms, 1940; Renner et al., 2007; Bachelier & Endress, 2007, 2008, 2009), combined with hetero- dic at least in Kirkiaceae and Sapindaceae. A trend toward floral monosymmetry is present (Fig. 8A—D). Petals tend to be the protective organs in floral E 3 dA kh 1 + sc si Manli incurved tips (Bachelier & Endress, 2009). The ovary is commonly superior. The presence of one or two ovules per carpel is predominant. Ovules are crassinucellar, relatively many are campylotropous, and in four families pachychalazal ovules occur (e.g.. Corner, 1976). They are commonly bitegmic, but unitegmic ovules have been reported in at least four families of the core clade (Wiger, 1935; Boesewinkel & Bouman, 1978; Bachelier & Endress, 2009). = HUERTEALES The flowers in this new order of three families are very poorly known apart from the original species descriptions (Worberg et al., 2009) (see also under Eurosids). Only female flowers of Perrottetia were described in more detail (Matthews & Endress, 2005a). Flowers are small and unisexual. A floral cup is common. There are one or two ovules per carpel BRASSICALES Brassicales, the glucosinolate-producing order, at present contains 17 families (APG, 2009), eight or nine of which form the core Brassicales (Hall et al., 2004). A trend toward floral monosymmetry is present (Fig. 8E—H). Floral dimery associated with double organ positions in corolla and androecium, and sometimes increase in carpel number, are character- istic for a group of families in the core Brassicales (Er , 2002; Ronse De Craene & Haston, 2006). whereas the basal state in the order is probably pentamery (Ronse De Craene, 2002; Ronse De Craene & Haston, 2006). Unisexual flowers regularly occur in several families (e.g.. Hall et al., 2004). -— M protective o in floral bud and petals are often retarded š ¿askiwa (pers. obs.; Ronse De Craene Annals of the Missouri Botanical Garden lot l iil i i 1 especially in the cae Damecales, whorcas basal families teal have anatropous ovules (Tobe & Raven, 2008). The inner integument is thicker than the outer in most of the core Brassicales, whereas the reverse is the case in the basal groups. Limnanthaceae have only one integument (Maheshwari & Johri, 1956). Ovules with Brassicales (Tobe & Raven, 2008). Arils occur scattered in at least six families. MALVALES Malvales currently embrace 10 families (APG, 2009). A trend toward floral monosymmetry is present, especially in Malvaceae (Fig. 8L-L). Polystemonous androecia with centrifugal stamen initiation on a ring meristem or on five sectorial primordia are common (Fig. 7G—I) (Malvaceae, van Heel, 1966; von structure (von Balthazar & Nyffeler, 2002). Thus the valean androecium is a hot spot region of evolutionary events. For gynoecium structure, see the discussion under Malvids. Ovules are crassinu- cellar and the micropyle is formed by both integu- ments and often has a zigzag shape. However, in Cistaceae and Dipterocarpaceae (Nandi, 1998b) and Cytinaceae (Igersheim € Endress, 1998), ovule curvature is weak and they ceae, Dipterocarpaceae, and Sarcolaenaceae (Nandi, 1998b), which form a subclade in Malvales (Nickrent, 2007); it was found also in Sphaerosepalaceae and Thymelaeaceae (Horn, 2004). There is a vascular bundle in the outer integument in some Dipterocar- paceae (Rao, 1955) and Malvaceae (Rao, 1954). Nectaries are present in the form of carpets of multicellular hairs on the upper surface of the sepals or adjacent areas in many Malvaceae, (Vogel, 2000) or in the form oÍ dises in Cytinaceae, Muntingiaceae, and Sarcolaenaceae (Vogel. lacking altogether in Bixaceae and most Cistaceae and Dipterocarpaceae, which produce only pollen as a reward (Vogel, 2000). Apodanthaceae (earlier Raf- flesiales) are a parasitic family with uncertain position (APG, 2009), fluctuating between Malvales (Nickrent, 2002) and Cucurbitales (Barkman et al., 2007). Apodanthaceae share three almost unique characters with Malvales but nothing of comparable distinction with Cucurbitales: the androecium has an athec. organization and forms a congenitally uniform tube around the style, and a carpet of unicellular to multicellular hairs is present on the inner base of the perianth organs (Blarer et al., 2004). Thus structural features support a position in Malvales. ASTERID LINEAGE S.L. The asterid lineage s.l. has a basal grade of five orders and two major large clades, the lamiids and campanulids. Although the composition of the orders is well supported, the exact position of Berberidopsidales, Santalales, and Caryophyllales is still not clear, and therefore they are not included in asterids s. str. (APG, 2009). All eudicots with a free central placenta bearing more than one ovule are in this clade (perhaps except for Podostemaceae). In the ovules there is a tendency toward a thin nucellus. Crassinucellar ovules are rare in the asterid lineage sl. (only in Caryophyllales crassinucellar ovules are common, in addition to weakly crassinucellar ovules). More common are weakly crassinucellar, incompletely tenuinucellar, tenuinucel- lar, and reduced tenuinucellar ovules. It is of special interest that this is also true for Santalales and Caryophyllales with their unsettled position. The ovules are unitegmic, except for some basal clades (bitegmic in most Caryophyllales, a few Santalales, many Ericales, and two unplaced families in lamiids: Vahliaceae and perhaps Icacinaceae, see below). If there are two integuments, the micropyle is consistently formed by the inner one (Berberidopsidales, Mauritzon, 1936; van Heel, 1977; Kubitzki, 2007; Santalales, Fagerlind, 1948; Caryophyllales, Eckardt, 1976; Ericales, e.g. Tsou, 1994; Vahliaceae, Raghavan & Srinivasan, 1942). BERBERIDOPSIDALES Of the two families in Berberidopsidales, the floral structure of Aextoxicaceae (Kubitzki, 2007; Ronse De Craene & Stuppy, 2010) appears quite different from that of Berberidopsidaceae (van Heel, 1977; Ronse De Craene, 2004). The enigmatic genus Streptothamnus, a possible additional member of the order, is insufficient- ly known (Ronse De Craene, 2004). Berberidopsidales are therefore difficult to characterize at this point. SANTALALES Santalales are an order of mainly parasitic plants in seven families (Malécot & Nickrent, 2008: APG, 2009). The flowers are in general small and inconspicuous, ted Loranthaceae. Petal volume 97, Number 4 2010 Endress 561 Evolution in Eudicots and Their Major Subclades aestivation is consistently valvate. Nectaries, if present, are lobes or rings around the gynoecium. There are various trends of reduction in floral organization. In the first trend the perianth is affected. The sepals, still equal in size to the petals in some Olacaceae (Endress, become small and disappear, and the petals have both protective and attractive functions. In the extreme case (female flowers of Balanophoraceae), the entire perianth disappears (Endress, 1595: Venti & Ronse De C raene, 2009). I th affected. At first the ovary septa, then the ibtd then the ovules (Fagerlind, 1948), and finally the entire inner morphological space of the gynoecium gradually disappear (Balanophora J. R. Forst. & G. Forst., Fagerlind, 1945b). Only some Olacaceae still have two integuments (Fagerlind, 1948). The other groups are Ram, 1959a, b), or lack ovules (some Loranthaceae, Johri & Fhainagar, PO The pe = a Mec anl I š x d, 1947; Bhatnagar & Sabharwal, 1969) or incompletely tenui- nucellar (Ram, 1957). Chalazal endosperm haustoria occur in all families (in Loranthaceae already the embryo sacs behave like haustoria); in some families micropylar haustoria also occur (Skottsberg, 1913; Maheshwari et al., 1957; Swamy, 1960; s 1961; Bhatnagar & Sabharwal, 1969). Molecular phylogenetic studies recently showed that Balanophor- aceae are part of Santalales (Nickrent et al., 2005). However, this systematic position has long been quite clear from the unique reduction of the gynoecium and the uniquely bent embryo sac. In Santalaceae, the reduction of the inner part of the ovary results in sharp ing of the embryo sac as it grows from the short ovule into the placenta. In Balanophora, although the inner morphological surface has completely ek and seed are formed, this sharp wH is retained (figures in Johri & Bhatnagar, 1961). This is an example of an unusual evolutionary trend and a unique structural feature for prediction of relationships between Balano- Phora and Santalales. Further support is provided by the male flowers, which have a valvate perianth and synandria as in some Santalaceae (Endress & Stumpf, : 1990. Eberwein et al., 2009). 3 CARYOPHYLLALES Caryophyllales in the current circumscription mint of. two major subel (1) the classical ades: x Caryophyllales s. str. (Centrospermae) and (2) a newly circumscribed subelade added later (Albert et al., 1992). Two families of the latter, Polygonaceae and Plumbaginaceae, were also sometimes posi close to Caryophyllales earlier. Caryophyllales s. str. are well characterized by floral structure (Eckardt, 1976; Hofmann, 1994), especially their uniform and unique ovule structure (campylotropous, with both integuments often only two cell layers thick, micro- pyle formed by the thickened rim of the inner integument, air space between the outer and inner integument at the base, nucellar cap, perisperm) (Rocén, 1927; Eckardt, 1976), whereas the second subclade has fewer conspicuously shared floral ER s (campylotro- n Frankeniaceae, Walia & Kapil, 1965). rene. in both subclades there is a trend to form imerous or trimerous Met with late closing ovaries and a single basal ovule (Amaranthaceae, Hakki, 1972; Basellaceae, Sattler & T 1988; Caryophyllaceae, Hofmann, 1994; Nyctaginaceae, Rohweder & Huber, 1974; Phytolaccaceae, Eckardt, 1955; Plumbaginaceae, De Laet et al., 1995; Poly- , De Laet et de 1995). Ovules commonly have has funicles (Amaranthaceae, Ronse de Craene et al., 1999; Cactaceae, Leins € Schwitalla, 1985; Caryophyllaceae, Rohweder, 1970; Nyctaginaceae, Rohweder & Huber, 1974; Plumbaginaceae, De Laet et al., 1995; Polygonaceae, Solntseva, 1983), equally thick integuments, and the micropyle formed by the inner integument, which has a thickened rim. The second subclade tends to have contorted petal aestivation As s usalskes; Caryophyllales are also character- ized by a simple perianth in many families. but in ceae, Nyctaginaceae, tulacaceae, some Caryophyllaceae, and, in the second clade, Nepenthaceae and Polygonaceae. Apetaly is most likely basal in Caryophyllales and petals have arisen more than once in the order (Brockington et al.. 2009). In some families, the colored perianth organs to — to dinis Nyctagi ., Phytolaccaceae, Portula- caceae) pe & Huber 1974). In the derived ortulacaceae androecium-related petals) are initiated centrifugally et al., 2001). Nectaries, if Annals of the Missouri Botanical Garden Figure Asterids. systematic dibus E F. Col — haceae (Pachystachys lutea Nees). —C. La IE Asteraceae (Carlina acaulis El Areas gya ranges aspera a -Ham. ex D. Don). —H. R udanthia with radiating colored L Api aceae (Orlaya grandiflora “ (Hieraci ium murorum L.). ) Hoffm.). — ASTERIDS Asterids show predominant sympetaly, and also a higher occurrence of synsepaly than rosids. However, synsepaly is unstable and often varies at the family or genus level. Unitegmic, incompletely tenuinucellar ovules with an endothelium are predominant. Endo- sperm haustoria are widespread. high Flowers exhibit synorganization of floral organs, with peaks in (1) Gentianales (Apocynaceae with fusions between almost all organs and pollen transport with translators), (2) Lamiales (highly specialized lip flowers in several families), and (3) Asterales (Asteraceae and relatives with postgenitally fused anthers and elaborate pollen release As a consequence of high organ eynorgsnisation. in some groups there is secondary pollen presentation, with at least three main occurrences: in some Ericales (especially epacrid Ericaceae, e e-8., MeConchie et al., 1986), in Gentianales (Loganiaceae, Erbar & Lom. 1999, and Rubiaceae, Igersheim, 1993: Puff et al., ored bracts (across all major subclades of asterids). —A. Te miaceae (Monarda punctata L.). — F-H. Colored sepals (especi ually —G. peripheral organs of three o kinds and with different eae (Cornus canadensis L.). ges eae pue i Lj. in Comales md bawa of Gentianales). — hylla Š D humac k & m mn. ). Klotzsch). I-L. Colored and ai enlarged al (espec tially in campanulids). aprifoliaceae (Scabiosa lucida V ill.). — aceae Asteroideae (Leucanthemum vulgare Lam.). . Asteraceae—Cichorioideae 1996, and in a very unusual way by pollinia attached to translators in Apocynaceae, M. E. Endress, 2 01), and in Asterales (Asteraceae. Campanulaceae, Caly- ceraceae, Goodeniaceae) (Leins & Erbar, 2006). In addition to the floral organs in the flowers being highly integrated in various ways, the flowers in the inflorescences are often integrated in forming pseu- danthia as they are best known in Asteraceae. Three morphological patterns of pseudanthia may be systematic distributions (Fig. 9). The first pattern (Fig. OA-E) has qe bracts and is scattered over the entire asterids, — ven in some Aster e (e.g. Carlina L. and MA e Mill.) (Sc hnell. 1960; Napp-Zinn & Heins. 1979; Classen-Bockhoff, 1990; Funk et al., 2009). The second pattern (Fig. 9F-H) has increased sepals, either at the periphery of the inflorescence or everywhere (Weber, 1955; Schnell, 1960; Classen-Bockhoff, 1990, 1996); it occurs in some Hydrangeaceae of Cornales and some Rubiacae of Gentianales. The third pattern (Fig. 9I-L) is the | Volume 97, Number 4 2010 Endress Evolution in Eudicots and Their Major Subclades most integrated, with increased petals in flowers at the periphery of the inflorescence; the petals may be differentially inereased, i.e., the more peripheral they are, the larger they are. This pattern especially occurs in campanulids; it is the familiar situation in Asteraceae, but is also represented in Apiales (e.g., Orlaya Hoffm., Heracleum L.) and Dipsacales (e.g., Scabiosa L., Viburnum L.). It is noteworthy that the most species-rich clades of ids, Lamiales, Gentianales, and Asteraceae, have elaborate (except for Gentianales, which are mostly monosymmetric) flowers with practically uniformly two carpels. They also have the most extremely tenuinucellar ovules. Other asterids often have three carpels, more rarely five or even more, and more often incompletely tenuinucellar ovules. In a number of lades, the ovules are completely unvascularized, which need more comparative study. GRADE OF BASAL ASTERIDS The first two orders in asterids, Cornales and Ericales, which form a grade, have retained two whorls of stamens in several families, a trait that is otherwise extremely rare in asterids, known only in Dialypeta- lanthus Kuhlm. (Rubiaceae) and Paracryphiaceae. More often than in core asterids (euasterids) there are flowers with more than five sepals and petals in Cornales and Ericales (and also in some Gentianales and Apiales). There is also a trend to form polyandrous flowers in some clades of both orders. Flowers are polysymmetric with very few exceptions and never elaborately monosymmetric. Gynoecia predominantly have more than two carpels, mostly three to five. CORNALES Cornales have relatively simple flowers (except for Loasaceae), with the sepals often reduced, the petals protective and attractive, and valvate, and the stamens in one or two whorls. However, polystemonous flowers are present in most Hydrangeaceae (Hufford, 1998, 2001) and Loasaceae (Hufford, 1990, 2003), and in Hydrangeaceae with centripetal and centrifugal initiation patterns (Hufford, 2001; Ge et al., 2007). rior ovaries are common. es are never tenuinucellar, but mostly incompletely tenuinucellar, weakly crassinucellar, or even i llar (the latter in some Cornaceae [Kamelina & Shevchenko, 1988] and some Nyssaceae [Tandon & Herr, 1971). ERICALES Ericales comprise 22 or more families (Schónen- _ berger et al., 2005; APG, 2009), some of which form more or less well-supported subclades (numeration as in Schónenberger et al., 2005: 276: I, Marcgravia- ceae-Tetrameristaceae-Balsaminaceae; Il, Polemo- niaceae-Fouquieriaceae; III, the families of the former Primulales plus Ebenaceae plus Sapotaceae; IV, Diapensi Styracaceae-Sympl Va, Ericaceae-Cyrillaceae-Clethraceae; Vb, Sarracenia- ceae-Actinidiaceae-Roridulaceae). The flowers in Ericales are unusually diverse, and those of some subclades appear far apart from others at first sight but share structural patterns in detail (Schónenberger & Grenhagen, 2005; Schónenberger, 2009; Schónenberger et al., 2010). An extreme case is the basal subclade I of Maregraviaceae—Tetramer- istaceae— i : The unusually elaborate monosymmetric flowers of Balsaminaceae appear to be the result of a rapid and recent diversification and anagenesis (Janssens et al., 2009). However, floral synapomorphies with the related Marcgraviaceae and Tetrameristaceae are still present (Schénenberger et al., 2010). A trend to form polystemonous flowers is present in more than one subclade (Actinidiaceae, van Heel, 1987; Lecythidaceae, Tsou & Mori, 2007; Theaceae, Tsou, 1998). Subclade V p.p. has anthers that are inverted at anthesis and have porelike slits (Stevens et al., 2004). In subclade Vb, nectar is not produced (except for some Sarraceniaceae) and the flowers offer only pollen to pollinators (Schmid, 1978; Renner, 1989). Double positions of stamens Phyllotaxis) occur in Fouquieriaceae (Schónenberger & Grenhagen, 2005) and were also found in the Cretaceous ericalean fossil Paradinan- dra (Schónenberger & Friis, 2001). In subclade Ill. antepetalous stamens and a free central placenta are highly characteristic, and nectaries, if present, are unusual; a (small) disc around the ovary base is only known from Coris L. (Myrsinaceae). Otherwise, nectaries are either inconspicuous areas of the upper ovary wall (in the basal family Maesaceae and some Primulaceae) or form patches of secretory hairs eophrastaceae and some Myrsinaceae) (Vogel. 1997). Ericales have retained another primitive trait in some families: ovules with two integuments. In these ovules there is, in turn, another interesting pattern: in some families the inner integument is thicker than the outer, and in others it is the other way around. The first is the case in the families of subclade IH but not Sapotaceae (e.g.. Warming, 1913; Dahlgren, 1916; Subramanyam & Narayana, 1968; Rao, 1972). In the diverse family Balsamina- ceae, transitional steps between bitegmic and uni- i es are present (McAbee et al., 2005). The second is the case in more basal families of Ericales (e.g.. Tsou, 1994; McAbee et al., 2005). Ovules are often campylotropous and in most groups are Annals of the Missouri Botanical Garden incompletely tenuinucellar with endothelium; how- ever, in many Lecythidaceae (Tsou, 1994), Myrsina- 970), and Pentaphylacaceae (Ternstroemiaceae) (Tsou, 1995), an endothelium is lacking. In subclade Va and in Primulaceae and ae, the ovules are tenuin jayaraghavan, 1969). In at least seven families, but not in subelade Va, the outer or only integument is vascularized; only in some Theaceae the base of the inner integument is vascularized (e.g., Warming, 1913; Bhatnagar & Gupta, 1970; Tsou, 1994, 1997). Endosperm haustoria are mainly present in subclade Va but are absent in a number of other families (Judd & Kron, 1993). Ericalean flowers are unusually well represented in the fossil record of the Cretaceous, which indicates an early rich diversification in the order (Christophel & Basinger, 1982; Friis, 1985; Nixon & Crepet, 1993; Keller et al., 1996; Sché- nenberger & Friis, 2001; Crepet et al., 2004; Schénenberger, 2005; Friis et al., 2006a; Crepet, 2008; Martínez-Millán et al., 2009). EUASTERIDS Euasterids contain two large clades, lamiids and asterids, both conspicuously diversified at various d the families Rubiaceae (Gentianales) and Asteraceae (Asterales). specially conspicuous is the trend to form elaborate monosymmetric flowers in the Lamiales-Solanales clade and, in a different way, in Asterales (Aster- aceae, Campanulaceae), always combined with oli- gandry (Endress, 1990; Jabbour et al., 2008). LAMIIDS (EUASTERIDS 1) - Lamiids are in general characterized by late sympetaly, in which the petals are free from each other at initiation and become confluent later, as discussed by Erbar (1991) and Erbar and Leins (1996). However, this feature is probably a mere consequence of a superior ovary, which is present in most lamiids (see discussion on campanulids). This 1994), Rubiaceae (Erbar € Leins, 1996), and Sphenocleaceae (Erbar, 1995). Contorted petal aestivation is present in many lamiids with poly- symmetric flowers, whereas cochlear aestivation is common in monosymmetric flowers. An almost exclusive character of lamiids is a pollen sac placentoid (i.e., a parenchymatic longitudinal ridge protruding into each pollen sac from the center of the anther), as found by Hartl (1963). It is overwhelm- ingly present in Lamiales and is also found in many Solanales. In Gentianales, in some Gentianaceae a tapetal (and not parenchymatic) pollen sac placen- toid is present; the same occurs in Ixorhea Fenzl (Boraginales, Di Fulvio, 1978). Outside of lamiids, weakly differentiated tapetal pollen sac placentoids may be present in Escalloniaceae (Escallonia Mutis ex L. f., Kamelina, 1984) and Apiaceae (Phlojodi- carpus Turcz. ex Ledeb., Grevtsova, 1987), as seen from illustrations. The presence of numerous ovules on protruding diffuse placentae is common in all orders (except Garryales) but not ubiquitous in any of them. Vascular bundles in the ovule integument are largely absent (except for some Oleaceae and Convolvulaceae). Petaloid sepals, explosive flower opening, and buzz pollination, although not charac- teristic for lamiids as a whole, have sparsely evolved in several subgroups, whereas they appear to be lacking in campanulids. GARRYALES The flowers of the small order Garryales are unisexual, simple, and more or less reduced. Two of the three families (Garryaceae and Eucommiaceae) are wind pollinated and lack petals and nectaries. Eucommiaceae also lack sepals. Ovaries are inferior (not applicable for Eucommia Oliv. because of its lack of outer floral organs). Garryales have unusual ovules: they are crassinucellar (not just weakly crassinucellar) and the micropyle is curved in an anticampylotropous direction (curvature in th normal campyl common in asterids, but also occur here and there in other, mostly smaller, groups, such as some Cornales. Aquifoliales, and Solanales, and anticampylotropous curvature is also rare otherwise. V LAMIALES AND SOLANALES There is a conspicuous trend to form monosym- metric flowers, sometimes very elaborate ones. especially in Lamiales (Fig. 10) (Reeves & Olmstead, ~ Monosymmetry is especially expressed in corolla, commonly also in the androecium by- ————————m ——————————en— Volume 97, Number 4 2010 Endress Evolution in Eudicots and T Their Major Subclades Fi : x gure 10. Lamiales. Monosymmetric flowers. A-F. Entir ig vesneniaceae (Aesc : a preme (Digitalis 7J. Pollination organs Ma. chynanthus speciosus Hook.). purpurea L.). —E. / edian orientation of style a Postgenitally uni turgescent mida —H. Plantaginaceae (Digitalis purpurea L oriented tur TUER —. Plantaginaceae (Antirrhinum majus L., the anthe gescent filaments. —J. Linderniaceae (Torenia fournieri E. Fourn., contigu "uous by > x - y converging turgescent filaments). reducti crosa aiaa apper (median) stamen and much M" um the stamen pairs. Because the flanking iln Ls pass in the sy mmetry plane, T ME e stigma (Fig. 106-J). presence Bc. — stamen could easily obstruct allow bibens : o es pollination apparatus or not reduction of vt "a may explain the predominant large dn med ian stamen. This trend occurs ina ion of Lamiales and in Solanaceae. H is =C. Acanthaceae (Brillantaisia nitens Lindau). —F- anc . —€. 1 L Á] e alltiici e flowers. —A. Calceolariaceae (Jovellana violacea G. Don). Bignoniaceae (Tecomaria capensis (Thunb.) Spach). —D. Lamiaceae (Phlomis fruticosa L.). Gesneriaceae (Columnea sp., s of each of the two pairs ntiguous by converging rs of each of the two pairs contiguous by parallelly only one stamen pair present, the two anthers commonly associated with cochlear petal aestivation (i.e., imbricate with one organ completely outside and one inside). LAMIALES Lamiales are one of the large orders in lamiids, with families richly diversified. Phylogenetic several of its the studies have led to profound changes in Annals of the Missouri Botanical Garden umscription and arrangement of the families (Wagstaff & Olmstead, 1998; Olmstead et al., 2001; = 5 as n basal families tetramerous flowers appear to ide predominant (Oleaceae, Sehr & Weber, 2009; Tetra- chondraceae, Wagstaff, groups there are vi cones hilabiate flowers, with an popper aag lower à e the concave upper is (Fig. T em 1994; Weber, 2004; Westerkamp & Classen-Bockhoff, 2007). Ne nna qe aie d L stamen (as mentioned above) varies; sometimes it is » but it is consistently present at least as a h: in Gesneriaceae and genera of ea families: e Lamiaceae, Scrophulariaceae, and Plantaginaceae. A trend to form synthecal anthers (with the two thecae confluent over the apex) is exhibited in Gesneriaceae, Lamiaceae, Plantaginaceae, and Scrophulariaceae (Endress & Stumpf, 1990). In certain cases, the presence or lack of a median arg has indicated that a genus was wrongly placed. The enigmatic Rehmannia Libosch. ex Fisch. & C. A. a and Paulownia Siebold & Zucc. completely lack a median stamen (Endress, 1998; Fischer, 2004), which does not support a position in Gesneriaceae or Bignonia- ceae, respectively, as earlier assumed, but both come lose chaceae in molecular studies (Tank et al., 2006; Albach et al., 2009; Xia et al., 2009), which is supported by the lack of a staminode. The gynoecium is constantly bicarpellate (with extremely rare exceptions, such as in Duranta L., Verbenaceae, Bocquillon, 1863), but there is a tendency for reduction to in several amat (Acanthaceae, Schénenberger & Endress. 998; Phrymaceae, Eckardt, 1937; Verbenaceae, ME 1863; Plantaginaceae, Eckardt, 1937). Ovules are predominantly tenuinucellar and also often incompletely tenuinucellar and have an endothelium; y are anatropous or campylotropous. see micropylar and chalazal e endosperm haust characteristic. The water plant family irit ceae, positioned for some time in Cornales, now appears to be close to the base of Lamiales (Burleigh et al., 2009), which is supported by the presence of tenuinucellar ovules (Rauh & Jáger-Zürn, 1966) and endosperm haustoria (Jüger-Zürn, 1965), neither present in Cornales (see also Leins & Erbar, 1988). SOLANALES Flowers of Solanales are commonly polysymmetric, but several monosymmetric genera also occur in ct families of the order, Solanaceae and Con- ae, and even some cryptic asymmetry by different keja of anther exposition is present in both families (Endress, in prep.). There is a trend to form funnelform or rotate flowers with only very short free petal parts (many Convolvulaceae and Solanaceae). A few genera of Solanaceae have a similar kind of floral monosymmetry and reduction of the odd stamen as do Lamiales (Robyns, 1931; Huber, 1980; Hunziker, 2001; Ampornpan & Armstrong, 2002), or the odd stamen and one of the stamen pairs (several genera, Hunziker, 2001), whereas in the rare monosymmetric flowers in Convolvulaceae, all five stamens are well developed (Humbertia Lam., Ipomoea lobata (Cerv.) Thell.) (Deroin, 1992). GENTIANALES Gentianales comprise two major subclades: the large family Rubiaceae plus a cluster of families including Gentianaceae, Apocynaceae, Gelsemiaceae, and Loganiaceae, of which Apocynaceae are also large (Backlund et al., 2000). Apocynaceae are another group with complex flowers, but complex in a very different direction than Lamiales. They are polysym- metric, not monosymmetric. Floral organs are exceed- ingly synorganized with each other and form organ complexes (Schick, 1982; Fallen, 1986; Endress. 1994; Endress & Bruyns, 2000; M. E. Endress, 2001). In general, in Gentianales petals are often contorted, but there is also a trend from contorted to valvate aestivation. In both Apocynaceae and Rubiaceae, re are groups with the corolla postgenitally united Mes the basal congenitally united (sympetalous) zone and there sometimes fenestrate (Fallen, 1986; Robbrecht, 1988; Endress, 1994; Endress & Bruyns. 2000). Among asterids, pollen dispersal, not in monads but in higher aggregations (tetrads, pollinia), is mainly concentrated in Gentianales (some Apo- cynaceae, Gentianaceae, Rubiaceae). So-called pollen buds (intine protrusions at the apertures) are also an unusual faint of scattered occurrence in some Gentianales ( , Huang, 1986; Gentiana- ceae, Drexler & Hakki, 1979; Rub Rubiaceae, Weber & Volume 97, Number 4 2010 Endress Evolution in Eudicots and Their Major Subclades Igersheim, 1994). Carpels that are flat (not plicate) and postgenitally united in the style or in some cases even in the ovary occur in some Apocynaceae (Fallen, 1985), Gentianaceae (Kissling et al., 2009), and Rubiaceae (Puff et al., 1 200 They are tenuinucellar (not incompletely tenuinucel- lar).—in some groups even reduced tenuinucellar— but an endothelium is lacking and endosperm haustoria are absent or poorly developed. Some groups that were erroneously placed in Gentianales, but have been recognized as members of other orders by molecular studies, had been excluded from Gentianales earlier because of their ovules, such as Menyanthaceae (earlier in Gentianaceae), which are incompletely tenuinucellar and have an endothelium a vascularized, thick integument (Stolt, 1921; Inoue & Tobe, 1999). They are now in Asterales, and Polypremum L. (earlier in Loganiaceae), which has an endothelium and a haustorial endosperm (Moore, 1948), is now in Tetrachondraceae of Lamiales. BORAGINALES Polysymmetric, funnel-shaped or rotate flowers with only short free petal parts are common in different subgroups of the single family Boraginaceae (if the former Hydrophyllaceae, Cordiaceae, Ehretiaceae, and Lennoaceae are all lumped into Boraginaceae, APG, 2009). Boraginales show a trend to an increase a floral merism, either in the perianth and androe- cum, as in Codon L. (in basal position, Ferguson, 1999) and Cordia L., or in the gynoecium of the parasitic Lennoa Lex. and Pholisma Nutt. ex Hook. (Yatskievych & Mason, 1986). Ovules, although often incompletely tenuinucellar (Berg, 2009), tend to be y crassinucellar in more than one subclade (Cordia, Khaleel, 1982; Ehretia P. Browne, Johri & Vasil, 1956; Heliotropium L., Khaleel, 1978), and endosperm haustoria are only chalazal (Billings, 1901; Berg, 2009) or inconspicuous (Johri & Vasil, 1956; Khaleel, 1978). UNPLACED GROUPS IN LAMIIDS The unplaced families in lamiids— Vahliaceae, Icacinaceae, Metteniusaceae, and Oncothecaceae (APG, 2009)—are poorly known in floral structure and embryology. Vahlia Thunb. has bitegmic ovules with the micropyle formed by the inner integument (Raghavan & Srinivasan, 1942), and rudimentary bitegmy was also reported from Phytocrene Wall. (Icacinaceae) (Fagerlind, 1945a). Metteniusa H. Karst. (González £: Rudall, 2010) shares long, valvate petals _ 4nd a unilocular ovary with two pendant ovules with Icacinaceae. So far no conspicuous floral structural features have come up that would suggest specific relationships of these families with any of the larger subclades. CAMPANULIDS (EUASTERIDS II) As lamiids, campanulids also show a basal split with a small order (Aquifoliales) and an unresolved complex of three (partly) larger clades (core campa- nulids) The core campanulids comprise Escallo- niales, Asterales, and a clade of Bruniales, Apiales, and Dipsacales plus Paracryphiales (APG, 2009). In addition to the pattern of anthia with enlarged peripheral petals of the peripheral flowers mentioned before (Fig. 9I-L), campanulids are char- acterized by early sympetaly, in which the corolla appears to be initiated ing p i di on which secondarily the petals become apparent (Erbar & Leins, 1996). This is probably a consequence of another characteristic of the campanulids, the dom- inance of inferior ovaries (see also Endress, 1997a; Roels, 1998). In such flowers, the floral apex becomes more or less concave in early floral development, long before the time of gynoecium initiation, which may then give the impression of a ring primordium when the corolla is initiated. Ronse De Craene and Smets (2000) discuss the difference between early and late with regard to the position of st primordia: either on the rim or inside the rim of the early cavity. Petals are commonly valvate with incurved tips and somewhat postgenitally united in bud (in addition to the congenitally united base) and thus have a protective function, whereas the calyx is modified into a pappus or a group of bristles or thorns in various of Asterales (Asteraceae, Calyceraceae, Bru- k (Dipsiscacéne) In contrast to lamiids, contorted petal aestivation is largely absent. In Apiales and Asterales, sometimes have three or more vascular traces. Presence of a single ovule per carpel or gynoecium 18 common though not ubiquitous. Integumentary vascu- lar bundles are common in Asterales and Dipsacales (Billings, 1901; Kamelina, 1980). Elaborations related to buzz pollination are almost absent (present only in some Pittosporaceae). AQUIFOLIALES The flowers are commonly small. Sepals are short, and petals are protective organs in bud, most with a valvate aestivation and a conspic- uously inflexed tip. Carpels have two (or one) pendan O ic d 52 due of the l ovules p ar Gailis studied so far: Aquifoliaceae (Herr, Annals of the Missouri Botanical Garden 1959), Cardiopteridaceae (Fagerlind, 1945a), and 'emonuraceae (Pad: 1961); in Aquifolia- ceae, curiously, these ovules have a well-developed endothelium. ESCALLONIALES The two families Escalloniaceae and Polyosmaceae have flowers with a tube formed by the basal part of the petals, which tend to be valvate and more or less postgenitally connected. The gynoecium has a long, pas S ae -4 MT Stat s or less parietal placentae. Except for a species Escallonia (Kamelina, 1984), the ovules are unstudied. ASTERALES Asteraceae, the most species-rich family of Asterales (and of all angiosperms), have attained the ability to produce both polysymmetric and monosymmetric flowers in the same inflorescences, especially in the largest subfamily, Asteroideae (Kim et al, 2008; Funk et al., 2009). Although this versatility is also present here and there in other campanulids, it became a key innovation in Aster- aceae. A striking theme in Asterales is secondary pollen presentation from the upper part of the style based on pronounced protandry. The style, to which the open anthers are apy l(i belades by postgenital fusion of the anthers), carries the pollen upward by elongation at the male stage, and pollination occurs by transport from there to flowers at the female stage (Erbar & Leins, 1995; Leins & Erbar, 2006). This is ubiquitous in the largest family, Asteraceae, but is also present in Calyceraceae, Goodeniaceae, and Campanulaceae. In Stylidiaceae, androecium and gynoecium are congenitally fused so that pollen presentation on the upper part of the style is primary and not secondary. It is noteworthy that (Alseuosmiaceae, Argophylla- ceae, Menyanthaceae, Pentaphragmataceae, Phelli- naceae, Rousseaceae). Petals with two conspicuous wings, associated with induplicate-valvate aestiva- tion, are shared by three families of the Pacific clade of Lundberg (2009) (Alseuosmiaceae, Goodeniaceae, and Menyanthaceae). In at least three families of Asterales (Asteraceae, Harling, 1950; Campanula- ceae, Rosén, 1932: Goodeniaceae, Rosén, 1946), genera with more than two meiocytes in the nucellus occur. Tenuinucellar ovules are ominant in Asteraceae and also occur in Pentaphragmataceae and Stylidiaceae, whereas incompletely tenuinucellar ovules are present in the other families studied. An endothelium is most common. The subclade of four families including Asteraceae (Lundberg, 2009) is characterized by ovules with a thick (more than 10 cell layers) and vascularized integument, not only Goodeniaceae and Asteraceae as mentioned by Tobe and Morin (1996), but also Calyceraceae (Dahlgren, 1915) and Menyanthaceae (Stolt, 1921; Inoue & Tobe, 1999); this character is present in parallel in Campanulaceae (Campanuloideae, but not Lobelioi- deae) (Kamelina & Shinkina, 1998) from another subclade of Asterales. Endosperm haustoria are common, but were not found in some families. BRUNIALES The assemblage of Bruniaceae, Columelliaceae, and Desfontainiaceae as order Bruniales (APG, ; based on Winkworth et al., 2008) needs profound comparative research in its floral structures. Shared characters of all three families are slight floral monosymmetry and a superior ovary (both not in all Bruniaceae). However, the close mutual relationship of these families is not obvious from what is known on their flowers to date. APIALES Flowers are commonly small. The calyx is often reduced to a small rim. The corolla is protective in bud. The incurved tip of the valvate petals is conspicuous in some Araliaceae (Nuraliev et al., 2010) and in Apiaceae (lobulum inflexum) and attains a diversity of forms (Jahnke & Froebe, 1984). A conspicuous trend to form polystemonous androecia on a single whorl of stamens) and, to a lesser degree, multicarpellate gynoecia, is present in Araliaceae (Endress, 2002, 2006; Sokoloff et al., 2007a). Commonly, there is only one ovule per carpel or even per gynoecium (Karehed, 2003). The occurrence of crassinucellar ovules in Aralidiaceae (Philipson & Stone, 1980) and some Araliaceae (D. Singh, 1954) and of weakly erassinucellar ovules in Griseliniaceae (Alimova, 1987) and some other Araliaceae is noteworthy. Nevertheless, the most common type is incompletely tenuinucellar, usually with an endothelium (lacking in Pittosporaceae). Campylotropous ovules are common. Some of the small families are poorly known in their floral (Pennantiaceae, Torricelliaceae, Melano- structure phyllaceae). DIPSACALES Flowers are predominantly monosymmetric in Caprifoliaceae, which represent the majority of B in the order, but polysymmetric in Adoxaceae; Volume 97, Number 4 2010 Endress 569 Evolution in Eudicots and Their Major Subclades monosymmetry in Caprifoliaceae may be based on duplications in DipsCYC genes (Howarth & Donoghue, 2005). Subtle asymmetries are caused by fertility of only one of the more than two carpels or formation of only one lateral stamen (Hofmann & Góttmann, 1990; Endress, 1999; Donoghue et al., 2003). The corolla is protective in bud (Roels & Smets, 1996). Floral nectar is secreted by dense carpets of multicellular hairs on the corolla base in both Adoxaceae and Caprifoliaceae, a character not known from other asterids (Wagenitz & Laing, 1984). Carpels (or often entire gynoecia) are consistently uniovulate. Ovules are weakly crassinucellar in Viburnum (Adoxaceae) (Suneson, 1933) and otherwise incompletely tenui- nucellar. PARACRYPHIALES In Paracryphiaceae and Sphenostemonaceae, there is an unusually low level of synorganization of floral parts. Sepals are caducous and petals are lacking; there is a trend of increase in stamen number up to more than 10 (Gilg & Schlechter, 1923; Jérémie, 2008). In Paracryphiaceae, the number of carpels is also increased, up to 15 (Endress, 2002; Jérémie, 2008). In both families, the gynoecium is barrel- shaped with a superior ovary and sessile stigma. Another unusual feature in Paracryphiaceae is that the stamens tend to be arranged in two whorls, as seen from their alternation with the sepals (Dickison & Baas, 1977: fig. 10). This low synorganization appears to be the reason why the representatives of the two families were originally placed in basal angiosperms (Paracryphiaceae in Chloranthaceae, and Sphenoste- monaceae in Monimiaceae or Trimeniaceae). In contrast, Quintiniaceae have 4- or 5-merous flowers with sepals and petals, and a style and inferior ovary of three to five carpels (Engler, 1930). Paracryphia- cae and Quintiniaceae may have crassinuce ovules, and in Quintiniaceae ovules may even be bitegmic (Dickison & Baas, 1977; Mauritzon, 1933: fig. 43B). Superficial floral structural features do not Support a close relationship of Quintiniaceae with the other two families. Comparative studies on the floral Structure and development of the three families are badly needed. CONCLUSIONS AND OUTLOOK Among the f. plored in this study, there are some that have not been conventionally considered in the characterization of larger clades (from the top of the phylogenetic hierarchy downward). (1) Structural features of the sporophytic domain of ovules are Strongly underexplored and are a promising field of study at higher systematic levels. It appears that some eatures of ovule diversity are even more strongly correlated with larger clades than previously assumed (e.g., integument number and thickness; nucellar differentation at the apex, flanks, and base at early meiosis; degree and direction of ovule curvature at anthesis; presence or absence of endothelium). With = Ass 1 E sd A + fal, 1 } Z FE w KK (traditionally only the cellular level has been consid- ered, e.g., cellular vs. nuclear endosperm or cellular division patterns in the Albach et al., 2001). (2) Distinction between congenital and post- genital fusion in and between carpels has often been neglected but is needed for a better functional and systematic understanding of the gynoecium. With regard to intercarpellary fusions, a specific gynoecial architecture is well represented in malvids. In several subclades, carpels are initially free in development, at least in their upper part, but later fuse postgenitally, which allows formation of a functional compitum in a different way from the common case in syncarpous ko arx sal e E Malvaceae + + ORE i 11 1 pp) (Endress et al., 1983; Matthews & Endress, 2005b; Bachelier & Endress, 2008, 2009). The feature is also known in more isolated occurrence Sabiaceae (Endress & Igersheim, 1999), Iteaceae of Saxifragales (Hermsen et al., 2003), and some Gentianales (Endress et al., 1983). (3) The relation- ships between sepal and petal development in mea 1 1 "e T l1 1* J : n has been recognized in the present study that petals more often than earlier believed (e.g.. by Endress, 3 3 1 1 sd ce taka the sale and become protective organs, beginning at a relatively early stage and often attaining a valvate aestivation. Such early-developing protective petals also tend to have broad (not narrow) bases. Several clades show a trend toward this behavior (e.g.. Vitales, Gerrath & Posluszny, 1989; Celastrales, Matthews & Endress, 2005a; Crossosomatales. Matthews & End- ress, 2005b; Sapindales, Bachelier & Endress, 2009; Santalales, Wanntorp & Ronse De Craene, 2009; Cornales, Hufford, 2001; campanulids, e.g.. Gustafsson & Bremer, 1995). This adds a new facet to the old and persistent. problem of sepal and petal identity and needs to be explored in additional clades and in more tal detail. rd trends of specialization occur in many larger clades. When mapped on a cladogram of angiosperms, some features appear as potential key innovations in more than one clade ss € 1, feature 3) in rosids and asterids, tricolporate ae (feature 4) in rosids (minus Saxifragales) Annals of the Missouri Botanical Garden asterids, incompletely tenuinucellar ovules (feature 5) in the COM clade and asterids (minus Cornales), elaborate monosymmetric flowers (feature 9) in Fabales of the nitrogen-fixing clade, in core lamiids, and in core campanulids. It is of interest to explore to what extent these features having evolved many times across eudicots or across subclades of eudicots are based on the same genetic machinery and, vice versa, how different they may be (e.g., Cronk, 2002). I appears that genetic systems for specific features are present in certain plant groups even if these features are not manifested there. An example is the genetic etfmiot ji. * £1 1 y etry in larg e i which was present much * 1 wo. 1 ~ groups of core earlier in eudicot ge groups with monosymmetric flowers in which it was initially detected (Cubas et al., 2001; Howarth & Donoghue, 2006). Thus, those clades in which particular features appear for the first time, especially novel features that are regarded as key innovations, were explored here. The first occurrence of such atures is often much earlier than when they appear at the base of a large clade where they may be regarded as key innovations (Endress, 2001b) (e.g., on F ig. 1, 5-merous flowers, compitum, tricolporate pollen, haplostemony, tenui- nucellar ovules). However, not all innovations became key innovations. Such delay in the establishment of a feature as a key innovation was discussed in detail at the generic level in spur evolution of Halenia Borkh. in an ecological and phylogeographic context (Kader- th eit & von Hagen, 2003). From the present study, the oro these, in addition to ecological factors, morphological factors may also play a role in that the global floral architecture may not yet be predisposed for a key innovation, even though a critical feature was manifested (cf. Fig. 1). An interesting example of the and has not been a key innovation in this clade. In contrast. in Lamiales, monosymmetry is more elabo- rate and has been a key innovation leading to great diversification, hot sy se regions that are inactive as cold spots for evolution. For instance, Ranunculaceae are hot or dynamically variable in contrast, carpel number is a cold spot in lamiids and campanulids, where carpels are almost invariably two. A detailed demonstration and discussion of such hot and cold evolutionary spots move beyond the scope of this paper and should be the topic of a separate wi In cases of uncertainty in the position of clades, floral features may provide support. This is briefly discussed for several clades, such as (1) COM clade as closer to malvids than fabids, (2) Apodanthaceae, with a position in Malvales rather than Cucurbitales, (3) Balanophoraceae, as in Santalales, (4) Hydrostachya- ceae, associated with Lamiales rather than Cornales, (5) Rehmannia, evinced as closer to Orobanchaceae rather than Gesneriaceae or Scrophulariaceae, and (6) Paulownia, as affined closer to Orobanchaceae rather than Bignoniaceae or Scrophulariaceae. In summary, it should be emphasized again that newly recognized clades need to be comparatively studied in structural features. This is an ongoing necessity. Likewise, unconventional floral features need to be explored, i.e., features that have not been previously considered by morphologists, embryolo- gists, and systematists in their conventional catalog of f for comparative studies. 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Mitoc pchondrial matk tinnahina t in ee BMC bul e T: 217. ASSEMBLING THE TREE OF THE = Thomas J. Givnish,? Mercedes Ames,? Joel R. MONOCOTYLEDONS: PLASTOME McNeal,* Michael R. McKain,* P. Roxanne Steele,* Claude W. dePamphilis,? Sean W. SEQUENCE PHYLOGENY AND Graham,* J. Chris Pires,* Dennis W. Stevenson,’ EVOLUTION OF POALES' Wendy B. Zomlefer,? Barbara G. Briggs,* Melvin R. Duvall? Michael J. Moore,'? J. Michael Heaney," Douglas E. Soltis," Pamela S. Soltis,” Kevin Thiele,'* and James H. Leebens-Macl? ABSTRACT The order jo s E ends lf, (7% od all osperms and 3 of monocots) and includes taxa of enemies economic and En e Molecular and morphological sa wer the best two decades, homero we present the results s an initial project d the Monocot AToL (A ngiosperm Tree of Life) team on phylogeny and evolution in Poales, using sequence data for 81 plastid genes (exceeding 101 ali gned kb) from 83 83 species of angiosperms. We recovered highly eiii y (MP), with 98.2% mean ML bootstrap support across monocots. For the first time, ML resolves ties among Poales and other commelinid orders with moderate to strong ae Anel provide strong support for or Bromeliaceae being sister to the rest of Poales; Typhaceae, Rapateaceae, and cy (sedges, rushes Graminids ses and their allies) and dde (Restionaceae and its alli es) are well su pported a as aer. taxa. MP identifies a id ade (Eriocaulaceae, Mayacaceae ae, Xyridaceae) sister to cyperids, but ML (nith much stronger support) places them as a grade with re respect to restiids + graminids. The conflict i in resolution between these analyses likely reflects long-hranch attraction and highly elevated Poal All oth pported by both MP an d ML — Character-stat li h ] Poales lived i fire-prone, ai an seasonally damp/wet, and possi d mutrient-podr sites, ‘and were animal pollinated. Fiv subsequent shifts to wind pollination—in Typhaceae, cyperids, restiids, Ecdeiocoleaceae, and the vast PACCMAD-BEP cur of grasses—are significantly correlated with shifts ks Pis gates oo tar-free flowers. Prime ecological movers Lr the repeated evol —Ó of wind pollinati Poales appear to "ollude open habitats combined with the high local dominance of onspecific taxa, with the kus resulting from large-scale disturbances, combined with tall plant stature, vigorous vegetative —— M ' This Nati ] Sci F. Jati E» nhED noono7rzo research was — by (NS 76 B-0829849, D ses of X f the M AToL Tam, and by ~ Hertel en Fund of the ond comin Madison w to ER G. - Janes “esa Jona. Vamosi, Spencer Barrett, and Kathleen Kay kindly ah his data set on the pi and George Fane graciously let us dcin. Meo a of dioecy across monocots. Lymn € Clark kindly rE information on bamboo seeds and Birch ided Bd helped provide permits and T os beate i in Tasmania; Joanne rch provi assistance and camaraderie while collecting at t Cradle M lame and M t Chan-a-Sue argaret ark n: s Cr W. id l Kaieteur Falls National P. - ; E wou ` M nay thank Frank a of the Australian cd Herbarium and Mark Clements of the Centre for Bl EE Andrew Meade, Mark Pagel, Ma Mark. Chase, Ken a Marie eS € Havey generously prov vided access to © important lab equipment. Chang Liu helped prepare DNA samples $ Elliott worked her digital magie with the de ess to the Y ASRA assembler. Kandis s ne Wardrop ontribu eantha VU MEA TM cipe Rr rsa el a maaa symposium ation: to P. Victoria Hollowell de be many contributions — per Victoria Hollowell for providing several helpful comments, and to * Department of Botany, University of Wiscons: sconsin, Madi * Department of Plant Biology, University of e Wisconsin 53706, U. x ` ue edu. Boa Biological Sciences, Univ ersity of Mi thens, Pus cen . Pennsy vania i š Uniy P. * Botanical Caen and Centre for Plant Research. : k niversity e Pennsylvania 16802, U "New York Botanical Garden, Bronx, New York 10458, US A. n Columbia, Vancouver BC. "Canada V6T 124. , Australia. Illinois U “Department of Biology, Oberlin College, Oberlin, LEE DeKalb, Illinois 60115, U.S.A. " Department of Botany, University of Fl orida, Gainesville, | Fl de ns m History, University of Faida. Cai vus ila 3201 ui: U.S.A estern Australian um, Western ustralia ^ mis Ç 7 o qe na iue A | Volume 97, Number 4 2010 š Givnish et al. Plastome Sequence Phylogeny of Poales spread, and positive ecological feedback. Reproductive assurance in the absence of reli e animal visitation probably favored wi ination i | ms avored wind pollination in annuals and short-statured perennials of Centrolepidaceae in ephemerally wet depressions and windswept alpine sites. Key words: monocots, plastid, plastome, restiids, x Commelinids, correlated evolution, cyperids, graminids, long-branch attraction, molecular systematics, yrids. / Monocots—with ca. 65,000 species in 82 families and 12 orders (Cameron et al., 2003; Givnish et al., 2006; Saarela et al., 2007; Angiosperm Phylogeny Group, 2009), and including such groups as the grasses, sedges, bromeliads, palms, gingers, orchids, irises, onions, asparagus, lilies, yams, pondweeds, aroids, and se one of the most diverse, morphologically varied, ecologically successful, and economically important clades of angiosperms. Since monocotyledons arose in the early Cretaceous (Herendeen & Crane, 1995; Bremer, 2000; Friis et al., 2004; Ramirez et al., 2007; Conran et al., 2009), they have radiated into almost every habitat on earth. Today, they dominate many terrestrial and aquatic ecosystems, display kaleidoscopic variation in vegetative and floral form, provide the basis for most . uman diet, support a huge horticultural _ industry, include large numbers of endangered taxa, and comprise nearly one fourth of all species and families of flowering plants. Understanding their origin, phylogeny, and patterns of morphological evolution, geographic diversification, and ecological radiation is thus a grand challenge and opportunity for evolutionary biologists. Over the past 18 years, molecular systematics has revolutionized our understanding of monocot relation- ships (Chase et al., 1993, 1995a, b, 2000, 2006; Duvall et al., 1993a, b; Les et al., 1997; Givnish et al., 1999, 2005; Bremer, 2000, 2002; Kress et al., 2001; Hahn, 2002; Cameron et al., 2003; Michelangeli et al, 2003; Davis et al., 2004; Graham et al., 2006; Pires et al., 2006; Saarela et al., 2008). Such studies have led to a dramatic reclassification of the monocots (Angiosperm Phylogeny Group, 1998, 2003 2009 with an ever-increasing understanding of relationships within and among the 12 orders currently recognized. Triumphs of monocot molecular systematics have included, first and foremost, the recognition of the commelinid clade (Chase et al., 1993, 1995a) composed of the orders Poales (the grasses, sedges, bromeliads, and their allies), Commelinales (the dayflowers, water hyacinths, and relatives), Zingiber- ales (the gingers, bananas, and related tropical monocots), Arecales (the palms), and the Australian Dasypogonal i — ? logeny Group, 2009, here recognized as 5 ae following Givnish et al., 1999). This finding was E buttressed by the demonstration that all five orders share UV-fluorescent ferulic acid bound to cell walls (Harris & Hartley, 1980; Dahlgren et al., 1985; Rudall & Caddick, 1994; Harris & Tretheway, 2009) despite their otherwise great divergence in form and despite based on molecular and morphological data (Chase, 2004; Graham et al., 2006). Other key advances have included the validation, to a large degree, of many of the orders inferred cladistically from morphology by Dahlgren et al. (1985); the identification of relation- ships among those orders; the placement of Acorus L. as sister to all other monocots (Duvall et al., 1993a); and the discovery that several genera, originally placed in Melanthiales based on morphology by Dahlgren et al. (1985) and Tamura (1998), actually belong to three other orders—including Tofieldia Huds. in Alismatales, Narthecium Huds. in Dioscore- ales, and Japonolirion Nakai in Petrosaviales (Chase et al., 1995a, b, 2000, 2006; Zomlefer, 1999; Tamura et al., 2004). Perhaps most remarkably, Saarela et al. (2007) recently showed that highly reduced members of the aquatic family Hydatellaceae were not—as had long been believed (Hamann, 1976; Dahlgren et al., 1985; Angiosperm Phylogeny Group, 1998, 2003; Davis et al., 2004)—members of order Poales, and not even monocots, but were instead sister to waterlilies and other Nymphaeales, one of the earliest divergent clades of angi (see Bosch et al., 2008, an Rudall et al., 2009, for corroborating morphological evidence). Chase et al. (2006) provided the most powerful study of relationships across monocots to date, in terms of its combination of extensive taxon sampling (125 species stratified across 77 of 82 families) and sequence data per taxon (four plastid genes, two mitochondrial genes, one nuclear ribosomal gene). Based on their maximum parsimony (MP) analysis, Acorus is sister to all other monocots, followed by the successive divergence of Alismatales, Petrosaviales, Dioscoreales-Pandanales, Liliales, Asparagales, and the commelinids (Fig. 1). Based on Chase et al. (2006). all orders appear to be strongly supported, and all relationships among orders are resolved and— outside the commelinids—moderately to strongly supported. Yet, the MP strict consensus tree resulting from that study left many relationships within orders weakly supported, as well as a few of those among rders. Areas of substantial uncertainty include Annals of the Missouri Botanical Garden 586 Chase et al. 2006:4 cpDNA genes, 2 mtDNA genes, 1 nrDNA gene ' commelinids | S t " Liliales Pandanales Bootstrap support: Dioscoreales *== 90-100% Petrosaviales = 75-89% i vie ten Alismatales Acorales Figure E Branching topology and support at the ordinal ja > two mitochondrial genes, and one “nuclear gene (4777 informative sites, or 34.9 ncmo sites/taxon). Adapted from Chase et al. (2006). cos ne man etnia piihin Poales, and positions of Asparagalco and Liliales relative to the commelinids; wi affinities of several families in Asparagales, Zingiberales, Dioscoreales, Pandanales, and Alisma- tales. In addition, relationships among commelinid orders found by Chase et al. (2006) weakly conflict with those identified by Graham et al. (2006) based on 16 kb of sequences for coding and noncoding plastid rogress (see symposia volumes edited by Rudall et la. 1995; Win & Morrison, 2000; Columbus et al., 2006, 7; Seberg et N 2010). Yet much remains to be To khu. these uncertainities, develop a better understanding of broadscale ips in mono- cots, and provide a strong basis for comparative iles of a — ecological, and geographic differentiation in this important group, the National Science Foundation—funded Monocot AToL (Assembling the Tree of Life) project ( irion of monocot evolution, building on the strong foundation of previous research by the international botanical community. Our aims are to: (1) develop a fully resolved, strongly supported, highly inclusive broadscale phylogeny for the monocots, sequencing transcriptomes of young leaf tissue for several dozen species, and whole-plastid genomes and targeted mitochondrial and nuclear genes for a few hun q specia ente all t famili d ) score more than 200 morphological characters k the same extant species and 75 fossil taxa; (3) reassess the stratigra- phy and classification of several fossil monocots and develop a new timeline for monocot evolution; (4) >) is conducting a 5-year and fossil plants; (5) use the resulting phylogeny to conduct analyses of morphological, developmental, ecological, and biogeographic evolution using hun- eds of taxa stratified across the monocots (e.g., see - Davies et al., 2004; Givnish et al., 2005; Dunn et al., 2007); and ultimately (6) help train and inspire a new generation of monocot systematists in phylogenetics, genomics, and evolutionary biology. As a key part of this effort, we will sequence and analyze hundreds of complete plastid genome sequences. Almost all studies to ies using DNA to infer relationships among m s and other angiosperms have been mcm i RE on sequences of only one or à few genes or gene spacers. Our approach will be new data with which to assess evolutionary relation- "e dn approech. has proved fruitful i in lendat bai ie (Lecbens-Mack et al., “2005; Coi et E 2006; Jansen et al., 2007: 7; Moore et al., 2007; Wang et al., 2009). However, high data density per taxon must be complemented with a reasonably dense stratifica- tion of taxon sampling across the range of organisms being investigated in order to minimize errors in phylogenetic inference due to aa eneh attraction (e.g., see Goremykin et al., 2003, vs. Soltis & Soltis, 2004; Leebens-Mack et al., 2005). In sequencing plastomes and targeted mitochondri- al and nuclear genes, we are collaborating closely with members of the Angiosperm AToL team () to sequence shoot transcriptomes for several dozen species. We believe that the unparal- leled amount of genetic information from all three plant genomes obtained in our AToL project should provide the most powerful analysis of relationships for any major plant group studied to date. In this paper, we present a demonstration of the utility of a plastome-based phylogenomic approach, focusing on relationships among families of Poales and their immediate relatives among the commelinids. Poales is the second largest order of monocots, and economically surely the most important, as a conse- quence of its including the cereal and pasture grasses, which contribute so much to the human diet, directly or indirectly; the bamboos, a key source of building materials: and the restioids, sedges, rushes, cattails, and bur reeds, which form such key components of wetland ecosystems locally and worldwide. Poales and the commelinids include many of the nodes in the monocot tree of life that have proven most difficult to resolve using traditional phylogenetic techniques. Here we present a new, plastome-based phylogeny for the monocots and discuss its implications for relationships among families of Poales and its immediate commelinid relatives. We then use this phylogeny to analyze broadscale evolutionary patterns within Poales, including habitat diversification and, especially, the pattern and potential causes of multiple origins of wind pollination, an otherwise iy uncommon mechanism in the conclude with a brief discussion of some of the limitations of plastome-based phylogenomics for understanding monocot phylogeny and evolution. monocots. We METHODS TAXON AND GENE SAMPLING The 83 taxa included in our study represent most major clades of angiosperms sensu Angiosperm Phylogeny Group (2009) E g q were genera 83 taxa included in the study (Appendix 1). These _ Rew data greatly increase the number of monocot _ Sequences included in plastid phylogenomic analyses. Sixty-four species acted as placeholders for 11 monocot orders and 32 of 82 monocot families. Taxon sampling is concentrated on Poales and, to a lesser extent, its putative relatives among the commelinids and Aspar- agales. Commelinids sequenced included members of 15 of 16 families of order Poales (Anarthriaceae not sampled); one of five families of Commelinales; two of Arecales and Dasypogonales (Dasypogonaceae sensu Angiosperm Phylogeny Group, 2009). Nonmonocot angiosperms inc representatives of an additional 18 orders of flowering plants (Appendix 1). We used Amborella Baill., the consensus sister taxon to all other angiosperms (Jansen et al., 2007; Moore et al., 2007) as the outgroup. PLASTOME SEQUENCING We used next-g ti I ing to generate 44 plastid genomes sequences (Appendix 1) using one of two strategies. Following methods described by Jansen et al. (2005), plastids of Lilium L., Hosta Tratt., Tradescantia L., Brocchinia Schult. f., Neoregelia L. B. Sm., Pitcairnia L'Hér., and Puya Molina were isolated on a sucrose gradient and used as templates for rolling circle DNA amplification. Plastome- enriched amplicons were sequenced on a Roche GS- FLX sequencer (Roche, Branford, Connecticut, U.S.A.) using 454 pyrosequencing technology (Moore et al, 2007) The remaining 37 draft plastome sequences were assembled from whole-genome shot- gun sequences generated on an Illumina GS sequenc- er (Illumina, Inc., San Diego, California, U.S.A.). The proportion of plastid DNA in isolated DNAs was estimated through quantitative real-time PCR ampli- fication of a 150-bp portion of the rbcL gene. Samples estimated to have at least 5% plastid DNA were prepared for whole-genom hotg juencing on Illumina sequencing platform, following the manufac- turer’s protocol. Bar codes were ligated to templates, and at least one million 75-bp reads were generated for each taxon. De novo assemblies of sequences generated on the 454 platform were constructed using the manufacturers Newbler assembler («http://www 454.com>) and the MIRA assembler (; Chevreux et al., 2004). Resulting assemblies were inspected using Consed (Gordon et al., 1998) and Sequencher (). Genes were anno- tated and gene sequences were extracted from assemblies using the DOGMA webserver (, Wyman et al., 2004, and see below). Sequences generated using the Illumina short-read platform were subjected to reference-based assembly using the YASRA assembler (Ratan, 2009; Annals of the Missouri Botanical Garden download available with documentation at ) to layer short reads on a reference genome while allowing substantial e divergence (< 85% sequence identity). For each taxon, the most closely related plastome genome sequence available in GenBank was initially used as the reference genome. In addition, our draft E ly Ex £. for assembly of related genomes. For example, the Cyperus alternifolius L. draft plastome was used as a reference for Juncus effusus L. and Thurnia sphaer- ocephala Hook. f. plastome assembly and vice versa. Final assemblies for each taxon were compiled in Sequencher. As described above, genes were anno- tated and extracted from the resulting contigs using DOGMA. DOGMA identifies genes through BLASTX searches against a database of amino acid sequences extracted from exemplar plastid genomes. As a consequence, gaps in the assemblies, rare sequencing errors, and assembly errors that introduce frame shifts or stop codons may result in annotation of gene fragments rather than full-length genes. Only full- or near-full-length gene annotations were included in alignments and phylogenetic analyses. Therefore, individual taxa may be missing genes due to low sequencing coverage, assembly errors, or evolutionary loss (e.g., the loss of the ycf2 gene in the inverted repeat [IR] region of the plastome on the branch leading to Poaceae/Ecdeiocoleaceae/Joinvilleaceae). The only taxa with substantial numbers of missi Joinvillea plicata (Hook. f.) Newell & B. C. Stone under ordinary direct sequencing. All gene sequences included in alignments and phylogenetic analyses have been deposited into GenBank. All analyses were based on the exons of 77 protein-coding plastid genes SEQUENCE ALIGNMENT Following Jansen et al. (2007), 81 plastome- encoded gene sequences were aligned individually and alignments concatenated into a single nexus file for phylogenetic analyses; the file is posted at the Monocot AToL project website (see ). Perl scripts were written to sort gene sequences extracted from DOGMA annotations for each taxon into multitaxon fasta files for each gene, to align gene seq ing MUSCLE (Edgar, 2004), and to concatenate alignments in a Nexus file. Missing genes were filled with Ns in the concatenated alignment. PHYLOGENETIC ANALYSES We inferred relationships among taxa from the nucleotide data using MP and maximum likelihood (ML). MP analyses were run using PAUP* 4.0d102 (Swofford, 2002). Individual nucleotides were consid- ered to be multistate, unordered characters of equal weight; unknown bases were treated as uncertainties. Gapped cells were treated as missing data and we did not attempt to score indels. To evaluate the possibility of multiple islands of equally most parsimonious trees (Maddison, 1991), we ran heuristic searches seeded with 100 random-addition sequences, employing tree bisection-recon ton (TRR) ppi 18 L:] Eros g up to 100 trees per iteration. Bootstrap analysis (Felsenstein, 1985) was used to assess the relative support for each node in the single shortest tree found, using 200 random resamplings of the data and retaining up to 100 trees per resampling. Consistency indices, including autapomorphies (CI) and excluding them (CI), were calculated to measure the relative extent of homoplasy in the data (Givnish & Sytsma, 1997). ML analyses were performed on concatenated alignments using RAxML version 7.0.4 (Stamatakis, 2004). A single substitution process was modeled as general time reversible (GTR) plus gamma for the entire concatenated ali nt (i.e., data were not partitioned). Among-site variation in substitution rates was modeled using the discrete approximation of the gamma distribution (Yang, 1994) with 25 rate classes. The ML bootstrap analysis included 250 pseudo- replicates drawn from the concatenated alignment. ANCESTRAL HABITAT RECONSTRUCTION To trace patterns of habitat evolution within the order Poales, we overlaid various environmental characteristics on the commelinid portion of the ML cladogram, simplified to the family level, using parsimony as implemented in MacClade 4.0 (Maddi- son & Maddison, 1992) to infer ancestral states, resolving all of the most parsimonious states at each node. Given their distinctive ecologies, we separated subfamily Anomochlooideae from the other Poaceae sampled (a subset of the bistigmatic clade subfamily Puelioideae + the PACCMAD-BEP clade of grasses; the later consists of Panicoideae, Arundinoideae, Chloridoideae, Centothecoideae, Mi- deae, Aristidoideae, Danthonioideae-Bambu- Volume 97, Number 4 2010 Givnish et al. Plastome Sequence Phylogeny of Poales oideae (unsampled in our phylogenetic study) between nomochlooideae and Puelioideae, given that recent molecular studies place them there with high support, and given the distinctive ecology of pharoids and puelioids versus most members of the huge PACC- MAD-BEP clade, which includes 99% of all grass genera and species (Soderstrom & Calderón, 1971; Clark et al., 1995, 2000; Grass Phylogeny Working Group I, 2001; Hodkinson et al., 2007a, b; Bouche- nak-Khelladi et al., 2008). Characteristics overlaid include: (a) light availability (sunny vs. shady); (b) moisture supply (soil wet or inundated vs. well drained or dry); (c) soil fertility (highly infertile [e.g., sand or sandstone] vs. fertile); and (d) fire prevalence (high vs. low/absent). were drawn from summaries in Dahlgren et al. (1985), Givnish et al. (1999, 2000, 2004, 2007), Linder and Rudall (2005), and Sokoloff et al. (2009). We used the ML phylogeny, including Poales and families of the other commelinids studied as ingroups and Apostasia Blume of Orchidaceae as the outgroup, because it resolves a few crucial nodes differently and with far higher support than the MP tree, and because ML generally is less susceptible to problems caused by extensive change in evolutionary rates over time (i.e., heterotachy) and long-branch attrac- tion (e.g., Huelsenbeck & Hillis, 1993; Huelsenbeck, 1995; Chang, 1996; Swofford et al., 2001; Gadagkar & Kumar, 2005; Leebens-Mack et al., 2005; Jansen et al., 2007; Moore et al., 2007; Whitfield & Lockhart, 2007; Wang et al., 2009). Where necessary in large, ecologically diverse groups represented by single taxa, we overlaid the ancestral conditions previously inferred for such families based on detailed infrafamilial molecular studies (e.g., Givnish et al., 2000, 2004, 2007) or inferred what those ancestral conditions would have been, given the habitats of the first several earliest-divergent lineag- es within those families (Appendix 2). ORIGINS OF WIND POLLINATION AND PATTERNS OF CORRELATED EVOLUTION We also overlaid wind versus animal pollination on the simplified Poales tree using MacClade, following earlier analyses by Givnish et al. (1999) and Linder and Rudall (2005). We drew data from those papers and from Newell (1969), Soderstrom and Calderon (1971, 1979), Henderson (1986), Stiitzel (1986, 1990). Listabarth (1992), Soreng and Davis (1998), Rosa and Scatena (2003, 2007), Blüthgen et al. (2004a, b). Blüthgen and Fiedler (2004), Ramos et al. (2005). Moura et al. (2008), Oriani et al. (2009). and Sokoloff et al. (2009) (see Appendix 2, Table A2). Previous authors have argued that wind pollination should be positively associated with visually inconspicuous, : Im. Ree f Š s J 1 growth in open or seasonally open, windy environ- ments; and a taxon's local abundance (see Faegri & van der Pijl, 1979; Regal, 1982; Cox, 1991; Linder, 1998; Weller et al., 1998; Givnish et al., 1999; Cully et al., 2002; Friedman & Barrett, 2008). To evaluate how these ideas apply to Poales, we conducted formal tests of correlated evolution of pollination mechanism i . animal) with plant habitat, nectaries ic vs. unisexual flowers), sexual system (cosexuality vs. dioecy), ovule number (one vs. many), floral size (small vs. large petals or other visual displays), and floral showiness (nonshowy vs. showy colors) using the for significant patterns of correlated evolution of two binary traits by comparing the fit (In likelihood) to 1J 4b. E iet ant: A dent evolution on the phylogeny provided using continuous- time Markov models (Pagel & Meade, 2006). For each trait, we conducted two sets of nested ML analyses, either setting the branch-length parameter K equal to 1 or allowing it to assume its optimal value under ML analysis. Values of k < 1 result in a scaling that reduces the length of longer branches more than shorter branches. Our approach directly parallels that used by Friedman and Barrett (2008) to test for correlated angiosperms. ion of our ML tree for topology and branch lengths. Character states for all taxa in the ML tree (see previously cited and from two data sets kindly provided by Jannice Friedman, Jana Vamosi, and Spencer Barrett, and by George Weiblen. We scored the highly unusual (if not, indeed, unique) case of Chamaedorea Willd. in which thrips are involved in releasing clouds of pollen that move from staminate plants to pistillate plants via the wind Li pollinated, given the role that animals play in this case of animal-induced wind pollination. RESULTS PHYLOGENY MP yielded a single, fully resolved tree of length 152,366 steps (Fig. 2). Overall, there were 25.107 parsimony-informative characters, of which 22.156 were informative within the monocots. Across all taxa, 12,634 characters were variable but uninformative and 71,834 were constant. Monocots were monophyletic and 590 Annals of the Missouri Botanical Garden MP plastome phylogeny graminids q Length = 152,366 steps CI = 0.384, CY 0.318 83 taxa (68 Poaceae 109,134 aligned bases 25,107 informative characters Ecdeiocoleaceae Joinvilleaceae es Flagellariaceae restiids ` — Restionaceae me 7 Mayacaceae xyrids x Eriocaulaceae cyperids , | k ne m Rapateaceae | Typhaceae Bromeliaceae d Arecaceae 1 Arecales | Commelinaceae J Commelinales 1 u A Dasypogonaceae |] Dasypogonales 56 Asparagaceae 5 a da iid Asparagales — Xanthorrhoeaceae - Iridaceae 10 < Asteliaceae 100 100 > 4 Orchidaceae il a d Dioscoreaceae - Dioscoreales | Lemna = Liliaceae Z Liliales xo Acorus americanus = Araceae - Alismatales Panax 4 34 7 Helianthus 5 t Medicago Eudicots 1 x Vitis Populus 100 Buxus - a o Drimys : - Magnoliales Miciurn , `w od Amborella net - Austrobaileyales —— 1000 changes - Amborellales A pl 2 he pe for the Mni" e tree - resulting from i analysis of the plastome data, rooted using Amborella Baill. shown above e corresponding Tame h. Monocots are highli anch. Bootstrap support for each node is ted with graminids, with colored boxes. Full scientific names and s ca 2a cel k den Ac i Tome ame `. enr e iet CHR commelinids as a whole, and each of their five orders, (Lemna D Liliales (Lil Di nies x = had 100% bootstrap support. Poales was resolved as (Dioscorea Pandan Plin and fi Sister to Arecales, and Dasypogonales as sister to agales "ign: ue eed Tingheisies, but both relationships had ES gressively Wei more recent nodes. Bootstrap branching AS support am the Within Poales, Bromeliaceae were sister to all other of Lili e x ^ ek es-Pandanales, "e taxa, with 100% bootstrap support, followed by the that for the enis bran ‘As C as was divergence of Typhaceae and Rapateaceae at the two i succeeding nodes, with 97% and 100% support, Volume 97, Number 4 2010 Givnish et al. 591 Plastome Sequence Phylogeny of Poales respectively (Fig. 2). The MP tree recovered the xyrids (Eriocaulaceae, Mayacaceae, Xyridaceae) as monophyletic with 68% bootstrap support and placed them sister to the cyperids (Cyperaceae, Juncaceae, Thurniaceae) with 78% bootstrap support. Within the xyrids, Mayaca Aubl. was placed sister to Syngo- nanthus Ruhland of Eriocaulaceae with 9946 boot- strap support. Branches among the cyperids all had 100% bootstrap support. The restiids (Restionaceae Centrolepidaceae, and Anathriaceae, with the last small family unsampled here) were monophyletic, with 100% bootstrap support, and were sister (with 94% bootstrap support) to the graminid fado fomes aña their allies. Within the graminids, Flagellaria L. was sister to all other taxa with 100% support; Joinvillea Gaudich. ex Brongn. & Gris was sister to the remaining taxa, also with 100% support. Finally, Ecdeiocoleaceae 1 d Lali LOMO rti J sictar to the grasses (94% support). Across monocots, inferred branch lengths were especially short in Acoraceae, Arecaceae, Bromelia- ceae, and Typhaceae, and especially long in the graminids, restiids, xyrids, and cyperids (Fig. 2). Seven of these eight clades are part of the commelinids. Relative to the commelinid crown-group root node, branch lengths averaged 1734 + 170 (mean + SD) steps for palms, 2112 + 103 for bromeliads, and 2701 + 67 for cattails and bur-reeds, compared with 7027 + 1062 for xyrids, 7821 + 1102 for cyperids, 8644 + 1210 for restiids, and 9152 + 1416 for graminids. Rates of plastid sequence evolution thus vary by as much as 5.2-fold within the commelinids, based on MP analysis. ML produced a single. fully resolved, well- supported phylogeny (Fig. 3). This tree is striki similar in most regards to the MP tree, with four key exceptions. First, Lilium (Liliales) was resolved as i Asparagales—commelinid clade; this tet agales had 100% bootstrap support as being mono- phyletic and 99% support as being sister to the commelinids in the ML tree, versus 56% tor both conditions in the MP tree. Support for the topology of the ML tree was generally higher than that for the MP tree, with 63 of 67 nodes within the monocots having > 94% bootstrap support, and all 18 nodes outside the monocots having 100% support (Fig. 3). Third, ML provided a different and much more strongly supported resolution of the commelinid orders, with Poales being sister to Commelinales—Zingiberales with 93% bootstrap support, and Arecales being sister to Dasypogonales with 86% bootstrap support. Finally, in the ML tree, the xyrids formed a grade, not a clade, and were associated with the graminid-restiid elade, not the cyperids. Abolboda Bonpl. of Xyrida- ceae was sister to the restiid-graminid clade with Syngonanthus of Eriocaulac boda plus the restiid-graminid clade (Fig. 3). ANCESTRAL HABITAT RECONSTRUCTION We infer that the ancestral Poales occupied habitats that were sunny, wet, possibly nutrient poor, and fireswept (Figs. 4, 5), much like the conditions occupied by Brocchinia prismatica L. B. Sm., B. melanacra L. B. ceae today (Givnish et al., 1997, 2007). Low-nutrient conditions characterize the ancestral Poales only under ACCTRAN. However, infertil il likely than fertile soils to favor fire (Givnish, 1980), the inferred condition for ancestral Poalean habitats (Fig. 5B). Both ACCTRAN and DELTAN reconstruet infertile soils as the ancestral state for the clade including Rapateaceae and its sister (Fig. 5A). Open habitats typify most of the early divergent families—from bromeliads to the restiids—although bromeliads and rapateads include a number of reinvasions of shaded sites (Givnish et al., 2000, 2004, 2007), as do sedges (e.g., in Becquerelia Brongn. and Carex L.) and rushes (e.g., in Luzula DC.), which can be inferred from the phylogenies provided by Drábková and Vlček (2009) and Muasya et al. (2009). Shady habitats were reinvaded by members of a grade rumning from Flagellaria and Joinvillea through the anomochlooid and pharoid grasses, with reinvasions of sunny habitats in Ecdeiocoleaceae and the PACCMAD- BEP grasses (Fig. 4A). Damp or wet soils appear to be the ancestral condition in Poales from bromeliads (e.g., Brocchinia, Lindmania Mez) through at least Xyridaceae (Abolboda), with a transition to well-drained rainforest soils for Flagellaria, Joinvillea, Anomochlooideae, and Pharoideae (Fig. 4B). Several Centrolepidaceae and Restionaceae grow in permanently or seasonally inun- dated soils, but others occupy well-drained sites. If we assume that the ancestral habitat of Poales had highly infertile soils (see above), then such soils would have characterized all families and ancestors from Bromeliaceae through the restiids, with the exception of Typhaceae, Cyperaceae, and Juncaceae on richer soils, although some members of the latter two families now occupy highly infertile substrates as well. The terminal clade of Poales (Flagellariaceae through Poaceae) typically occupies more fertile substrates, with the exception of Ecdeiocoleaceae. Finally, fireswept habitats characterized families from Bromeliaceae through Xyridaceae and possibly the restiids, with such disturbance being lost in the aquatic Thurnia Hook. f. (but perhaps not in Prionium E. Mey.), the aquatic Mayaca, the aquatic and alpine ical Garden issouri Annals of the LANCET IT TON IT TE ET ITO LLIN `səxoq pə1o|oə qu^ perjsipusn| əre spturues:d pue “spirinsə: “spuáx “spriodA) "uoueaq Surpuodsoir əy) əaoqe umoys st siooouour oy} uyum əpou yəLə aoj uoddns deujsjoog 'sapou q[e 20; de:jsjooq 25001 W^ *[ o1n314 ur umoys jeu oj [eorpuopr *1949«og *sr uoniod jeu jo uornosaz au ‘UMOYs JOU st 9a.) oY) Jo uoniod 1020uoumuou ƏL 291) TW us our 10j urexdop&ug “€ air snup2yawp snioy [ 91s/suonmpnsqns so'o 9t8'SpCE98 - - 1 ul J*u15 KueBojAud əuioase|d 4W r nn ee ek ire EIEN ORO E avin ee rn ANY TY Volume 97, Number 4 Givnish et al. 2010 Plastome Sequence Phylogeny of Poales A. Light ve gee Poaceae B. Moisture supply Poaceae 1 n na f- PACCMAD-BEP peee n |- PACCMAD-BEP m |- Puelioideae n - Puelioideae W |- Pharoideae u F Pharoideae m L Anomochlooideae n LAnomochlooideae — E pEcdeiocoleaceae o Ecdeiocoleaceae m Joinvilleaceae u Joinvilleaceae m Flagellariaceae o Flagellariaceae D Restionaceae SResionaceae “| n Centrolepidaceae n Centrolepidaceae T o Xyridaceae m Xyridaceae i o Mayacaceae g Mayacaceae xyrids o Eriocaulaceae 8 Eriocaulaceae rs Cyperaceae 8 Cyperaceae ; aek m Juncaceae cyperids AAEE m Thurniaceae d D Rapateaceae g Rapateaceae D Typhaceae g Typhaceae T Bromeliaceae g Bromeliaceae r Commelinales m Commelinales m Zingiberales —a Zingiberales ri Dasypogonales pem m Arecales nane "RR o Orchidaceae Inferred evolution of (A) light availability and (B) moisture supply in Poales and immediate outgroups at the i a ] character Figure 4 family level under parsimony. Cases in which the ancestral c (see text) were coded as polymorphic, and both character state state for a family could not be inferred unequivocally s for the current-day, terminal taxa are indicated in the split box. Gray branches indicate equivocal resolution of character states in ancestral taxa Centrolepidaceae, and the forest-inhabiting grade from Flagellaria through the early divergent grass families, with fire ecology recurring in Ecdeiocolea- ceae and Poaceae (Fig. 5B). If Anarthriaceae had been included in this analysis, sister to the other restiid subfamilies as in other recent analyses (e.g.. Chase et al., 2006), then Restionaceae would have been resolved as retaining fireswept habitats rather than invading them anew. MULTIPLE ORIGINS OF WIND POLLINATION AND CORRELATED TRAITS Ancestral character-state reconstruction using the ML tree implies that wind pollination evolved at least five times in Poales: in Typhaceae, cyperids, restiids, Ecdeiocoleaceae, and the PACCMAD-BEP clade of Poaceae (Fig. 6). Animal pollination is inferred to be homologous across the commelinids. Based on ML testing in BayesTraits, pollination mechanisms in Poales and its immediate relatives showed correlated evolution with (1) floral showiness, (2) flower size, (3) floral sexuality, (4) nectar production. and (5) habitat openness (Table 1). Wind pollination was, as expected, associated with smaller, less pollination mechanism and ovule numbe a system (cosexuality vs. dioecy); the latter finding Annals of the Missouri Botanical Garden A. Nutrient supply poaceae O Sand and sandstone m |- PACCMAD-BEP m Fertile 1 + Puelioideae @ + Pharoideae m - Anomochlooideae O Rapateaceae tg Typhaceae — nm Bromeliaceae —— a Commelinales Zingiberales r—ü Dasypogonales Arecales — a Orchidaceae d lan Fia > 1 X Figure 5. Inf level (see Fig. 4). implies that unisexual flowers associated with wind pollination are typically found in cosexual plants. DiscussioN PHYLOGENY ML analysis of 81 coding regions from the plastid genome produced— within the limits of taxon sam- pling—the best resolved and most strongly supported phylogeny to date of Poales, the commelinids, and the monocots as whole, with a mean bootstrap support of 98.2% for all monocot nodes (Fig. 3). We focus on the ML tree because it had much higher bootstrap support for several crucial nodes within and outside Poales than the MP tree, including some that differ between the two trees; because Poales exhibits striking rate heterogeneity and a combination of very short and B. Fire Poaceae Ë B Rare m |- PACCMAD-BEP @ Frequent m Equivocal O F Puelioideae o f Pharoideae graminids B -Anomochlooideae m Ecdeiocoleaceae O Joinvilleaceae o Flagellariaceae m Restionaceae <0 Centrolepidaceae m Xyridaceae = oO Mayacaceae xyrids m Eriocaulaceae restiids 8 Cyperaceae üg Juncaceae cyperids — u Thurniaceae at the familv F very long branches in close proximity; and because ML generally outperforms MP in reconstructing phylogenies when faced with rate heterogeneity and long-branch attraction. The nodes at which the ML and MP trees differ are just those with very short and very long branches immediately juxtaposed, where long-branch attraction might be expected to be especially likely to distort phylogenetic reconstruction via parsimony. This was seen in the placement of the xyrids within Poales, the monophyly of the xyrids, the sister group to the Poales, relationships among the other commelinid orders, and the placement of Liliales (Fig. 3). The much higher rates of evolutionary divergence of plastid coding regions in Poaceae and allied families versus Arecaceae and Bromeliaceae have long been recognized (Gaut et al., 1992, 1996; > Givnish et al., 1999, 2004; Smith & Donoghue, 2008). u: A eet a a eae et | Nei aa SO Gl ac Saar no a epee REI cee anc hatin vee dh DIM d Lr dui perpe ADU EE MIS I M up Aha Lene cro P C Volume 97, Number 4 Givnish et al. 2010 lastome Sequence Phylogeny of Poales Pollination mode Poaceae a m | PACCMAD-BEP m Wind m + Puelioideae o A o - Anomochlooideae m Ecdeiocoleaceae o Joinvilleaceae o Flagellariaceae m Restionaceae m Centrolepidaceae o Xyridaceae dli o Mayacaceae xyrids o Eriocaulaceae m Cyperaceae m Juncaceae m Thurniaceae o Rapateaceae m Typhaceae o Bromeliaceae o Commelinales o Zingiberales o Dasypogonales o Arecales = x` Lidaraza Aree immediate outgroups, plotted at < - einn From top to bottom: Tripsacum dactyloi hexandra B. G. Briggs & L. A.S S. nee =. fastigiata R. Br. (Restionaceae), staminate illat plants; Carex pilulifera Willd. ex Kunth (Cyperaceae), staminate and pistillate stillate portions of inflorescence. ing (often centrally attached) anthers. Figure 6. Minimum of five independent origins of wind pollination within Poales and mo level. Drawings show typical floral and/or infloresce € for eac (Poaceae), staminate and pistillate portions of e (Ecol eaceae), floral spi ike with zones of male and female bonn s ns an portions of inflorescence; and Sparganium emersu » Rd (Typhaceae), staminate and pisti Note long and/or plumose branches of styles in à case and mostly large, dangli Annals of the Missouri Botanical Garden Table 1. Summary of tests for correlated evolution of wind pollination with various plant traits. Significance Significance Trait with k = 1 with optimal « Flower size P « 0.012 P « 0.027 Floral showiness P « 0.0034 P « 0013 Floral sexuality P « 0.0002 P « 0.0005 Habitat openness P « 0.013 P « 0.02 Nectar production P « 0.035 P « 0.038 Dioecy NS NS Ovule number NS NS NS, not significant. RELATIONSHIPS WITHIN POALES The ML and MP trees agree in placing, with strong support, Bromeliaceae, Typhaceae, and Rapateaceae as successive sister li to all other members of order Poales (Figs. 2, 3). The lowest support, with 87%—97% bootstrap T is T - position of Typhaceae, whose sister gr branch for any family within Poales. ae a the relation- ships among these three families has been problem- atie. Michelangeli et al. (2003) used sequences of "— rbcL and mitochondrial atpB to place Rapa- teaceae plus the xyrids as sister to all other Poales. Bremer (2002) and Davis et al. (2004), using the same genes, placed Rapateaceae alone as sister to all other Poales, with Bromeliaceae being sister to Typhaceae, and both being sister to the remainder of the order, followed by Eriocaulaceae plus most Xyridaceae; jackknife support for most of these relationships, however, was quite low. Givnish et al. (2005, 2006) F sequences to place Bromeliaceae plus Typhaceae sister to all other Poales, followed by Rapateaceae. Christin et al. (2008) used ndhF and rbcL to reach a similar soigne but did not include Rapateaceae. Graham et al. (2006) used sequences of 17 plastid genes and spacers to place Typhaceae as sister to all other Poales, followed by Bromeliaceae. Only Chase et al. (2006), using data for four plastid genes, two nuclear genes, and one mitochondrial ge gene recovered the branching pattern for Bromeliaceae, Typhaceae, and Rapateaceae that we found, but they had low (less than 50%) bootstrap support for the position of Typhaceae. The stro support for the branching pattern of * e sala minie to other Poales in both their position and branching pattern. The absence of nectaries from all Poales except dice and a few derived Rapateaceae (where such nectaries have apparently reevolved [Givnish et al, 2000] helps suppor the placement of Bromeliaceae at the base of the order. ML placed the cyperids sister to all other Poales except Bromeliaceae, Typhaceae, and Rapa- teaceae, with the branching topology among the three amilies identical to that found by most broadscale monocot analyses since Givnish et al. (1999) used rbcL sequences to place Cyperaceae and Juncaceae. The most vexing issue involves the position of the xyrids. Our MP tree identified these as monophyletic and sister to the cyperids, but it identified Abolboda of Xyridaceae as sister to Mayaca of Mayacaceae and Syngonanthus of Eriocaulaceae (Fig. 2). However, there was only 68% bootstrap support for the monophyly of the xyrids in the MP tree, and only 78% support for its position sister to the cyperids. In the ML tree (Fig. 3), the xyrids were a grade rather than a clade, with Abolboda sister to the restiids— graminids with 100% support, followed by Mayaca- Syngonanthus with 97% support. The difficulty here, undoubtedly, is the great length of the branches leading to each of the three families of xyrids, relative to the short length of branches joining those families. Our placement of the xyrid families, based on the ML tree, should be viewed as tentative, with a need for sequencing additional species to help break up the long branches within i Thurniaceae sister to Eriocaulaceae and Xyridaceae sister to each other in analyses that included Mayaca; Bremer (2002) placed these families sister to each other but did not include Mayaca. Givnish et al. (2005, 2006) placed Eriocau- laceae—Xyridaceae sister to the cyperids, with Maya- ceae sister to the broader group; Chase et al. (2006) identified Mayaca as sister to the ae followed by Eriocaulaceae—Xyridaceae. Graham e ) obtained results consistent with those of bison et al. (2005, 2006), but - not include Eriocaulaceae. Davis et al. (2004) placed Mayaca plus Xyris L. (plus Hydatella Diels) aaa to the cyperids, with the remainder of Xyridaceae plus Eriocaulaceae sister to that group. Givnish et al. (1999), Bremer (2002), and Christin et al. (2008) placed Eriocaulaceae—Xyrida- ceae sister to the restiid-graminid clade. We note that that position is consistent with Eriocaulaceae and Xyridaceae sharing the absence of a parietal cell in the nucellus with the graminids, but excluding Flagellaria (Rudall, 1997) and restiids (Givnish et al, 1999). Missing data for the xyrids (see above) do not account for their placement. When we exclude all genes not represented in all three xyrid placeholders, ML yi yields exactly the same branching topology (albeit with weaker support) within Poales. Placement of the xyrids should not be viewed simply as a choice being sister to the cyperids versus the clade. Volume 97, Number 4 Givnish et al. 2010 Plastome Phylogeny of Poales own analyses, Mayaca was sister to the cyperids plus assumed or concluded that Joinvillea was sister to the the restiid-graminid clade. Christin et al. (2008) placed Mayaca sister to the cyperids alone. Morphologically, there is relatively little evidence tying Mayacaceae to Eriocaulaceae and Xyridaceae (see Givnish et al., 1999; Stevens, 2009). These three families are the remnants of the order Commelinales recognized by Dahlgren and Clifford (1982) and Dahlgren et al. (1985) before Givnish et al. (1999) used rbcL sequence data to exclude Commelinaceae and Rapateaceae. All five families share nuclear endosperm and showy flowers with differentiated petals and sepals; both characters are more broadly plesiomorphic in commelinids (Givnish et al., 1999; Stevens, 2009). In other words, there is relatively little evidence to support an expectation that these three families will form a clade when additional plastome sequence data are added to future analyses. The position of the restiids as sister to the graminids in both the MP and ML trees (Figs. 2, 3) accords with the results presented by Chase et al. 2006) and is consistent with their positions in the incompletely resolved tree presented by Givnish et al. (2005, 2006). The only point of disagreement involves the placement of Flagellaria, which was sister to the restiids and the graminids by Michelangeli et al. 2003), sister to the cyperids plus Xyris, Mayaca, and Trithuria Hook. f. (Hydatellaceae) by Davis et al. (2004), and sister to Elegia L. (Restionaceae) plus representatives of the other graminid families by Givnish et al. (1999) and Graham et al. (2006). Our sampling includes only a single representative for each of the families Restionaceae and Centrolepida- ceae, with none for Anarthriaceae. Anarthriaceae, when included in broadscale phylogenetic studies based on molecular data, has usually been placed sister to Centrolepidaceae—Restionaceae (Briggs et - ; Bremer, 2002; Michelangeli et al., 2003; Davis et al., 2004; Chase et al., 2006). Centrolepida- ceae was sister to Restionaceae in most broadscale molecular studies, but some (e.g. Bremer, 2002; Briggs et al., 2010) have embedded it in Restiona- ceae, while Briggs and Linder (2009) regarded its — ved. Within the graminids, our data confirm that agellariaceae, Joinvilleaceae, and Ecdeiocoleaceae are successively sister to ever-narrower subsets of the graminids, with Ecdeiocoleaceae sister to Poaceae- This branching topology concurs with those docu- mented by Bremer (2002), Chase et al. (2006), and Graham et al. (2006), but conflicts with those of Marchant and Briggs (2007), Christin et al. (2008), and others that place Joinvillea sister to i leaceae, with both sister to Poaceae. Early studies on morphological or molecular data either grasses (e.g., Campbell & Kellogg, 1987; Chase et al., 1995a, b; Clark et al., 1995; Kellogg & Linder, 1995; Stevenson & Loconte, 1995; Soreng & Davis, 1998; Grass Phylogeny Working Group I, 2001). Briggs et al. (2010) were unable to resolve a trichotomy involving the grasses, Joinvillea, and Ecdeiocoleaceae. Doyle et al. (1992) discovered a 28-kb inversion in the chloroplast genome that united Joinvilleaceae, Ec- deiocoleaceae, and Poaceae; they detected a 6-kb inversion in Joinvilleaceae and Poaceae, but were unable to amplify the region in question for Ecdeiocoleaceae. Several subsequent authors con- fused the absence of data on the 6-kb inversion with absence of that inversion in Ecdeiocoleaceae, until Michelangeli et al. (2003) demonstrated that the inversion was indeed present in that family, and that rbcL and atpB sequence data supported (albeit quite weakly) a sister-group relationship between Ecdei- ocolea F. Muell. and the grasses. In retrospect, a key morphological character used Campbell and Kellogg (1987), Kellogg and Linder (1995), and Kellogg (2000) as a sy y to unite Join- villeaceae and P: ly, the presence and short cells in the leaf epidermis—may be seen to exclude Ecdeiocoleaceae. Although adult plants of Ecdeiocolea have scarcely any development of leaf blades, juvenile plants of i and adult Georgeantha B. G. Briggs & L. A. S. Johnson (Briggs & Johnson, 1998) show substantial leaf blades with no evidence of a long and short cell pattern (Briggs, pers. obs.). Thus, the presence of long and short cells in the leaf epidermis either evolved twice (in Poaceae and Joinvilleaceae) or—perhaps more likely—arose once in the common ancestor of Joinvilleaceae-(Ecdeioco- leaceae-Poaceae) and ntly was lost in the highly reduced Ecdeiocoleaceae. Within Poaceae, our data confirm that Anomochloa Brongn. and Streptochaeta Schrad. ex Nees are sister taxa, forming subfamily Anomochlooideae; this sub- family is, in turn, sister to the remainder of the family (see Clark et al., 1995; Grass Phylogeny Working Group I, 2001; Christin et al., 2008). The latter lineage is characterized by the presence of the typical ideae spikelet clade (Grass Phylogeny Working Group I, 2001). Relationships among the remaining grasses generally accord with those found using molecular data by Grass Phylogeny Working Group I (2001), Hodkinson et al. (20072, b), Bouchenak-Khelladi et al. (2008), and Saarela and Graham (2010). We hope to add several additional plastome sequences in the near future to permit detailed analyses of evolution within the Poaceae. 598 Annals of the Missouri Botanical Garden RELATIONSHIPS AMONG COMMELINID ORDERS The ML phylogeny presented provides the first Lun ag (93% bootstrap) evidence for the sister grou h grasses, bromeliads, and their allies (Fig. 3). The two remaining commelinid orders, Arecales and Dasypo- gonales, also form a clade with relatively strong (87% bootstrap) support, which is sister to the clade formed by ers. Me of the recent ng monocots ypogonales sister to Commelinales—Zingiber- ales plus — Given that our MP analysis retrieved alternative, albeit weakly supported topology (Fig. 2), our T conchis regerding stil relatiop- wae We plan to include multiple representa- tives of each family in analyses in the near future, using increased taxon sampling density to confront the difficulties caused by long-branch attraction and striking variation in evolutionary rates within the commelinids. For now, however, we note that the sister-group relationship between Poales and Comme- linales—Zingiberales is supported by possession of (1) starchy endosperm across all taxa surveyed and (2)a distichous or tristichous phyllotaxy across most families (except for Bromeliaceae, Mayacaceae, Cannaceae, Costaceae, Musaceae, and scattered cases in other families, e.g., Palisota Rehb. ex Endl. in Commelinaceae [Faden, 1988; Givnish et al., 1999]. The sister-group relationship of Arecales e Dasy- pogonales is supported by the possession of a woody habit in all of the former and most of the latter. Identification of woodiness as a synapomorphy for Arecales-Dasypogonales must await further evidence on relationships within Dasypogonaceae ANCESTRAL HABITAT RECONSTRUCTIONS Th anal Esos DEE » h Rh sunny, damp to wet, highly infertile, ai rite (see Givnish et al., 1999; Linder & Rudall, 2005). Today, these conditions typify the family, either as a whole or in early divergent members (e.g., Brocchinia) in six cases: Bromeliaceae, Rapateaceae, Eriocaula- ceae, Xyridaceae, Ecdeiocoleaceae, and Restionaceae (see Figs. 4, 5). However, the most species-rich families, Poaceae and Cyperaceae, often occur on more fertile substrates. Relatively few families and species are associated with forest — _ environments (Fig. 4A), which h elps t wind pollination within the cles. £ USCA y UL REPEATED EVOLUTION OF WIND POLLINATION IN POALES Analyses based on our ML phylogeny indicate that wind pollination has arisen at least five times within es—in Typhaceae, the cyperids, the restiids, Ecdeiocoleaceae, avi the lu clade of Poaceae (Fig. 6). This contrasts with three origins of wind pollination in Poales as inferred by Givnish et al. (1999) and Linder and Rudall (2005). Partly, this difference in conclusions is a result of different branching topologies, and partly, of different assump- tions as to which taxa are wind pollinated. We assumed that insects pollinate Flagellaria and Join- that insects pollinate Anomochloa, Streptochaeta, and Pharus P. Browne in Poaceae. Nothing certain is known about the pollina- tion of these grasses. But the fact that all three lack feathery stigmas and versatile anthers on slender stamen filaments, both of which are usually associated with wind pollination, argues for their pollination by animals (Soderstrom, 1981; Soreng & Davis, 1998). In addition, Anomochloa, Streptochaeta, and at least one member of Pharoideae have grouped pollen granules with high exine relief, characters that are not associated with wind pollination in Poaceae (Page. 1978). Insect pollination has also been observed or inferred in a number of forest-dwelling bamboo grasses in herbaceous tribes Olyreae, Parianeae, and woody Bambuseae (Soderstrom & Calderén, 1971, 1979; Chapman, 1990; Salgado-Labouriau et al., 1992; Soreng & Davis, 1998); the placement of bamboos in the BEP clade (Grass Phylogeny Working Group I, 2001; Bouchenak-Khelladi et al., 2008) animal-plliassed F "e and Joinvillea in rai and li gap “cleanly argues din any additional £ uud lh + graminids t would he an addis; i: igi In ruin. animal pollination in Aiid and Pharoideae supports separate origins of wind pollination in Ecdeiocoleaceae and the PACCMAD-BEP clade of Poaceae based on our phylogeny (Fig. 6). As predicted by several investigators and demon- strated across a wide sampling of angiosperms by Friedman ane Barrett e we feld that animal pollinati significan lation with floral showiness, flower size, floral decim. nectar pro- duction, and habitat openness (Table 1). Wind pollination was strongly associated, as predicted, with smaller, less conspicuous, often unisexual flowers. absence of nectar, and open habitats. Smaller and less Volume 97, Number 4 Givnish et al. Plastome Sequence Phylogeny of Poales brightly colored flowers, often involving the loss of petals and/or sepals and nectar, are expected in wind- pollinated species given the energetic costs of these attractive structures, as well as the lack of utility of such structures in wind-pollinated taxa, and the possibility that the presence of petals and/or sepals, especially large ones, might interfere with the arrival of wind-borne pollen to stigmatic surfaces (see Linder, 1998; Culley et al., 2002; Linder & Rudall, 2005; Friedman & Barrett, 2008). It should be recognized that there is no need to invoke reevolution of petals and/or sepals in Flagellaria and Joinvillea, given the continuity of an ancestral line pollinated by animals up to the PACCMAD-BEP clade (Fig. 6). Wind pollination and unisexual flowers—and their animal pollination with hermaphroditic hould be associated because the reduced cost and increased benefits of attractive structures for attracting and dispersing pollen in hermaphroditic flowers applies only to animal-pollinated taxa (Giv- nish, 1980; Pts — p — unisexuality could help gging in Vitia riolfinated ii given that the latter produce large amounts of pollen (Givnish, 1980; Lloyd & Webb, 1986; Charlesworth, 1993). The exceptional statistical significance of correlated evolution between wind pollination and unisexual flowers in analyses that include or exclude optimization of x (P < 0.0005 and P < 0.0002, respectively) most likely has to do with the widespread occurrence of unisexual flowers in Poales, in nine of 16 families and a total of at least six clades E that are open and windswept—even if only asonally, as in the canopy of temperate deciduous end favor wind d conversely, windless understories favor animal pollination (Lin- der, 1998; Culley et al., 2002: adil & Barrett 2008). However, the large number of stead patton ed families of Poales found ancestrally in open habitats (Bromeliaceae, Eriocaulaceae, Mayacaceae, Xyridaceae) reduces the strength of the evolutionary correlation between habitat and pollination mecha- nism in the order. There is, however, a nearly P inverse, flowers—s oma elacoing - including Typhaceae and the cyperids in open wetlands, and restiids, Ecdeiocoleaceae, and the PACCMAD-BEP clade of Poaceae in open, often seasonally arid or fireswept upland habitats. Note the association of putative insect pollination with forest understories and edges in Flagellaria. Join- villea, and anomoochloid, pharoid, and olyroid grasses (see Soderstrom & Calderón, 1971, and preceding discussion). amas haqta e to insect : nation (not shown in Fig.6) hav e occured in scattered species in several genera ‘of Cyperaceae with brightly colored or fragrant inflorescences (e.g., Ascolepis Nees ex Steud., haris R. Br., Hypolytrum Rich., Mapania Aubl., Vahl sect. Dichromena (Michx.) Griseb. [Goetghebeur, 1998; Magalhàes et al., 2009)); several of these taxa grow in forest dili Nectar production should be negatively associated with wind pollination given the costs of producing nectar and its lack of utility in anemophilous species. Conversely, in some (but not all) animal-pollinated species, nectar ies as an dent. The correlation in Poales is PRORA but surprisingly weak (T. ned > with the latter probably reflecting the near of ies in the order outside the ad Even though Friedman and Barrett (2008) found that nectar production had the strongest pattern of correlated evolution with pollination mechanism of any factor they surveyed across the angiosperms, it would be difficult for such a pattern to occur in any lineage that is nearly uniform in nectar production or its absence. We coded Potarophytum Seidwith, the metae for Rapateaceae, as having septal nectari on their presence in Spathanthus Dos: (Venturelli & Bouman, 1988) of tribe Rapateeae and in Guacamaya Maguire, Kun- hardtia Maguire, and Schoenocephalium Seub. of tribe Schoenocephalieae (Givnish et al., 2004). However, are probably only of sporadic occur- rence in Rapateaceae; they have not been observed as yet in other members of the n: and Renner (1989) described buzz pollination for Saxo-fridericia R. H. Schomb. (tribe E acia) and Stegolepis Klotzsch ex Kórn. (tribe Stegolepideae). lf we assume that the ancestral condition for Rapateaceae is a lack of nectaries, then the e cas betweeen pollination mechanism and nectar tion remains weakly significant (P « 0.045 e K = l and P « 0.032 for Ds K). ectaries appear to have evolved independently in ae variously associated with petal ap- ndages, staminodes, —— and pistils (Stützel, 1986; Rosa & Scatena, 2003, 2007; Ramos et al., 2005; Oriani et al., 2009), and in Xyridaceae, associated with stylar appendages in Abolboda (Stützel, 1990). Flagellaria secretes large amounts of nectar, with high concentrations of sugar and amino acids, from extrafloral nectaries and attracts large numbers of ants (Blüthgen « et al., —À " — & Fiedler, 2004); th 969) almost surely are attracted by these almost no effect on the significance of correlated evolution between pollination mechanism and nectar Annals of the Missouri Botanical Garden production, with P < 0.047 for tests with and without optimization of K. If scoring were reversed for Flagellaria and Rapateaceae, the correlation between pollination mechanism and nectar production would be marginally nonsignificant (P < 0.058 for k = 1 and P < 0.064 for optimal x). The near absence of dioecy in Poales outside the restiids probably explains the nonsignificance of correlated evolution between wind pollination and dioecy in the order (Ta able 1). Ta such a pattern is manifest acros , only the restiids show a high proportion of doc: species within Poales, with seattered dioecious species or populations—not likely to be scored in an analysis involving so few terminals as the current study—in Cyperaceae, Eriocaulaceae, Poaceae, and Typhaceae (Connor, 1981; Linder & Rudall, 2005). Low levels of dioecy at the familial level in Poales might be expected as based on the near absence of the woody habit and fleshy fruits at that level, given that both traits are strongly associated with dioec i and gymnosperms (Givnish, 1980; Renner & Ricklefs, 1995). Finally. phylogenetic conservatism appears account for the lack tion to a single ovule is expected in wind-pollinated taxa given the presumed low probability of multiple pollen grains arriving on a single stigma (Dowding, 1987; Linder, 1998; Friedman & Barrett, 2008; but see Friedman & Barrett, 2009). However, in Poales, single ovules per carpel characterize the entire restiid-graminid clade irrespective of pollination mode, while multiple ovules characterize many o the taxa in the grade including Rapateaceae, the cyperids, and xyrids, again largely independent of pollination mode. Two general questions that have not been satisfac- torily addressed by previous authors remain: (1) why is wind pollination so widespread in Poales? and (2) why has wind pollination evolved five times indepen- dently in a single monocot order, when wind pollination is so rare in monocots? Of the factors just tested for correlated evolution with wind pollination, only one—open habitats—could be considered a 1982; Dahlgren et al., 1985; Lider 1998; Sakae & Barrett, 2009). Potential factors favoring wind pollination identified by previous authors include open, windswept habitats (see above), local domi- nance by conspecifics (Regal, 1982), and the absence or inefficiency of animal pollinators or the low quality of pollen delivered by them (Whitehead, 1983; Berry & Calvo, 1989; Cox, 1991; Weller et al., 1998; Culley et al., 2002). Strongly windswept habitats might also have poor animal visitation, so the first and third of these mechanisms are partly linked. Regal (1982) argued that high densities of conspecifics would favor wind-pollinated species, given the inherent ineffi- ciencies of pollen delivery. to conspecific stigmas in several studies show that pollen delivery to conspe- cific stigmas drops rapidly with decreasing conspe- cific density in wind-pollinated taxa (Friedman & Barrett, 2009), and that such taxa have very high pollen:ovule ratios (Cruden, 1977, 2000). But why have Poales evolved and retained wind pollination so frequently? One factor surely is that ng. fire, and/or extreme soil infertility, and that open G. Kakita were reinvaded by two additional lineages, Ecdeiocoleaceae and the PACC- MAD-BEP clade of Poaceae (Figs. 4—6). In addition, we pro that four additional prime movers favor wind pollination in herbs, including (1) tall stature, (2) vigorous vegetative spread, (3) adaptation to patchy disturbance by fire and/or flooding, and (4) positive f ck on conspecific abundance. These traits would all help generate high local dominance—and (1) through (3) above characterize all lineages that evolved or retained wind pollination in Poales, except for Ecdeiocoleaceae and Centrolepidaceae. Win pollination in the latter two families may have favored selection for reproductive assurance in i harsh, windswept alpine habitats and extremely infertile, fireswept, or seasonally inundated microsites they occupy. Goodwillie (1999) argued that wind pollination could provide such assurance—without the disadvantage of inbreeding associated with self- important for annual plants, given their need to produce seeds at the end of each growing season if an individual's genes are to enter the next generation, and given the likely spatial autocorrelation of poor conditions for pollinators. Tall stature, vigorous vegetative spread, adaptation to patchy disturbances, and/or positive feedback on conspecific i "icula RUNS mM Cer UU repr sau Volume 97, Number 4 2010 Givnish et al. Plastome Sequence Phylogeny of Poales habitats subject to frequent flooding and siltation, which are inimical to seedling establishment in most species, and to which few other species are adapted; Typhaceae gain high local dominance through advantages in height, rapid rhizomatous spread, and ili in wet, anoxic soils. Many grow below closed canopies, where wind pollination should be a disadvantage. However, there are some genera (e.g., Brocchinia [Bromeliaceae] and Stegolepis [Rapateaceae]) in these two families that spread and form extensive, dense colonies on wet soil or rock surfaces, and it is not clear why wind pollination has not evolved in them. Extremely low growth rates in such habitats might prevent such plants from spreading and reachin dominance for a substantial period after initial colonization of area, working against wind pollination. The origin of wind pollination in the cyperids may be related to invasion and rapid rhizomatous spread within frequently flooded or burnt areas. Thurnia of Thurniaceae forms massive colonies in streams on the Guayana Shield where few other plants grow; Prionium of the same family forms large monocultures in seasonal stream- beds on sandstone in South Africa, which are flooded and burnt at frequent intervals. Retention of animal pollination by Eriocaulaceae, Xyridaceae, and Mayacaceae despite their occurrence in frequently flooded or burnt sites may be related to their short stature and limited ability to achieve local dominance and spread laterally for any substantial distance. Their small size and slow growth almost surely reflect their occurrence in areas with wet, exceedingly poor soil. They usually inhabit sandy seepage zones and seasonal ponds where nutrients are not delivered in substantial amounts of transported sediment, unlike large-statured Thurnia and Prionium found in streams on similar sand or sandstone substrates. Invasion of fire-prone, summer-dry upland habitats over infertile soils, as well as seasonall microsites, by the restiids may help account for their local dominance and evolution of wind pollination (Linder & Rudall, 2005). Frequent, heavy rainfall and Strong winds in some parts of western and montane Tasmania— where several early divergent taxa occur might also favor wind pollination in restiids for pollination assurance. We argue (see above) that pollinator assurance was the primary driver toward anemophily in annual Centrolepidaceae that inhabit extremely infertile, seasonally wet depressions and rock pockets in southern Australia (Pignatti & Pignatti, 1994, 2005; Cooke, 2010). Pollination assurance probably also drove the origin and maintenance of wind pollination in tiny, perennial centrolepid cushion plants at high elevations in Tasmania and New Guinea, given local the harsh conditions for pollinators there and the extremely short stature and lack of local dominance of the centrolepids. Interestingly, both kinds of communi- ties are also inhabited by strikingly convergent species of Trithuria (Nymphaeales: Hydatellaceae). Preliminary studies suggest that at least one of these (T. submersa Hook. f., in Western Australia) is also wind pollinated (Taylor & Williams, 2009). Reinvasion of shaded habitats on more fertile, well- drained, unburnt sites by Flagellaria and Joinvillea favored reevolution of animal pollination, accompa- nied in Flagellaria by a small but conspicuously white corolla and scented flowers (Backer, 1951), abundant supply of extrafloral nectar (Blüthgen et al., 2004a, b; Blüthgen & Fiedler, 2004), and visitation by ants (Newell, 1969). Apparent retention of animal pollina- tion in the anomoochloid and pharoi ` presumably was favored by their restriction to forest understories. Finally, evolution and retention of wind pollination in the vast PACCMAD-BEP clade of Poaceae appear to have been favored by invasion of open habitats and achievement of high local domi- nance. Factors promoting such dominance might include (1) moderate to tall stature, usually combined with rapid rhizomatous spread; (2) morphological and physiological adaptations of grasses (e.g.. narrow, erect foliage, C4 photosynthesis) to widespread drought under bright, warm conditions starting in the Eocene and intensifying in the Miocene (Kellogg. 2000: Edwards & Smith, 2010); (3) positive feedback among grasses, fire, and nitrogen, given the low nitrogen dd position rate of C, grasses and thus their flammability, the tolerance of grasses to fire due to their basal leaf meristems, the volatilization of nitrogen during fires, and the low nitrogen i of C, grasses (Seastedt et al, 1991; Wedin, 1995; Blair, 1997; Knapp et al., 1998; Reed et al., 2005); (4) positive feedback between grasses and grazers, given the attractiveness of grasses to many grazers, their resistance to grazing damage conferred by basal meristems, and collateral damage by grazers to other plants while seeking grasses (Archibald, 2008); and (5) positive feedback between grasses and their horizontally and vertically transmitted fungal endophytes (e-g-» Epichloë Tul. & C. Tul., Clavicipi- taceae, Ascomycota), based on protection against herbivores provided by the alkaloids secreted by the endophytes, resulting increases in the local frequency of infected grasses, and consequent increases in transmission of the endophytes to uninfected grasses (see Rudgers et al, 2009). An additional factor favoring at least temporary local dominance in grasses may involve (6) the negative effect that certain grasses have on nongrasses, at least in the short term, via the very large absorptive root surface developed by content Annals of the Missouri Botanical Garden grasses and their consequent ability to reduce the levels of soil nitrate available to other plants di Craine, Re Dybzinski & Tilman, 2007). The gre. id grasses in cool areas (Ed Smith, c might reflect (1), (4), (5), aie (6), or some as yet unidentified ecological advantage of that "€ the quiu of panicoid grasses in warmer, dryer robably reflects at least factors (1) le (o. det tun none of the proposed factors would have operated in early divergent grasses native to tropical forest understories. Wind pollination ost woody bamboos probably reflects its origin in the E PACCMAD-BEP m (Fig. 6). The alternative— that it represents yet another gain (i.e., a transition from animal-pollinated bamboos)—seems unlikely, given the restriction of known instances of animal pollination to a few understory genera of herbaceous bamboos, such as Eremitis Dóll, Ol & Calderón, 1971, 1979), which appear to be sister to the woody bamboos (see Bouchenak-Khelladi et al., 2008). Animal pollination might occur in a few woody bamboos (e.g., Chusquea Kunth; Janzen, 1976). If it does, it vids, represent a secondary gain of animal pollination, but our knowledge of bamboo pollination is far too rudimentary to hazard any analysis at this time. The retention of wind pollination in woody bamboos might be due to (7) their inability to sustain animal pollinators over the multi-year intervals between mass flowering events, driven by selection to satiate seed predators that feed on the unusually numerous (and sometimes unusually large) bamboo seeds, which like other grass seeds are nutritious and chemically unprotected (Janzen, 1976). Our is of the evolution of wind pollination in Poales has thus produced several new insights, including a revision upward from three independent origins of wind pollination. In addition, we have shown that some traits that show a significant correlation with wind pollination across the angio- sperms fail to do so within Poales, apparently due to phylogenetic conservatism in ovule number and non- dioecious breeding systems. Our analyses confirm that open habitats, lack of nectar production, and small, nonshowy, unisexual flowers show significant patterns of correlated evolution with wind pollination. Finally, we have proposed specific mechanisms— including several new ideas regarding the potential significance of plant stature, vegetative spread, and local positive feedback—to account for each of the five origins of wind pollination in Poales. Our predictions call for several new tests and for rigorous studies of pollination biology in some critical taxa (e. g-, Flagellaria, Join- villea, and the anomochlooid, pharoid, puelioid, and bambusoid grasses). e tudi latively widespread Pharus J 11 might be especially interesting. CONCLUSION Deriving a monocot phylogeny based on plas- of the Monocot AToL Team—is designed to increase, to the maximum extent possible, the t ha plerieguiittin ENANA that can be cenom: tomes—a core numbers of bases per taxon resolution and likely acc uracy of the resulting estimates of phylogen taxonomic groups w dense and aai sampling of taxa (Hillis, 1996; Givnish & Sytsma, 1997; Graybeal, 1998; Soltis et al., 1998; Hillis et al., 2003; Graham et al., 2006 Jansen et al., 2007). Our plastid data, including 25,107 informative sites, represent a 38-fold increase in the number of such sites over the pioneering study of monocot phylogeny by Duvall et al. (1993b), based on sequences of the single plastid gene rbcL and a comparable number of taxa. In the intervening years, monocot researchers increased the number of infor- mative characters by sequencing genes that evolve faster (e.g., Fuse & Tamura, 2000, for matK; Givnish et al., 2005, for ndhF) or by concatenating and analyzing the sequences of several genes. The latter, multigene strategy has proven the more productive approach (e.g., see Chase et al., 2000; Soltis et al., 2000; Qiu et al., 2005), partly due to the difficulty of dindi increase the sasa 1997). Chase et al d 4777 informative sites dion seven genes from the plastid, nuclear, and mitochondrial genomes to reconstruct relationships among 136 monocot taxa; Graham et al. (2 used 5617 informative sites from 17 plastid omoplasy associated with such regions (Givnish & (2006) use monocot taxa. informative characters 5.3- to 8.6-fold over Duvall et al. (1993b) and increased the number of informative characters per taxon from 6.3 to 26 to 60. The study presented here—using 81 plastid genes and over 100 kb of aligned sequence data per taxon— represents a further inerease of fourfold to sixfold in data density per taxon, resulting in a ratio of informative sites per taxon. Our study, and similar ones recently using 61 to 81 plastid gene egg (Goremykin et al., ; Leebens-Mack et al., 2005; Cai et al., 2006; Min et al., 2007; Moore et al, 2007) to address angiosperm and land-plant relationships, mark the transition from plant multi- gene phylogenetics to phylogenomics. However, it Volume 97, Number 4 2010 Givnish et al. Plastome Sequence Phylogeny of Poales must be recognized that obtaining an avalanche of data—by sequencing plastomes in this project and, ultimately, transcriptomes and whole nuclear genomes in future analyses—will not relieve us of the need to complement large amounts of data per taxon with adequate taxon sampling. Long-branch attraction is a challenge that must constantly be kept in mind (Soltis bens-Mack et al., 2005; Whitfield more than fivefold variation in evolutionary rates in commelinids, the presence of numerous very long and very short branches in immediate proximity to each other, the conflict between the results of MP and ML analyses, and the current density of taxon sampling, long-branch attraction is clearly an issue. Relation- ships of the xyrids to each other, and to other members of the order, manifestly need additional taxon sampling and analysis to resolve. The appropriate level of taxon sampling density required to comple- ment ever-rising amounts of sequence data per taxon is a central issue that must continue to be confronted theoretically (e.g., Geuten et al., 2007) and empiri- cally (e.g., Soltis & Soltis, 2004; Leebens-Mack et al., 2005). To address these and other concerns, in the near future we plan to increase taxon sampling in Poales several-fold, and to explore additional analyt- ical techniques (e.g., Lartillot et al., 2007) that may be less sensitive to long-branch attraction. Increased taxon sampling will also increase the power of comparative studies and of searches for morphological and anatomical synapomorphies for individual clades, and make careful calibration of our molecular tree and biogeographic analyses possible. The results present- ed here, however, show that even with the existing extent of taxon sampling, inferring a phylogeny — 9n whole plastid genomes can produce numerous ne insights into monocot relationships and patterns of ive evolution at broad scales. 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Is sparse taxon sampling a problem for phylogenetic inference? Syst. Biol. 52: 124—126. Hiratsuka, J., H. Shimada, R. Whittier, T. Ishibashi, M. Sakamoto, M. Mori, C. Kondo, Y. Honji, C. R. de B. Y. counts for a major plastid DNA inversion duri E tion of cereals. Molec. Gen. Genet. 217: 1 Hodkinson, T. R., M. W. Chase, Y. Bouchenak- Khelladi, S. A. aaa & V. Savolainen. 2007a. Large trees, supertrees and diversification of the grass family. Aliso 23: 248-258, — V. Sav laa S. W. L. Jacobs, Y. Bouchenak- Khelladi, M. S. Kinney & N. Salamin. 2007b. Pp. 275- 295 in T. R & J. A. N. Pamell pe Press, Boca Raton, Florida. Huelsenbeck, J LP. 1995. The robustness of two Phylogenetic of maximum likelihood over neighbor joining. g. Molec. Biol. Evol. 12: 843-849. & D. M. Hillis. 1993. Success of prae methods in the ai; Bs J. Alverson. R. Peery, S. J. Herman, H. M. Fourcade, J. V. Kuehl, J. R. Volume 97, Number 4 2010 Givnish et al. Plastome Sequence Phylogeny of Poales McNeal, J. Leebens-Mack & L. Cui. 2005. Methods for obtaining and analyzing chloroplast genome sequences. Meth. Enzymol. 395: 348-384. vi Caittanis, + prid S. B. Lee, J. Tomkins, A. J. Alverson & H. Dani 006. Phylogenetic — of Vitis “Wi itaceae) he on ee chloroplast genome sequences: Effects of taxon sampling and lacada: methods on resolving relationships among rosids. BMC Evol. Biol. 6: 32. Z. Cai, L. A. Raubeson, H. Daniell, C. W. diPusphilis; š: P = F. pean Gui- singer-Bellian, R. C. K. . W. Chumley, S. -B. Lee, R. "cl R LN V v. ica FL Boon 2007. Analysis of 81 genes from 64 plastid genomes resolves relationships in angiosperms and identifies genome-scale evolutionary patterns. Proc. Natl. Acad. Sci. U.S.A. 104: 19369-19374. Janssen, T. & K. Bremer. 2004. The age of major monocot LE inferred from 800-- rbcL sequences. Bot. J. Linn. Soc. 146: 385—398 m D. H. 19 76. Why n wait so long to flower. nn. Rev. Ecol. Syst. 7: 347— ee L. B. 2005. Phylogeny w. RE ro and the Zingiberales based on six DNA regions. Syst. 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Monocots— of the stematics ws im ution. y: Interna rence on the tional C the Monocots, Puri CSIRO, Melbourne tes. J. Molec. Evol. 39: 3 306-314. ond Zomletr, : W. B. 1999. Mepa in nin rm n Compara Biology of Soc. 126: 58-62. be N.-S. Lin & C.-S. Lin. 2009. "—— MT us latiflorus Bambusa old- enomes. hes Phys e^ 847-856. & J.L oore. 2004. Automatic i Maximum MN phylogenetic sequences h variable rates over paragales. J. Torr y Bot. APPENDIX l. Taxa included in study, with GenBank accession numbers and voucher data. GenBank accession Major clade Order Family Species numbers* Voucher data' Basal Amborellales Amborellaceae reg trichopoda NC_005086 Goremykin et al., angiosperms Bail a Nymphaeales Nymphaeaceae Mucio Aiton NC 008788 Raubeson et al., 2007 Austrobaileyales Schisandraceae a Nn NC. 009600 Hansen et al., 2007 rr. & Chun Magnoliids Canellales Winteraceae d mys granadensis L. f. | Cai et al., 2006 Laurales Calycanthaceae Calycanthus floridus L. NC_004993 Goremykin et al., 2003b Magnoliales Magnoliaceae ndron — L. NC_008326 Cai et al., XN iperales raceae Piper cenocladum Di NC. 008457 Cai et al., Eudicots Ranunculales Berberidaceae Nandina domestica oue NC. 0083. ceed a 3 ra 2007 Proteales Platanaceae Platanus occidentalis L. NC_008335 Moore et al., 2006 Buxales Buxaceae Buxus microphylla NC_009599 Hansen et "i 2007 Siebold & Zucc Cucurbitales Cucurbitaceae Cucumis sativus L NC_007144 Plader et al., 2007 Fabales Fabaceae Medicago truncatula NC_003119 Matsushima et al., 2008 Gaertn. Malpighiales Salicaceae Populus alba L NC_008235 Okumura et al., 2007 Vitales Vitaceae Vitis vinifera L. NC 007957 Jansen Caryophyllales Amaranthaceae Spinacia oleracea L. NC_002202 Sklinibi-Linseweler et Gentianales Rubiaceae Coffea arabica L. NC 008535 ^ Samson et al., 2007 Asterales Asteraceae Helianthus annuus L. NC. 007977 Jansen et al., 2007 Apiales Apiaceae Anethum graveolens L. EU016721- Jansen et al., 2007 al: EU016801 tia, d Araliaceae Panax ginseng C. A. Mey. NC | Kim & Lee, 2004 corales A Acorus americanus (Raf.) 7- Leebens-Mack et al., Raf. DQ069702, 2005 EU0167701- - EUO16 Alismatales Araceae Acorus calamus L. NC_007407 Goremykin et al., 2005 : Lemna minor L. NC 010109 Mardanov et al., 2008 Dioscoreales Dioscoreaceae — Dioscorea e Hansen et al., 2007 d (L'Hér.) Engl. Lee Pandanaceae P. utilis this study* Zomlefer 2348 (GA) es Liliaceae Lilium superbum L. this study* Giunish UW-8-2009-1 U : S Asparagales Amaryllidaceae Agapanthus praecox Willd. this study* e 2311 (GA) Asparagaceae — Albuca kirkii (Baker) this study* —— MeKain 111 (GA) Brenan Asparagus officinalis L. — (his study* — Jeebens-Mack 1001- . Volume 97, Number 4 | 2010 Plastome Sequence Phylogeny of Poales | APPENDIX l. Continued. GenBank accession Order Family Species numbers* Voucher data* Chlorophytum this study* McKain 110 (GA) rhizopendulum Bjorá & Hemp Hesperaloe parvi; this study* McKain 102 (GA) (Torr.) J. M. Coult. Hosta ventricosa (Salisb.) this study* McKain 106 (GA) Lomandra longifolia this study* Steele 1087 (UMO) Nolina atopocarpa this study* McKain 114 (GÀ) Yucca schidigera DQ069337- ^ Leebens-Mack et al., Ortgies 2005 EU016681- EU016700 Asteliaceae Neoastelia spectabilis this study* Bruhl 2767, Quinn J. B. Williams 95289 (NE) Hypoxidaceae — Curculigo capitulata this study* Steele 1081 (UMO) (Lour.) Kuntze Iridaceae Iris virginica L. this study* Pires 2009-101 (UMO) Orchidaceae Apostasia wallichii R. Br. this study* Zich 634; CNS130807 (CNS) Phalaenopsis aphrodite NC 007499 Chang et al., 2006 Rchb. f. Xanthorrhoeaceae Phormium tenax this study* Givnish Tas-2009-5 J. R. Forst. & G. Forst. (WIS) Arecales Arecaceae Chamaedorea seifrizii this study* Zomlefer 2358 (GA) Burret Elaeis oleifera (Kunth) EU016883- Leebens-Mack et al., Cortés EU016962 Ravenea hi this study* Zomlefer 2357 (GA) C. D. Bouché Dasypogonales Dasypogonaceae Dasypogon this study* KRT3702 (PERTH) bromeliiforlius R. Br. Kingia australis R. Br. this study — KRT3703 (PERTH) Commelinales Commelinaceae Belosynapsis ciliata this study* Winters, Higgins & “ (Blume) R. S. Rao Higgins 186, pl 2. 1982-232 (SI) Tradescantia ohiensis Raf. this study* Moore 337 (FLA) ingi acuminata Colla EUO16983- ^ Leebens-Mack et al Zingiberales Musaceae Musa EU017063 2005 Zingiberaceae — Renealmia alpina (Rotb.) this study" Zomlefer 2322 (GA) Maas i. Givnish 2 Poales Bromeliaceae Brocchinia micrantha this study* E Fosterella Rauh this study* Rauh 40573A (SEL) Navia saxicola L. B. Sm. _ this study* Givnish 3/16/1987 carolinas (Boer) this study? McKain 112 (CA) Sm. ‘Argentea’ Chev.) Harms & Mildbr. (SEL) i Se this study* Leebens-Mack 1003- Puya lra L P 2010 (GA) 612 Annals of the Missouri Botanical Garden APPENDIX l. Continued. | en ; accession Major clade Order Family Species numbers* Voucher data‘ Centrolepidaceae Centrolepis monogyna this study* — McKain 116 (GA) | Cyperaceae Cyperus alternifolius L. this study* —— Leebens-Mack 1002- | 0 (GA) | Ecdeiocoleaceae Ecdeiocolea monostachya F. this study* — KRT3786 (PERTH) | Mue | Georgeantha hexandra B. G. this study* — KRT3775 (PERTH) | Briggs & L. A. S. Johnson | Eriocaulaceae — Syngonanthus chrysanth this study* — M. Ames 10/15/2009 | Ruhland i ariac Flagellaria indica L. this study* — K. Hansen 77-394 (BH) I Joinvilleaceae Joinvillea ascendens this study* Lorence 9066 (NTBG), u Gaudich. ex Brongn. & 800379 (NTBG) Joni “peq (Hook.f) FJ486219- Leseberg € Duvall, | Newell & B. C. Stone FJ486269 2009 | Juncaceae Juncus diei this study* McKain 113 (GA) | Mayacaceae Mayaca fluviatilis Aubl. this study* — McKain 118 es) | Poaceae Agrostis stolonifera L. NC 008591 Saski et al., 200 | Anomochloa marantoidea NC_014062 Morris & Duvall, M | rongn. Bambusa oldhamii Munro NC 012927 Wu et al., 2009 | Eleusine coracana (L.) this study* — Leebens-Mack 1003- | aertn. 2010 (GA) | Hordeum DAN L. NC_008590 i et | Oryza sati NC 001320 Hiratsuka et al., 1989 Puelia lá (Franch.) Clayton 1060 (MO) | Clayton | Saccharum officinarum L. NC 006084 Asano et al., 2004 I Sorghum bicolor (L.) Moench NC. 00860 ki 2007 | Streptochaeta angustifolia this study* J. I. Davis 757 (BH) | en | Triticum aestivum L. NC 002762 Ogihara et al., 2002 x Zea mays L. NC 001666 Maier et al., 1995 Rapateaceae Potarophytum riparium this study* Givnish GUY-09-2 ith (BRG) | Restionaceae insignis this study* Givnish UW-8-2009-3 | Mast. , Sparganiaceae —— eurycarpum this study* Ames 10/21/2009 (WIS) f ngelm. | Thumiaceae Thurnia sphaerocephala “this study* — Cimish GUY-09-5 | ook. f. (BRG) i Typhaceae Typha latifolia L. NC 013823 Guisinger et al., 2010 Xyridaceae bolboda macrostachya this study* Givnish GUY-09-7 Spruce ex Malme (BRG) ] 1 1 x 1 | 1 3 E H3 1 * GenBank accession numbers for listing individual accession number for ous ise ouches specimen elsewhere). te án newly sequenced in this study are HQ180399-HQ183709. A spreadsheet h region species is available at , and noches Conert appear not be ored by fire among E e divergent lineages. implying i Frese pt condition so ancestr: una iaia ittm, nidis, fenum sites on extremely infertile soils in southwest (Linder et al., luk Lade & Red. 05. Men Fri 1 y QUI L. > ks Ë and inundated microsi the molecular ony of Linder et al. (2003), wel to one Australian clade (consisting of Sporadanthus F. Calorophus Muell. ex J. Buch., Labill. poire Br), 5 oni ies when Winifredia L. Johnson & B. G. Briggs, Ws rode n dta de Cox ides SM. co a S e i pr oan their oe, ira € Australian T— al now Sporadanthoideae) and by early divergent n ña e urychorde B. G. Briggs & L. A. S. Johnson, Empodisma, Wi , Taraxis B. G. Briggs | LAS Jinan) the nod Anan clade (v Leptocarpoideae). ons sparsely vegetated = in eren vet or rmanently microsites, near sea level s wet cut turfs (Pignatti s Maite 1994, 2005; Cooke, 1998, es Section, Such sites 2009), are very = to pues folis (Linder & Rudall, 2005). Mayaca grows y, dao ites on | eiui ‘ake 1900) di generally immune to fire (Linder & Rudall, the phylogenies ed by Si et al. 200, [ome and Višek an and Muasya et al. (2009 to infe hab funde t gr art onset aera he eceupancy of such site () by bol pro ce ceed (0 iv hasa piña Lk. J. Jacq., subcongesta (Š. Watson) Jeps., L piperi (Coville) M. E. Jones, J. potaninii Buc Buchenau, J. oxyearpus E » Mey. ex Kunth J. stygius L., and other taxa sister to all remaining or of the indi eii a O pias Cala 614 Annals of the Missouri Botanical Garden Table A1. appendix or data sources Habitat characteristics assigned to Poalean ingroups and outgroups for character-state reconstruction. See Light availability* Moisture supply! Nutrient supply: Fire prevalence? Poaceae, PACCMAD-BEP clade P. lioideae oaceae, Pharoideae Poaceae, Anomochlooideae Ecdeiocoleaceae Joinvilleaceae š ; e *0- DM habitats; 1 — sunny habitats. t 0 = Well-drained microsites; 1 = seasonall :0- Ee sands or peats; 1 = fertile substra: * 0 — Fires ancestral given their occurrence in mapanioids and the icrodraco Coleoc ides-Trilepis clade. Well-drained substrates and lack of fire are also in Juncaceae, given their occurrence in J. Jacq. J. trifidus L. and in est divergent rush li ymorphic, given extremely infertile substrates (ie., near lack of soil) in J. monanthos and J. richer soils in Luzula and Juncus uncus L. subg. Juncus (Table Al), All habitats inhabited by Rapateaceae are exceedingly infertile, and almost ye are => (except for those occupied by Epidryos Maguire, Aubl., and Windsorina Ca a wet to a wisa asi (save those occupied by Epidryos and Rapatea), and ema (but for those occupied by Epidryos, hogy teas R possibly the unstudied um O: y al. (2004), — wet, amas and M infertile - are din ancestral for Rapateaceae Typha L. occhinia and the current multilocus phylogeny for that pes (see Givnish et al. 1997, L £ -.eg oooocco past HMOrorocooocosco - O O m m m Om eoS$coowee ee Se Oror co C R C O Cp L = C C OO O CC OO D KF OR RF ee e — og emet inundated. rare/absent; 1 = fires frequent relative to € of plant regrowth. occur in both fireswept habitats (es L. guianensis) and that appear to burn rarely if at all (e. 8 L. arachnoidea (L. B. Sm., Steyerm. & H. Rob.) L B. members of the third divergent subfamily Tillandsioideae (Givnish et al., in prep.) rarely experience fi fire Among the soak beak £4 h were scored as as open, wet, nutrient poor, and fire based on the sharing of these characteristics by Hanguana Blume, Cila R. Br., Philydrella Caruel, and Anigo- zanthos Labill./Xiphidium Aubl. and on the phylogeny of Saarela et al. (2008). By comparison, the ancestral habi these environ- ments being shared by present-day Lowiaceae, Heliconia L./ Musa L. and the “ginger” families (Cannaceae, Marantaceae, Costaceae, Zingiberaceae), and on the valiai of em families to each other and Strelitziaceae in the multiloc and neither extremely infertile nor fireswept, based a, (2008) and the sharing of such habitats today by most calamoids and coryphoids. Exceptions to these rules are numerous; for — in the predominantly — dwell C w qi ies), Ma AIC IOT fire frequency (Table A given that several early divergent &£ B. prismatica, B. melanacra) jen. while members of of Lindmania LE d related seasonally d dr Finally, ancestral habitats for were scored as shaded, well drained, moder- T Volume 97, Number 4 Givnish et al. 615 2010 Plastome Sequence Phylogeny of Poales | | E : I : Table A2. Habitat and floral characteristics of taxa included in tests of correlated evolution. See text for data sources. Wind pollina- Habitat Ovules Flowers Flowers Flow tion open Dioecy Nectar multiple unisexual large e assk. es oor oo SY * Ecdeiocolea F. Muell. | Elaeis Jacq. Eleusine Gaertn. Flagellaria L. Fosterella L. B. Sm. Georgeantha B. G. Briggs & L. A. S. Johnson L um L. Joinvillea-1 Gaudich. ex Brongn. & Gris Joinvillea-2 Juncus L Kingia R.B Mayaca Aubl. Musa L. Navia Schult. f. Neoastelia J. E In Neoregel, elia L. Oryz L. Ea Blume Pitcairnia L'Hér. P otarophytum Sandwith uelia Franch i i i 1 | Sorghum Mocuch Sparganium L. Streptochaeta Schrad. ex Nees Syngonanthus Ruhlan mnochortus D000-00» 00000059 = = O m mw — = = = G G C€ C oo ee O oer oe oor KH C = Ç ° = cocorwocoorwr coe e oer O m O m m m O w = m = ewe OS ee oem = S S @ —= OM eo eH eH oe @ @ = 1i Ro — — — — — @— = — —@ — @— — Ç Ç Ç Ç — @ — — @ = — — a e — — — — — == O — — — — — — — = = oM = — — — Ç =< Ç @ @ @ C — —@— —@ —@ Ó O O A = — — = = = — — O M M M CD o M OOM rR = Ç Ç C i CY C Cor oo eee OF OOF OO? = C == OO OO = O Y CO > C OO = ° eer ocr — = — —— —-K— > — —— — — —2b XK — — — — à — — — — — — — 22 — — = — — — — — — ZG — @ GO C CO CO CC i O O T C o O O mo O m m m m Om COC OO mK OC OF OOF Or oe CO CC O = @ @ O = = 00000» 05910 O om O m m m m — = — G C C O = O CC CoCo oC O = OOO A oo O Om Zea L, loff et al. (2010) argue instead that the a traditional interpretation is that centrolepid ue are unisexual, but Sokol ence" is a highly reduced hermaphroditic flow: : Lex.. C. rochilum Franch., C. ately fertile, and unlikely to burn, based on the sharing of irapeanum ken & m plect E s i oi a Pio s in present-day habitats of veloci logenies for the family (Cox et al. p e Hs pre ay ero -— sie mx th < mi £ of Apostasioideae, "d some early divergent Cypripedium L. (Les C 616 Annals of the Missouri Botanical Garden CORRELATED EVOLUTION BETWEEN WIND POLLINATION AND Various Pant Trarts We conducted tests for pattems. of correlated evolution of floral sexuality, sexual system, vule number, floral size, and plast plumose Pen Gens Heslop Harison & aak, ok ination. Linder (1987) udall (2005) considered Flagellaria and genera lack a stigmas (Soreng y" rule 1998). white flowers s (aska, 1951), and e visi Joinvillea Towers (Newell, 1969) * while the plant (Blüthgen & Fiedler, 2004; Blüthgen et al, 2004a, b) Anomochloa, St well as several possessing simple stigm: pollen with sculpture e 2 ie typical ^t iad pollinated grasses & Calderón, 1971, 1979; Soderstrom, 1981; Soreng & pal 1998). As a Conseryatiye measure, Puelia Franch. was scored as wind pollinated, S A r 2 £ E = (Cc EDS Loon Working Group I, 2001). Nothing is known about the pollination biology of Puelia and its sister Guaduella Franch., of several of our tests for correlated evolution involving wind Ponien wak i increase. from individual generi (Table A» to familiesorders is For Eriocaulac aceae, few rigorous studies on the s of pollination have been conducted; those that have (i.e., Stützel, Rosa & Scatena, 2003, 2007; Ramos et al., 2005; Oriani . 2009) have identified biotic pollination as being oir Thus, even though many previous authors Es Eriocaulaceae as de wind pollinated, we score the family as animal pollinated. For palms, iti is clear that the nsect pollinated Given their diss position in the current molecular phylogeny (Baker et al., 2009), we conclude that animal lino is the ancestral condition for the palm family. EVOLUTIONARY HISTORY OF THE MONOCOT FLOWER' Margarita V. Remizowa,? Dmitry D. Sokoloff.? and P. J. Rudall ABSTRACT This pa paper Dee monocot flower siructuse and gynoecium development and evaluates these data to clarify the history delimitation and d psa etic relationship TY gardi the suites that eco the septal nectaries. It is likely that the trimerous y Is virtually absent from th _ res of monocot en lites, and (2) a radians in ipee to A ocot enin nen a "a degree of aliia in monocot floral evolution. om a on two as 0 the typical. monocot groundplan of trimerous-pentacyelic o F de 1 kL £ " ts; thi n y rd + "a k aL £ groundplan i phylogenet etic group is analogous with the absence z = ya eudicot flower groundplan i in basal eudicots, though i in both es the underlying constraints are mio: re. lead us to favor a hypothesis that the anc septal ( m pleural) nectaries. which suggest that the ancestral mo k A í o This Aaa optimization contrasts with optimizations inl morphological nocot flower possessed congenitally united "A srg no contribution of peel homme] lacked septal nectaries. Among extant early divergent arpe ae, Arecaceae, ad with several gai that iui Bec-camellate species s ow significa e" ords: Apocarpy, congenital fusion, flower evolution, monocoty esc aii Petrosaviales) appear to most closely resemble those of the ated monocots. A a derived condition i in ns of apocarp y in Alismatales and palms. All three monocot groupe nt variation in their individual fl ledon, postgenital fusion, septal nectary, syncarpy, Monocots form a well-supported clade that encom- Passes a considerable portion of angiosperm diversity. Although no single morphological character can be used to distinguish monocots from other angiosperms, they are morphologically well defined by a combina- tion of characters, including the possession of trimerous-pentacyelic flowers. Most authors (e.g.. Dahlgren et al., 1985; Takhtajan, 1987; Cronquist, 1988) have accepted monocots as a monophyletic unit derived from within a group of early divergent angiosperms (subclass Magnoliidae; sensu Takhtajan, 1987). This view is confirmed by molecular phyloge- netic data (summarized in Angiosperm Phylogeny Group III, 2009). More detailed hypotheses, such as a *ister-group relationship between monocots and e Nymphaeales (e.g., Schaffner, 1904; Hallier, 1905; Takhtajan, 1980, or Piperales and Chloranthaceae (see Burger, 1977; Dahlgren et al., ` We are grateful to Vladimir Choob, Sean Graham, 1985). are not supported by recent molecular analyses. Thus, in contrast with many other plant groups, monocot boundaries have survived the aec revolution in phylogenetics almost intact. The only exception is Hydatellaceae, a small family of tiny aquatics with highly modified reproductive structures. Although previously thought to be mono- cots of uncertain affinity (Hamann, 1976; Dahlgren et ll were based Hydatellaceae nd mum wi of mi and Sabine von Mering for discnssio® and Harperocalis (which m for a cpi reviews. Lisa Campbell and Dennis Stevenson provided ided material of Triglochin, and the subject of a forthcoming collaborative paper). Alexei as ee material of Tofieldia. M.V.R. and D.D.S. acknow 4, Russian Foundation for ee Research (RFBR) grant no. State University, Moscow 119991, Russia. remizowa@yahoo.com, “tea (FCP “Kadry”, NK-54111/P314) “koloff-v@yandex w oí Higher Plants, Faculty of Biology, Moscow rel Laboratory, Royal Botanic Gardens, Kew, Richmond, Surrey, T “org. - tei: 10.3417/2000142 ek and Ministry of Education and Sc 3AB, United Kingdom. Author for correspondence: 645. PUBLISHED 2010. ANN. Missourt Bor. Garb. 97: 617-040 "m m E Annals of the Missouri Botanical Garden and Hydatellaceae. Indeed, detailed descriptions of the waterlily female gametophyte, which closely les that of Hydatellaceae (Friedman, 2008; Rudall et al, 2008), were published relatively monoc plastids in Hydatellaceae is not supported in a new investigation (Tratt et al., 2009). owever, despite some congruence between molec- ular and morphological data on the delimitation and phylogenetic relationships of monocots, their floral evolution remains poorly understood. There is currently no universally accepted view on the morphology of the ancestral monocot flower, reflecting a high degree of parallelism in monocot floral evolution. Significant progress has been achieved in monocot phylogenetics since the first international monocot meeting in 1993, which included a timely and comprehensive review of monocot flowers (Endress, 1995). There are now considerable new data on flower structure and development in key groups, especially among early divergent monocots. In this paper, we review and evaluate th dads d Iw. ua É at ta lary history of the monocot flower and present a new model for floral evolution. We focus on two character suites that encompass the key features of monocot flowers: (1) the typical groundplan of trimerous-pentacyclic flow- ers, and (2) a character suite related to carpel fusion, including postgenital fusion between carpels and the presence of septal nectaries, We broadly follow the Angiosperm Phylogeny Group classifications (e.g., Angiosperm Phylogeny Group III, 2009), which recognize 11 or 12 monocot orders, based primarily, on molecular phylogenetic data (e.g., Davis et al., 2004; Chase et al, 2006; Graham et al, 2006). Specifically, the monocots consist of three informal groupings: (1) a grade of two early divergent lineages consisting of Acorales (Acoraceae, with the single genus Acorus L., which is sister to all other monocots) and Alismatales (Araceae, Tofieldiaceae, and 11 families of former Helobieae, here termed as the core alismatids); (2) a grade of five lilioid orders including Petrosaviales (two genera in a single family), Dioscoreales (three families), Pandanales (five families), Liliales (10 families). and Asparagales (14 families), with Dios- coreales and Pandanales pairing as sister to one another; (3) a clade of five commelinid consisting of Arecales (the palm family), Commeli- nales (five families). Dasypogonales (four genera ina single family, sometimes unplaced to order), Poales (16 families), and Zingiberales (eight families), with linales and Zingerales Pairing as sister to one r. to Ciarliy anothe TRIMEROUS-PENTACYCLIC FLOWERS The typical monocot groundplan consists of six tepals in two alternating whorls (generally not differentiated into petals and sepals), six stamens in two alternating whorls, and three c ls (ie., trimerous-pentacyclic flowers). Sectorial differentia- tion in monocot flowers was discussed in detail by Endress (1995), who noted that this arrangement is more readily achievable in trimerous than in pentam- erous flowers because the sectors are broader. In many monocots, tepals and stamens inserted on the same radii are intimately linked with each other by (1) initiation as a common tepal-stamen primordium, (2) basal congenital fusion of a tepal and a stamen, (3) insertion of inner tepal-stamen complexes above the outer tepal-stamen complexes, thus affecting precise whorl alternation, or (4) functional synorganization within a tepal-stamen complex. Endress (1995) highlighted the lack of a clear correlation between the presence or absence of common primordia and the occurrence of tepal-stamen fusion in monocots. He found that both features are homoplastic within large monocot clades and in monocots in general. In the following review, we consider only the number and position of organs, not their shape, functional elaboration, or synorganization. A trimer- ous-pentacyclic groundplan occurs in some members of all monocot orders, but with variable frequency. The widespread occurrence of trimerous-pentacyclic flowers in monocots contrasts with their virtual nce from early divergent angiosperms, magno- liids, and non-core eudicots. However, trimery itself is common among these groups, though rare in core eudicots (e.g., Kubitzki, 1987; Endress, 1996). For A typical monocot flowers (six tepals, six stamens, three carpels), but all six stamens belong to the same whorl (e.g., Tucker & Douglas, 1996; Endress, 2001; Rudall et al, 2009) Flowers of the magnoliid Orophea corymbosa (Blume) Miq. (Annonaceae, Magnoliales) possess three sepals, 3 + 3 petals, 3 + 3 stamens, and three carpels (e.g., Buchheim, 1964), and differ from typical monocot flowers only in the presence of an extra perianth whorl. Some other Annonaceae possess a perianth of only three sepals and three petals (e.g-, Dennettia Baker f.), but in all of these cases, stamens and carpels are numerous (see Kessler, 1993)- Flowers of the magnoliid Lactoris Phil. (Lactoridaceae, Piperales) possess three (rather than 3 + 3) tepals, 3 + 3 stamens, and three carpels (Tucker & Douglas, 1996). Some non-core eudicots, such as Menisperma- ceae and Lardizabalaceae (Ranunculales) have 3 * 3 sepals, 3 + 3 petals, 3 + 3 stamens, and three or 3 + 3 adis a a A qusqa s E IUE LR RR up qar asas sy. ; Volume 97, Number 4 2010 Remizowa et al. 619 Evolutionary History of the Monocot Flower carpels (e.g. Takhtajan, 2009). There are a few examples of trimerous-pentacyclic flowers among the early divergent core eudicots (see also Endress, 1996). For example, flowers of Pterostegia Fisch. & C. A. Mey. (Polygonaceae, Caryophyllales) and Trihaloragis M. L. Moody & Les (Haloragaceae, Saxifragales) are trimerous and pentacyclic (e.g., Yurtseva & Choob, 2005; Moody & Les Because the erintercaspentaó la flower is so common in monocots, this review focuses on the exceptions. This presentation mode inevitably implies that the trimerous-pentacyclic flower represents the ancestral condition, but this implication will be discussed later. Note that this implication is not universally accepted (reviewed by Ronse de Craene & Smets, 1995). There are three different types of deviation from the typical trimerous-pentacyclic flower arrangement in monocots. (1) Reduction of some organs can occur without altering the positions of the remaining organs. This type is often associated with synorganization of floral organs (e.g., orchids, gingers, irises). Examples of this type are scattered across the monocot phylogenetic tree. (2) Changes can occur in flower merism, while retaining a pentacyclic isomerous construction (i.e., occurrence of the same number of organs in all whorls of a given flower). This type is surprisingly rare, and there is no obvious pattern in its distribution in monocots. For example, increased merism occurs in Paris L. (Trilliaceae, Liliales) and decreased merism occurs in dimerous flowers in Maianthemum F. H. Wigg. (Aspagaraceae, Asparagales). (3) Finally, significant changes can occur in the groundplan, with insertion of new whorl(s) (as in the gynoecium of Sagittaria L., Alismataceae, Alismatales), complete loss of whorl(s) affecting the Positions of other organs (as in Trillium apetalon Makino, Trilliaceae, Liliales; see below), and/or loss isomery due to multiplication of some organs (e-g- in Pleea tenuifolia Michx., Tofieldiaceae, Alismatales, with six stamens in the outer whorl of the androecium, all other floral whorls being trimerous). Significant groundplan changes are unequally distributed in monocots; they are common in Alismatales, Panda- nales, and palms and are also present in a few Scattered and species-poor groups of Liliales, some , and Poales LY DIVERGENT MONOCOTS Both species of Acorus (Acoraceae) possess trimer- oe flowers, with occasional exceptions in the most distal region of the i clic groundplan is remarkably rare i in Alismatales. In most Araceae, flowers are highly modified by changes in merism, loss of perianth, and/ or unisexuality, although a trimerous-pentacyclic Spathiphylleae (Mayo et al., 1997). However, even here, merism of the varies between two and pe cag Hotta), and the gynoecium can be monomerous or (Pothoi- dium Schott) (Mayo et al, 1997; Buzgo, 2001). Furthermore, in the few aroids with trimerous- pentacyclic flowers, the median outer tepal is adaxial rather than abaxial, and flower orientation with respect to the primary inflorescence axis is upside down — with most other monocots, including Acorus (Buzgo, 2001). In the alismatid family Tofieldiaceae, flowers are trimerous and pentacyclic IL in Pleea = with increased stamen number), bu t they additional trimerous whorl of phyllomes dcn outside (and alternating with) the outer-whorl tepals. The calyculus resembles a third perianth whorl (Remizowa & Sokoloff, 2003; Remizowa et al., 2006a). Among the core alismatids, flowers are often trimerous and pentacyclic in the monospecific family Scheuchzeriaceae , 1983), but even here akhtajan, 2009; see ingh 1972, 1977; Posluszny & Sattler, 1974a, b; Posluszny & Tomlinson, 1977; Posluszny et al., 1986). for example, to Flower merism can be decreased, A two organs per whorl in Ruppia L. (Rupp: uppiaceae) or one in Triglochin scilloides (Poir.) Mering & i ) or š if w Kae Duet eues L Poanogs inii as t though the perianth and etramerous, can also be interpreted as dimerous flowers also occur within the range of variation in Triglochin L. species) Annals of the Missouri Botanical Garden 2. There can be loss of isomery between floral whorls. For example, in Potamogeton (Potamoge- tonaceae), tepals and stamens can be interpreted as occurring in dimerous whorls, but the carpels are unquestionably in a tetramerous whorl. In Alisma L., the perianth is trimerous, there are six stamens in a single whorl, and the carpel whorl is polymerous, triangular, and with sequential carpel initiation starting with three initial carpels. In many species of Aponogeton L. f., there are two tepals, 3 + 3 stamens, and three carpels. There can be an increase or decrease in the number " floral whorls. For example, there is a single perianth whorl in Althenia Petit (Zanni- chelliaceae, but united with Potamogetonaceae in Angiosperm Phylogeny Group III, 2009) and Thalassia Banks ex K. D. Koenig (Hydro- charitaceae), multiple stamen whorls in many Hydrocharitaceae and Limnocharitaceae (united _ with Alismataceae in Angiosperm Phylogeny Group HI, 2009), a single stamen whorl in Alisma and Ruppia, and more than one carpel whorl in Ruppia, Sagittaria (Alismataceae), and Triglochin. Flowers can be unisexual (e.g., Thalassia, Cymo- doceaceae, Zannichelliaceae). A synandrium can be present, with loss of stamen individuality (e.g., Lepilaena J. Drumm. ex Harv. and some Zannichellia L. and Cymodoceaceae). P > e Figure 1 shows some variants of the flower groundplan in Aponogeton. Although Aponogeton pent possesses two tepals, six stamens, and three arpels, variation occurs in the number of organs of I category, illustrating the instability of the flower groundplan in the core alismatids. LILIOID MONOCOTS Trimerous-pentacyclic flowers are common and probably plesiomorphic in at least four of the lilioid orders, although considerable variation occurs in the small but highly diverse order Pandanales. Petrosa- viales represent a taxonomically isolated and species- poor lineage of two genera, Japonolirion Nakai and Prises Bere. tamem et al. m .. mpo in MEN ni^ hat Takhtajan (2009) and s zowa (in press) accepted two disti t monogeneric families. Flowers peas gn Petrosavia are normally trimerous and pentacyclic, although there have been occasional records of a bicarpellate gynoecium in Japonolirion (Remizowa et al., 2006b). Iu Pandensles, Joss af ilie pie ical monconi flower e F ALCS eo g t TEPSPORE OI the inflorescence-flower boundary is often problem- atic (Rudall, 2003, 2008; Rudall & Bateman, 2006). For example, if the female reproductive units of Sararanga Hemsl. (Pandanaceae) are interpreted as flowers, they possess up to 80 carpels united to form a unilocular ovary, and the receptacle is folded in several places, so that carpels are ar along a zigzag line. A similar carpel arrangement, with dorsiventral planes of carpels ise rotated through 90* toward the center of the flow in Zacandonia E. Martínez & Ramos, Triuris Miers, and Peltophyllum Gardner (Triuridaceae), recalling a comparable pattern of carpel arrangement on a e receptacle in an asterid eudicot, Tupidanthus & Thomson, in the family Araliaceae vs 1901; Sokoloff et al., 2007). Unisexual flowers occur in most Cyclanthaceae, Pandanaceae, and Triuridaceae, and organ numbers are frequently atypical for monocots in these families. The pattern of gender distribution on the inflorescence is highly unusual in Cyclanthaceae, either with each female flower surrounded by four male flowers (in subfamily Carludovicoideae) or with female and male flowers united in rings (in Cyclanthoideae), with a resulting loss of flower individuality (Goebel, 1931 1958). In the remarkable, inside-out bisexual repro- ductive units of Lacandonia (Triuridaceae), the carpels are inserted outside the stamens, and the dorsiventral carpel orientation is inverted with respect to carpel position in phylogenetically related taxa (Ambrose et al., 2006; Rudall, 2008). Flowers are at least superficially closer to the typical monocot structure in Stemonaceae and Velloziaceae. However, in Stemonaceae the perianth and an ium are either dimerous or pentamerous, and the gynoecium is either monomerous or trimerous (Rudall et al., 2005). Within Velloziaceae, some species possess a corona of six petaloid appendages, and others show increased stamen number (Menezes & Semir, 1990; Mello-Silva, 1995; Sajo et al., 2010). The remaining lilioid orders are relatively conser- vative in their floral groundplan. In Dioscore deviations such as loss of one of two perianth sri and loss of one of two stamen whorls can largely be explained by reduction. In Liliales, most of the interesting deviations from trimerous-pentacyclic flowers are found in Smilacaceae and Trilliaceae (ca. three genera that are placed within Melanthiaceae in Angiosperm Phylogeny Group III, 2009). The flowers of a few Smilacaceae possess three to 15 stamens (Takhtajan, 2009) or up to 18 stamens (Dahlgren et al., 1985) in trimerous whorls. In Trilliaceae, a highly stable organization of the vegetative shoots and highly conservative pattern of flower arrangement are associated with exceptional aetan aia le Volume 97, Number 4 Flo Ower with single iul rn that ach Remizowa et al. pean History of the Monocot Flower f si s) with a M t. Cene ae, Alismatales + A í ef t stachyus L. f. — —A. “lower with tw ved. ynoec Flowers of iponogeton R ponogeton Gk T ve been remov rpels some stamen & Thonn. Flower with two tepals, stamens, and three carpe" ‘ponogeton subc 'onjugatus nnii whorl stamen: t. S = an with two united tep Scale bars = 250 um. Annals of the Missouri Botanical Garden lability in the number and arrangement of flower parts. Flowers of Trilliaceae are solitary and terminal on lateral shoots, and an involucral whorl of foliage leaves is present below each flower (e.g., Dahlgren et al., 1985; Zomlefer, 1996; Takhtajan, 2009). Merism of the involucral whorl is often the same as in the flower; the outer-whorl tepals alternate with the involucral leaves. In species of Trillium L. that lack a pedicel, the involucre positionally resembles a third perianth whorl. In some other species, the inner perianth members are absent, either due to suppres- sion (Paris tetraphylla A. Gray, P. incompleta M. Bieb.) or loss (T. apetalon) (Takahashi, 1994; Remizowa et al, 2007a; Choob, 2008; Narita & Takahashi, 2008). In cases where the inner tepals (petals) are entirely lost (T. apetalon), the carpels and outer-whorl stamens develop on radii that alternate with the remaining tepals, so the orientation of the Within T. smallii s. str., there is infraspecific variation in petal number from one to three, or petals can be absent, in which case they are replaced by additional stamens, thus increasing the stamen number to nine (Chase & Chase, 1997). Within Paris s.l. (including Daiswa Raf. and Kinugasa Tatew. & Suto; see Ji et al., 2006), flower merism is typically increased (because Paris s.l. is monophyletic, the increased merism is a to three, four, five, or even six whorls. The species with increased stamen whorls (P. dunniana H. Lév., P. cronquistii (Takht.) H. Li, P. vietnamensis (Takht.) H. Li) formed a clade in the molecular phylogenetic analysis of Ji et al. (2006), whereas a group of Paris — with 2-whorled stamens was paraphyletic. e Asnaragal aay Idi AUS aL trimerous-pentacyclic groundplan, including the most species-rich family Orchidaceae, which is sister to all other Asparagales in most analyses (e.g., Givnish et al., 2006; Graham et al., 2006). Orchid flowers are clearly derived from trimerous-pentacyclic flowers, possibly by suppression or loss of three, four, and fiye stamens (from both whorls) in different orchid clades (Rudall & Bateman, 2002). Some other Asparagales such as Pauridia Harv. (Hypoxidaceae) and Iridaceae. lack one of the two stamen whorls, but the positions of the other organs, including the carpels, are the same as in more typical monocot flowers. À few are dimerous (e.g., M. Y» tetramerous (e.g., some Aspidistra Ker Gawl., Aspar- agaceae), or even pentamerous to heptamerous (Neoastelia J. B. Williams, Asteliaceae; Takhtajan, 2009). Different patterns of polyandry have evolved at least three times in Asparagales (Kocyan, 2007), including stamen fascicles in Gethyllis L. (Amarylli- daceae) and a single folded stamen whorl in Curculigo racemosa Ridl. (Hypoxidaceae) (Dahlgren et al., 1985; Kocyan, 2007). In A. dodecandra (Gagnep.) Tillich, stamen number is twice the number of the perian lobes (Tillich, 2005). Flowers of A. locii Arnautov & Bogner superficially resemble the inflorescences of the eudicot Ficus L. (Moraceae); all tepals are united to form a chamber up to 3 cm long, with a narrow opening (to 2 mm diam.), and there are 12 to 14 stamens and apparently four carpels (Bogner & Arnautov, 2004). Some Amaryllidaceae, including arcissus L., possess a floral corona that is morpho- logically similar to the corona in Velloziaceae (Pandanales). In general, significant deviations from typical monocot flower groundplan (except losses of some stamens) are extremely rare in As es COMMELINID MONOCOTS Considerable floral diversity exists among the commelinid monocots, but it seems likely that trimerous-pentacyclic flowers are plesiomorphic for each of the four (or three) commelinid lineages, Arecales (palms), the sister-orders Commelinales and Zingiberales, Poales, and Dasypogonaceae (a small family of unclear affinity that is sister to Poales in some analyses, e.g., Chase et al., 2006; see also Rudall, in press). Dasypogonaceae possess trimerous- pentacyclic flowers, although these are sometimes functionally unisexual. Secondary modifications in the Drak eage that includes the orders Comm linales and Zingiberales include losses of some organs, especially in the androecium, but apparently no organ increase. The large order Poales encompasses a grade of three families (Bromeliaceae, Rapateaceae, Typhaceae) and four other clades, informally termed “graminids, restiids, cyperids, and xyrids” (Linder & Rudall, 2005). Many Poales are characterized by abiotic (usually wind) pollination (graminids, restiids, cyperids, and Typhaceae), although some members of these clades are biotically pollinated. There could have been several shifts to wind pollination in Poales, often associated with reductions in carpel and ovule number (Linder, 1998; Linder & Rudall, 2005). Flowers are trimerous-pentacyclic in most bioti- cally pollinated Poales (e.g., Bromeliaceae, Rapatea- ceae), or floral variation can be readily explained by ion or loss of organs from ancestral trimerous- pentacyclic flowers (e.g., Eriocaulaceae, Xyridaceae). MAMMA LO d E E Volume 97, Number 4 2010 Remizowa et al. 623 Evolutionary History of the Monocot Flower Hamann (1964) reproduced a floral diagram of Rapatea paludosa Aubl. (Rapateaceae) in which the carpels are on the same radii as the inner-whorl tepals and inner-whorl stamens, an arrangement that is fundamentally different from that of other monocots. rvations on another member of Rapateaceae, phalostemon R. H. Schomb. sp. (P. J. Rudall & M. G. Sajo, unpublished), show regular alternation of whorls. More comparative data on flowers of Rapa- teaceae are needed to resolve this apparent variation. Similarly, flowers of Mayacaceae were reported to be trimerous-tetracyclic, with a single stamen whorl and all whorls regularly alternating so that the carpels occupy the sites where the inner stamen whorl would be expected (T. Stiitzel, pers. comm., cited in Dahlgren et al., 1985: 388). However, illustrations from a recent study by Carvalho et al. (2009) confirm earlier observations (e.g., Hamann, 1964) that carpels in Mayacaceae lie on the same radii as the outer-whorl tepals, as in other monocots with trimerous flowers. Most wind-pollinated (or self-pollinated) Poales show high diversity in floral groundplan, not always restricted to reductions of trimerous-pentacyclic flowers. Extant Typhaceae (including Sparganiaceae) have unisexual flowers with an unstable number of tepals, which are modified into hairlike structures in Typha L. (Müller-Doblies, 1970). Extant taxa possess from one to eight stamens and typically a single carpel, although teratologically up to three unit carpels can be found (Müller-Doblies, 1970; Dahlgren et al, 1985). Some Tertiary fossil Sparganium L. possessed up to 7-locular fruits (Dorofeev, 1979). Among the graminids and restiids, which are predominantly wind pollinated, flowers of several families (Anarthriaceae, Ecdeiocoleaceae, Flagellar- iaceae, Joinvilleaceae, Restionaceae) can be readily derived from trimerous-pentacyclic flowers by reduc- tion of certain organs (e.g., the outer stamen w in Restionaceae) and transitions from trimery to dimery. re has been considerable discussion regarding the morphological interpretation of the grass flower, but flowers of most grasses can be derived from trimerous- pentacyclic flowers by reduction. Stamen number is highly variable in grasses (Gramineae or Poaceae), sometimes even within a single genus; the most common numbers are three and two, but these can be interpreted as belonging to more than one whorl (Rudall & Bateman, 2004). Some oe stamens (Oryza L.), and stamen multiplication has occurred in a few grass genera (e.g-, 0c Thwaites, with up to 120 stamens). The uniovulate and unilocular grass ovary usually bears two, but some- times one, three, or even four stigmas (Philipson, 985). Highly unusual reproductive structures occur in Centrolepidaceae, a family closely related to Restionaceae. with its center of diversity in Australia. During recent decades, the uctive units of Centrolepidaceae have usually been understood as highly i grated p lama: p k p s pel late naked female flowers and unistaminate naked male flowers (e.g., Cooke, 1998; Takhtajan, ). However, + oo at (Sol LAT ot 1, 2009) supported a euanthial interpretation of these reproduc- tive structures. Fl f Centrol pi 1 I ty d to about 30 carpels. It is an open question whether phyllomes surrounding these flowers represent tepals or bracts. Multicarpellate gynoecia of is Labill. are unique among angiosperm gynoecia. Carpels are arranged in a single whorl, but one side of the gynoecium is uplifted due to strong, unequal receptacle growth, so that in anthetic flowers carpels appear to be inserted in two rows along a common stalk. Some Centrolepidaceae possess po- ymerous gynoecia (the highest carpel number in Poales), but some other members of the family (Aphelia R. Br.) have a truly monomerous gynoecium, with no evidence of : In the cyperid clade, flowers are trimerous- pentacyclic in Thurniaceae and most Juncaceae. The inner stamen whorl or inner tepal whorl is occasion- ally lacking in Juncaceae (Dahlgren et al., 1985), but (as in Mayacaceae) the absence of the inner stamen whorl d + affect I ] position at least in Juncus minutulus (Albert & Jahand.) Prain (D. Sokoloff, pers. obs). There is considerable flower diversity in Cyperaceae, which is currently subdivided into two subfamilies, Mapanioideae and Cyperoideae, that represent monophyletic sister groups (Simpson et al., 2003). Flowers of Cyperoideae could be derived from the trimerous-pentacyclic type, with floral reduction — i with a single central ovule. The e donis ied to be modified pde they can follow the 3 + 3 pattern (Vrijdaghs et al., ). In Carex L., which represents the most extreme case of reduction, flowers are unisexual and naked, with either two to three stamens (in male flowers) or two to three united carpels (in female flowers). In tricarpellate female flowers of Carex, carpel orientation appears to differ from the usual ~ condition in monocots (in which the median carpel is typically adaxial), if the bract subtending the utricle with enclosed gynoecium is interpreted as the flower- :ng bract. However, the utricle is actually the flower-subtending bract in Carex (reviewed in Alex- eev. 1996), and therefore the median carpel is abaxial, as in other monocots. 624 Annals of the Missouri Botanical Garden Not all flower diversity in Cyperaceae can be mecum For set Evandra R. Br. and up to six carpels (Déligin cal. gr Vrijdaghs (2006) listed six other Cyperoideae with more than six stamens; for example, Reedia spathacea F. Muell. has more than 20 stamens and eight stigmatic branches. Some cyperids possess more than six perianth parts. For example, five of the eight tepals in Dulichium arundinaceum (L.) Britton correspond with five of the six tepals in Scirpus L.; the nib. +L. + k. Y. Pus. p: E a dad s ak. site of the sixth, adaxial tepal of Scirpus (Vrijdaghs et "m is Eriophora L. aR tipak pèiniordis are perianth parts nia — in several whorls (Vrijdaghs et al., 2005 The reproductive art of Mapanioideae are often interpreted as highly specialized pseudanthia com- female flower (e.g., Dahlgren et al., 1985; Richards et al., 2006). In some Mapanioideae, sterile bracts inserted on the main axis above the male flowers surroun ile. — flower. An eios epre ut tis a Boc | in which the structures conunonly described are actually tepal homologues (e.g., Bentham, 1877; Halts. 1948; Goetghebeur, 1998). The main problem with the latter i interpretation is the presence of these putative tepals above the d of insertion of the outer stamens. However, an anal homology between the . units of eee deae and the structures that flowers in Cyperoideae (e.g., faka 1877; Sie 1948). Within this concept, if mapanioid reproductive units are pseudanthia, then e ise | eyperoid prefloral unils. a concept uo xu À, ° ; "- of our current understanding of diu ng of the phyl genetic placement of Cyperaceae. phylo- — the Palm order Arecales exhibits ides. z TUE MN nt, and initiation. sequence. Many palms have trimerous- pni flowers, although they are often function- ally or female, with pistillodes and staminodes, A nra (Dransfield et al, 2008). Some palm n" 1 £ 4d kel rs ‘A For example, in Nypa Steck (Arecaceae), female flowers have 3 + 3 tepals, no staminodes, and three carpels, and male flowers have 3 + 3 tepals, three stamens united in a synandrium, and no rudimentary gynoecium (Uhl, 1972). Some palms belonging to several unrelated groups possess polystaminate flowers with up to 950 stamens (Dransficld et al., Stamens in polymerous androecia are never arranged spirally but instead form several whorls or groups associated with the inner-whorl and outer-whorl tepals, or stamen arrangement is chaotic. Stamen development can be either centrifugal (e.g., phytelophantoid p or centripetal (e.g., Uhl & Dransfield, 1984). times carpel number is increased, although "d gynoecium is always single-whorle s are unusual among monocots in that there are strong differences between the inner and outer perianth whorls, so that they could be termed “sepals and petals.” In some palms, the inner and outer perianth whorls form Hiii sepal and petal tubes, and there is a tendency that only petals are associated with stamens (e.g., Dransfield et al., 2008; Stauffer et al., 2009). Perianth differentiation into sepals and petals is also pronounced in some other commelinids (e.g., Commelinaceae in Commelinales, Xyridaceae in Poales) and also in orchids. Stamen association with the petals occurs in some early divergent Poales (e.g., Bromeliaceae, Rapateaceae). CARPEL FUSION Carpels are fused in flowers of the majority of monocots, in contrast with early divergent (ANA grade, sometimes termed “ANITA grade") angio- sperms and magnoliids, in which gynoecia are predominantly free-carpellate (apocarpous). The pres- ence of fused carpels in Acorus (Fig. 3). the putative sister to all other monocots, and in other early divergent monocots has led some authors (e.g.. Doyle & Endress, 2000; Chen et al, 2004) to postulate multiple origins of a gynoecium with free carpels in s. Earlier, Dahlgren et al. (1985) had also postulated that apocarpy is derived in monocots. although they used a different phylogenetic frame- work. It is important to note that there are different views regarding the use of the term “apocarpy.” All authors agree that gynoecia with free carpels are apocarpous, but some follow Leinfellner (1950) and consider gynoecia in which the carpels are postgeni- - usa united (i.e., fused at anthesis) to be structurally Volume 97, Number 4 Remizow al. 625 Leid. History of the Monocot Flower ps L. (Juncaginaceae) (SE M). The gynoecium ea of three All six carp "aa are — via the floral center. —A. Young se of anthesis. Arrowhead x ates the Fig Gy noecium and flower morphol ogy in migas outer-whor sterile cape als and three inner- „whorl fertile gynoecium. —B. Young gynoecium dissected ogi. level of i insertion of licita stamens and tepals: arrow in : x ower at female stage of anthesis. ic, inner- a fertile carpe a]; is, inne er-whor s stan ri n: it, L os, revben e stamen; ot, outer- -whorl tepal; re, eiii possibly -- T = 200 um B — 150 um; € — 600 um; D = 800 pm. vut stamens and tepals. —U oc, outer- whorl steri le Figure 3 I 5. Gynoecium and flower of Acorus of three congenitally united carpels /pper part slits. —C. Apical view of s. —B. ^ Ap a gynoecium. —D adaxial stamens are visible, with the t lot, lateral outer tepal. Scale bars hree a 200 yn apocarpous, whereas others (e.g.. Takhtajan, 1966, 2009) restrict the term “apocarpy” to the condition between carpels is lacking at any stage in development. Thus, in general we avoid without clarification, and Mate to apocarpous. where any type of fusion using the term "apocarpy" prefer free-carpe gramineus Sol. ex Aiton (Acoraceae) (SE of a gynoecium with one - Anthetic flower sh baxial stamens revealed later. abot. 1. Annals of the Missouri Botanical Garden $ isthing M). —A. Entire gynoecium, ps i ; “re septa carpel removed to show nonsecretory sept: : " r three noecium with three fused carpels; only t owing top of gy E ae ana: abaxial outer tepal; adit, adaxial inner tep Some monocots are free-carpellate merely d they possess a single carpel, a condition a "monomery." Monomerous species have - significance for inferring ancestral morphology, partly because it can be difficult to distinguish between — noecia pseudomonomerous and truly monomerous gy Volume 97, Number 4 Remizowa 627 EUR | Hey of the Monocot Flower (e.g., Eckardt, 1937; Philipson, 1985; Shamrov, 2009; González & Rudall, 2010) and partly because even as an extreme form meristic variation (e.g., in Centrolepidaceae; Sokoloff et al., 2009). Thus, the presence of both monomery and carpel fusion in the same group does not necessarily indicate that the presence of free carpels is an ancestral condition in the group. A similar pem of variation (true — plus syncarpy, but no polymerous arpy) occurs in the eudicot order Caryophyllales, i in which Volgin ics inferred that monomery e m syncarpy, at least within ER ee in the subfamily E E Within the monocot order Pandanales, Rudall and Bateman (2006) speculated that the monomerous gynoecium that occurs in Stemonaceae could have been derived from a gynoecium with united carpels (present in Velloziaceae) and could have given rise to the free- carpellate condition that occurs in extant Triuridaceae (see also Rudall et al., 2005). In many angiosperm groups, the conclusion that monomery represents a derived condition can be inferred from the phylogeny, but it is rare ^» find s. Mise that support m syncarpy tot mery (rather I p y) as in Phytolaccaceae. In monocots, non-monomerous free-carpellate gy- noecia are restricted to the core alismatids, Triur- (see Eber, 1934; Igersheim et al., 2001), carpels are me (or rarely weakly connate via the floral center at the very base) in most members of three clades: (1) Alismataceae—Limnocharitaceae, (2) Aponogetona- vean pie Fig. 1C with Aponogeton distachyus L. f.), and (3 ] ae—Ruppia- ceae Zannichelliaceae (Posidoniaceae and Zostera- ceae, monomerous or, in the case of Zosteraceae, possibly pseudomono- merous). In contrast, carpels are fused together in some other core alismatid clades: (1) Butomaceae plus Hydrocharitaceae, (2) Scheuchzeriaceae, and (3) Juncaginaceae (except wo monomerous Triglochin arpellate clades are intezmixed with the an syncarpous clades in molecular phylogenies of Alismatales. MODES OF CARPEL FUSION Three modes of carpel fusion occur in monocots: congenital, postgenital, and fusion via the floral center. Both congenital and postgenital ap fusion can co-occur during development of differe nt parts within the gynoecium (Fig. 4) (see also Remizowa et al., 2008). Congenital carpel fusion, the most common condition in eudicots, is present in some monocots (Fig. 5), E the basal lineage Acorus (Fig. 3), which also lacks septal nectaries (e.g, Rudall & Furness, 1997; seu & Endress, 2000). Despite the presence of congenital fusion between carpels in Acorus, the putative sister to all other monocots, Remizowa et al. (2006b) concluded that postgenital ion between carpels, which is associated with nectary formation, probably represents the wort condition in monocots. Postgenital carpel fusion is common in monocots, but relatively rare among eudicots, rare among syncarpous magno- liids, and absent from early divergent (ANA grade) angiosperms, in which only some Nymphaeaceae possess united carpels, and these are congenitally fused (Endress, 2001). Carpel fusion via the floral center, not combined with other types of fusion, is an unusual condition that is probably restricted to the core alismatids among monocots. In this condition, an internal compitum is always lacking. It could be interpreted as either (1) congenital fusion of the ventral side of each carpel to an extended receptacle (i.e., a form of apocarpy), or (2) congenital fusion between the ventral sides of all carpels, although in practice it is almost impossible to confidently differentiate between these two types (see also Eber, 1934; Igersheim et al., 2001). In most Juncaginaceae, carpels are are united via the floral center, but their flanks are completely free (Figs. 2, 6). Many species of Triglochin (Juncaginaceae) possess three outer-whorl sterile carpels plus three inner-whorl fertile carpels. Commonly, both sterile and fertile carpels are united via the flower center (Fig. 2B). Hosen in * lesa some members of bulbosa L. d by Kócke et al 2010) only the fertile i are united while the sterile carpels remain small and free (Fig. 6), an arrangement that is probably unique to certain Triglochin species monocots. Fusion via the floral center is also present in Potamogeton crispus L. (Potamogetona- ceae), some Aponogeton geton (Aponogetonaceae), Maundia F. Muell. (Maundiaceae, family placement after von Mering & Kadereit, 2010), Damasonium Mill. (Alis- mataceae; to a lesser degree also in other Alismata- ceae; Eber, 1934), and Limnocharitaceae (Troll, 1932; marl 1934; et al, 2001). A related m somewhat different) condition occurs in some charitaceae, e.g-, Ottelia Pers. (Kaul, 1969), in which the receptacle is strongly concave and the dorsal carpel surfaces are congenitally united with the receptacle. Carpel flanks are almost free in some Hydrocharitaceae (as in Ottelia) but so united in others (Troll, 1931; Eber, 1934; Annals of the Missouri Botanical Garden Figure 4. Gynoecium develo postgenital carpel fusion (SEM). ciere united at their flanks. Not genital a pment in Ledebouria socialis Jessop (Asparagaceae), e c — of Mat: congenita —A. Very young gynoecium with three horseshoe-shaped c —C. Later r stage similar to B, with one carp ! postgenital carpel fusion does not occur at this s removed, —E. Detai il of D ne s. —B. Later stage wit carpels el removed to a areas of congenial c cape pe stage. —D. Young gynoecium before postgenita al carpel fusion, wi e » With the region of c ongenital fusion between c arpels enlarged. —F. ( ital >ynoecium after postgen! Volume 97, Number 4 2010 Remizowa et al. Evolutionary History of the Monocot Flower 1969; Igersheim et al., 2001). À concave receptacle could also contribute to formation of the outer ovary wall in other monocots, although its precise morpho- logical identification is problematic (see below). SEPTAL NECTARIES Septal (gynopleural) nectaries are apparently re- stricted to the monocots and probably represent a key innovation of this group, although they are absent from Acorus (Rudall & Furness, 1997; Buzgo & Endress, 2000) and therefore might be synapomorphic for a clade comprising all monocots except Acorus. The fact that es are nt from some Alismatales (including | Aree) could suggest that this nect is synapomorphic for a clade comprising all monocots except Acorus and Alisma- tales. However, we believe that the presence of typical nectaries in some (though not all) genera of Tofieldiaceae supports the origin of septal nectaries ow the "€ between Alismatales and other monocots. Im this context, it is instructive that Tofieldiaceae ee than Araceae) could represent the most basal lineage of Alismatales (S. W. Graham, pers. comm., Aug. 2010). Typically, septal nectaries (see Fig. 7) are located between the ovary locules and disperse nectar through three narrow "enin e e s. pon on Lal surface of the ovary, often 1970; Hartl & Severin, 1981; Schmid, 1985: van Heel, 1988; Simpson, 1993; Smets et al., 2000; Kocyan & Endress, 2001; Rudall, 2002; Remizowa et al., 2006b, Danmann ). nectaries” ius & Cresens, l ) because in some taxa (e.g. Tofieldia Huds., Tofieldiaceae, Alismatales) they are located below the ovary locules (i.e., infralocular nectaries: Figs. 7A, B, 8A, B). In some species, a large common triradiate cavity is present at the ovary center; toward the style this cavity divides into three separate canals. This type of septal nectary is often correlated with inferior ovary formation (Daumann, 1970; Hartl & Severin, 1981; Schmid, 1985; Sajo et al., 2004). Baum (1948), Hartl and Severin (1981), and Sey van | Heel Hem sehen quie congenital and A fusion in the oa of septal nectaries. In syncarpous gynoecia with septal nectaries, D are always initiated by individual 4 fusion between n cape cut longitudinally. The space between regi feet ef. region of congenital septal ne =L Young flo wer. Note trimerous-pentacyclie groundplan. bars: A, C, E, — 30 um; B, D, F-H = 100 um; 1 — 300 um. primordia. The ventral sides of adjacent carpels unite postgenitally at a he late developmental stage. The fusion area, w efines the inner boundary of the nectary, is on very narrow. The outer boundary of the nectary is formed by the outer wall of the ovary, without postgenital fusion (Fig. 4). The outer wall develops as a tubular structure that links all the carpels, resulting in considerable deformation of the of the free carpel regions. Growth of the outer ovary wall extends to the level of the openings of the septal nectaries (Fig. 9A) and determines their position: the more extensive the growth of the ovary wall, the more distal are the nectary ope Morphological interpretation of the outer ovary wall is problematic; it could represent either the congen- itally fused dorsal regions of all the carpels, or a concave receptacle. In terms of morphogenesis, the development of the outer wall of a superior ovary with septal nectaries resembles the development of an inferior ovary wall except in the localization of intercalary zonal growth. In a superior ovary, tissue proliferation is confined to a ring below the periphery of the bases of the young carpels (Fig. 9A); in an inferior (or semi-inferior) ovary, this ring is thicker and extends outward to the region of the receptacle below the tepal bases (Fig. 9B). In some monocots (e.g., Tofieldia, cf. T. c Fig. 8), the nectaries are located below the ovary locules or in the basalmost part of the septa (Igersheim et al., 2001; Rudall, 2002; Remizowa et 2006b). In flowers with infralocular nectaries, the carpels often possess stipes and/or a pronounced ascidiate zone. Carpel stipes can be obliquely inserted on a concave receptacle, giving rise to a peculiar type of internalized nectary, as seen in Tofieldia. In the palm Licuala oreh, in en to iie co = inner surface y nectariferous sox et al. a. In contrast with typical septal nectaries, infralocular nectaries typically open along their outer edge if the ovary is superior. If the ovary is inferior, the nectary opens by long canal(s) extending up to the top of the ovary, as in Heliconia L. (Heliconiaceae, Zingiberales) (Kirchoff et al., 2009). In flowers with infralocular nectaries, the carpels remain completely free until a very late ; developmental stage. carpel fusion is entirely postgenital (van Heel, 1988; Kocyan & Endress, = Remizowa et al., 2006b). ernua Sm., ons of congenital and postgenital fusion vill develop into a fusion; pf. region of postgenital fusion. Scale Annals of the Missouri Botanical Garden ‘i 5 s f sk i s > a s na X usively 5. Gynoecium development in Tric — LE (Liliaceae), in which carpels are almost ex Figu congenitally united, and septal nectaries are abse (SEM). — s are congenitally united from their i initiation: dn La de noecium by postgenital fusion of carpel margins. Scale bars: A-C. neristem; A, B. Gynoecium initiation as an entire triangular me n 1 ter de oo al stage )—F. Stigma development ar E = 106 um; D. F = 300 pm. Volume 97, Number 4 2010 Remizowa et al. 631 Evolutionary History of the Monocot Flower A peculiar type of infralocular nectary occurs in some core alismatids (especially Alismataceae, e.g., lisma, Damasonium) with carpels that are almost free, and united only at their bases via the floral center (e.g., van Heel, 1988; Igersheim et al., 2001). In these species, the nectaries are confined to the lateral carpel flanks in the region of basal carpel adnation at the floral center, either level with the lowermost part of the ovary locules or just below the locules. These nectaries are open along the outer It is raion assumed that the evolution of was directed toward their internal- ization, Le., ud their position within the septa of the gynoecium as almost closed cavities with narrow openings (Fig. 7C—E; e.g., Daumann, 1970; van Heel, 1988). This internalization hypothesis would suggest that gynoecia with infralocular nectaries are more E than those with typical septal nectaries. Van Heel (1988) postulated that during the course of evolutionary internalization, the secretory surfaces shifted from the carpel stipes and the base of the gynoecium toward the ovary itself, allowing a significant increase in the secretory surface, and hence potentially more nectar. Internalization of the nectaries took place via the development of a common outer ovary wall at a relatively late stage. The intemalization hy sis appears to be congruent with the relatively Dy divergence of some taxa with ular nectaries in the monocot phylogeny (e-g., Alismataceae, Japonolirion). However, some aspects of this hypothesis are problematic. For example, van Heel (1988) was unable to find taxa with nectaries that could be regarded as intermediate between typical septal nectaries and infralocular nectaries. Infralocular nectaries are present in A of relatively derived monocot lineages, such es, Poales, Arecales, Zingiberales, and . Suggested that the location of septal nectaries in the ascidiate or plicate zone of carpels is evolutionarily . ore conservative than their location relative to the m fertile portion of the ov vary position is a crios? factor in evaluating the o evolutionary relationships between | septal nectaries. This = scenario has ue pro; Bromeliaceae, Haemodoraceae, Nartheciaceae, and aceae (Simpson, 1998; Rudall, - Sajo infralocular and : ad ds not contribute tc to fusion between carpels. et al, 2004; Remizowa et al, 2008) In these instances, change in ovary position is a key transformation responsible for the change in nectary type. Septal nectaries with relatively distal openings are adaptively less advantageous in flowers with a mpa omy cent nectar is = umen » $2 s. nectary openings at the gynoccium ae facilitates specialized adaptations to particular pollinators and increases the opportunities for contact between the pollinator body and the anthers and stigmas. For obvious reasons, nectaries of any kind are absent from wind-pollinated and iiir pollo monocots. However, septal nectaries are also absent from some biotically pollinated groups and are frequently substituted by other nectary types or other pollinator rewards (e.g., moniliform hairs on stamen filaments). For example, septal nectaries are absent from all Liliales and all Orchidaceae, and in both some species instead possess specialized nectar-secreting regions on their tepals, sometimes in a spur (Rudall et al, 2000; Smets et al., 2000; Rudall, 2002). Perigonal nectaries, which are rela- tively uncommon in monocots (except Liliales), are frequently associated with epigyny (Rudall et al., me Presence and absence nectaries can cur within a single family, e.g., in Nartheciaceae Dicecar), Iridaceae (Asparagales), Das ceae (unplaced in commelinids), Tofieldiaceae (Alis- — ), Arecaceae (Arecales), Pontederiaceae, and emodoraceae (Commelinales). ong other angiosperms, structures that are cians similar to ri nectaries have been described in some early divergen angiosperms, such as Saruma Oliv. ae Piperales) and some cies of Nymphaea L. (Nymphaeaceae, Nymphaeales) (reviewed by Igersheim & Endress, 1998). These structures are nonsecretory septal slits between the incompletely united margins of adjacent IL, 1933; Moseley, 1961; Igersheim & gynoecia with nectaries is that fusion d carpels is tid congenital in Nym- genital fusion does occur ium A ien of L e z Aristolochiaceae, it is restricted to the sealing 0 individual = Endress & Igersheim, 2000) CHARACTER OPTIMIZATIONS Among the key features of monocot flowers, only nectaries is restricted to presence of septal m (Endress dress, 1995), none is universally present all monocots, wi a few highly unusual monocots m : Annals Missouri Botanical Garden 21 1 | L| | hA Pe ee development in Triglochin t Ls str. (/ A-C ) and T. barrelieri Loisel. (D-H), t noecr he —— e omplex x (Kócke et al, nac , show ng fusion via the floral C sists e" < amies 'onsists of s el in two whorls. ( x isi inner-w eei (fertile je e are united via th herl st ot ta remain free from each other. —; - Carpels initiated. —B. T a visible. £. 0 ule: icine —D. Enlarged view of carpels. —E. "reanthetic ; reanthetic gvnoecium at s lightly earlier stage than in E. center M). e floral center. [he outer- iate nature of the erae T noecium with stign other. se ith one inner-whorl c arpel removed. —G. inner-whorl carpel t as facing e Volume 97, Number 4 2010 lack all of them. Their absence is sometimes due to drastic reduction, but other discordant examples are readily interpretable as a consequence of . reduction. Because all of the key features of monocot flowers are homoplastic, at least to some degree, it is |... questionable whether they represent monocot synapo- morphies with subsequent reversals, or whether they evolved iteratively during the course of monocot evolution. Character mapping onto a molecular phylogenetic tree is one way to explore this question. Mapping the presence versus absence of the 3 ical monocot flower groundplan” (i.e., the trimer- . ous-pentacyclic groundplan) reveals that trimerous- pentacyclic flowers are synapomorphic to all mono- cots, with several subsequent reversals. However, this feature is strictly a complex character; its absence does not represent a single character state, because deviations from "typical" groundplan differ radically. |t is possible to subdivide this complex - Character into several characters, such as perianth merism, androecium merism, gynoeciu lepal number, stamen number, and c Optimizations of each of these characters would yield the result that all character states present in the “typical” monocot flower are plesiomorphic within monocots. Some of these character states, such as trimery, are shared with the outgroups, thus poten- tially obscuring the trimerous-pentacyclic groundplan as a key innovation of monocots. Evaluation of carpel fusion and the presence or absence of ee nectaries are similarly problematic. Mapping a character as “carpels fused versus (Fig. 10, lef) would indicate that fused carpels is the ancestral character state for monocots, with at least four reversals to the free-carpellate condition (and additional reversals within Arecaceae—Coryphoideae; Rudall et al. -, in prep.). The general conclusions are not affected if “carpel fusion via the floral center” is treated as apocarpous or syncarpous, because this ion as a complex character, because the character state “carpels united” incorporates gynoecia with erent modes of carpel fusion (congenital and/or Ü Postgenital) However, coding congenital and post- - genital carpel fusion as two separate characters, m Scored as presence versus absence, suggested th congenita ] onocots Wig 10, right), and that postgenital carpel fusion — -whorl fertile Remizowa et al. 633 Evolutionary History of the Monocot Flower (Fig. 11, left) evolved independently in many line- ages. Our parsimonious optimizations also found the absence of septal nectaries to be the plesiomorphic character state, with multiple origins of se a character that is monocot specific. However, this optimization is highly sensitive to taxon sampling and character coding. Minor changes in tree topology and character information affect this reconstruction and make optimization of the ancestral node equivocal. For example, if the basal trichotomy in Pandanales is resolved with Velloziaceae sister to the rest of the order (Rudall & Bateman, 2006), then optimization of the ancestral monocot node changes to equivocal. Another source of inconsistency is Poales. Septal Rudall, pers. obs.), but other families of Poales lack them. If not all Rapateaceae possess septal nectaries, the ancestral condition in Poales could be determined s “lacking septal nectaries,” depending on the distribution of this feature within Rapateaceae. In this case, even with Velloziaceae sister to the rest o the absence of septal nectaries is e "U an es, plesiomorphic en suggest that primitive monocot flow re trimerous-pentacyclie, with congenitally lied ds (no contribution of postgenital fusion) and without septal nectaries. However, in the following discussion we outline our reasons for partial rejection of this hypothesis. in monocots. Thus, CHARACTER CORRELATIONS Some features characteristic of monocot flowers are Endress (1995) observed, the frequent sec torial differentiation of flowers could result from their trimery, because wider gaps between organs of the same whorl allow T and functional links between organs of di whorls that are situated on the same radii (e.g.. ds sed tepals and outer- whorl stamens). We suggest that the presence of only two tepal and two stamen whorls also represents a precondition for sectorial differentiation. Indeed, in flowers with more than two (or only one) tepal and/or stamen whorls (as in some magnoliids), it is spatially ertile carpel; is, inner- -whorl stamen; it, inner-whorl tepal: oc, i C in F. —H. Nearly anthetic gynoecium. M inner ad i epal: $e receptacle (or perhaps the united ventral parts of U horl sterile carpel; os, ou s r-whorl stamen; ot, _ o ceo. All scale bars = 100 um. 634 Annals of the Missouri Botanical Garden aad A . u . . . . P E E ^ "1 1 = " B E E E L - E r YYII I - QUU 0 iL = AAA AA N 'TTTTTTTT TTITITTTTTTT] PITTI TT p" igure L D of septum is on nie A. Toe Wa H = s in longitudinal section. In all secti ons, the iwi is on the right and the Becc. rv — D. } uds. (Tofieldiaceae). —B. Japonolirion Nakai (Petrosaviaceae). —C. Petr osav ia stellaris (Nartheciaceae). —F. Tricyrt es --—— (Lili temen Leia o tener eal. 2008). ——E. Narthec m Huds Endress, 2000). Regions of poste fusi T oh Vasa —H. Acorus L (corra) (Bago ovules; gray, other tissues ton are shown by horizont y by verti ack, Volume 97, Number 4 2010 Remizowa et Evolutionary History of the Monocot Flower problematic to arrange all tepals and stamens in sectorially associated pairs. It is clear that the presence or absence of common primordia is highly homoplastic in monocots (Endress, 1995), although we do not illustrate the character optimization, due to insufficient comparative data. In fact, the presence of common primordia can be questioned in certain taxa where they have been reported (M. V. Remizowa, unpublished). For exam- ple, the presence or absence of common primordia is variable within a single species, Tofieldia pusilla (Michx.) Pers. (Remizowa et al., 2005). We speculate that pre-primordial patterning of the floral meristem in most monocots could include identification of sites of six tepal-stamen complexes in two whorls. At later stages, each site then divides into separate tepal and stamen sites. This sectorial model could explain both the apparent multiple homoplastic origins of common primordia and the occurrence of intermediate condi- tions. This hypothesis is testable by studies of gene- expression patterns in early floral meristems. Howev- er, at least the observation in the lilioid Trillium apetalon contradicts the sectorial model. As outlined above, T. on lacks inner whorl perianth members, and the positions of subsequent organs, including the carpels, differ from the condition in closely related taxa, suggesting that at least in this species and its close relatives, the stamens and perianth members are patterned individually and acropetally. On the other hand, the complete absence of any visible traces of the inner-whorl stamens does not affect the gynoecium position in monocots for ch we possess detailed data (e.g., Iridaceae, Mayaca Aubl., Juncus minutulus, Scirpus). All three monocot groups that include some members with free carpels (Alismatales, Arecales, Pandanales) are characterized by strong variation in flower groundplan. All free-carpellate members of Alismatales and pd deviate considerably m the trimerous-pentacyclic flower morphology. Within Arecales, the lose isolated free- carpellate mangrove palm Nypa also deviates from the typical monocot flower groundplan. Indeed, the groundplan of the male flower in Nypa resembles that of many Triuridaceae, another free-carpellate . Monocot family. Some free-carpellate Cory — (Arecaceae) possess trimerous-pentacyclie flowers e.g., Trithrinax Mart., i phileae), i gh flowers of Chamaerops L. and Pi Phoenix L. _ are functionally unisexual, and Phoenix occasionally has three or nine stamens. It is significant that the - diversity of the flower groundplan is very high in all - three orders of Alismatales, Arecales, and Panda- nales, including taxa with united a ora sues arpel. For example, Zombia L. H. Bailey and Coccothrinax Sarg. (Arecaceae, tribe Cryosophileae) possess a highly reduced perianth, multistaminate androecium, and monocarpellate gynoecium (Drans- field et al., 2008). The correlation between the stability of trimerous- pentacyclic flowers and presence of a syncarpous gynoecium in many monocots was understood in earlier studies of monocot evolution. For example, Takhtajan's (1966, 1980, 1987) evolutionary diagrams implied that monocots with conserved trimerous- pentacyclic flowers and united carpels evolved as a large clade in which lilioids represented a basal group. Takhtajan's classification placed all free- carpellate monocots and their supposed relatives with unstable and unusual flower groundplan outside this large lilioid clade and their sup descendants. The groups not placed within Takhtajan's lilioid radiation were the core alismatids (formerly Helo- bieae), True vd the scm epee or idae 1 aroids, Cyclanthepége, pom and Typhaceae. Taki n uet that "^ oud not » free carpels. Thus, ERE. view was that the yncarpous gynoecium and the trimerous-pentacyclic cantina stabilized simultaneously. This concept of monocot flower evolution emphasized that exhibiting variant traits are relatively primitive. : contrast, the reverse paradigm, which suggests the more common attributes reflect the ini states in monocots, is closer to the views of Dahlgre et al. (1985) and is generally supported by parsimo- nious interpretation of current molecular phylogenetic topologies. Endress (1990) emphasized that stabiliza- tion of flower groundplan and syncarpy characterizes floral evolution in angiosperms in concept of common as "uam implies reversals to a free-carpellate gynoecium during the course of monocot evolution (Dahlgren et al., 1985; Doyle & Endress, 2000; Chen et al., 2004). Compitum formation is considered to be a major adaptive dv (Endress, 1982; Armbruster et al., 2002). An evolutionary scenari scenario that implies a reversal to free-carpellate condition should attempt to explain why carpel fusion was lost despite its adaptive advantages. Recent evidence shows that at least some free-carpellate Alismatales (Sagittaria getifolia Merr .. Alismataceae) have a peculiar type of nh vidi via the receptacle (Wang et rw n to internal compitum forma- tion. A similar mode of pollen-tube growth via the receptacle has been documented in Lac (Triuridaceae) with bisexual flowers oe man et al., 1993). In In Lacandonia, the bisexual flowers 636 Annals of the Missouri Botanical Garden UU H i: eh os HM r C A yeg: Eon 1 3 B e a A A * i LA M LO re Gynoecium structure i ear ml ight imapi, rides a on Sm. (Tofieldiaceae, Alismatales) in serial transverse sections of a ia ed oa . ralocular, triradiate septal n al nectary, and differing patterns of postgenital fusion oo real Sir radial e. —A. Central triradiate nectary at the region where the carpel stipes : d pir is e i P of vascular bundles at the nhe of the section supply six tepal- stipes are —D. Postgenit al t show gynoecium only). —B, ry openings at the level where carpe genitally united, ascidiate zones. —E-G. Post s. united, plicate zones throug Volume 97, Number 4 Remizowa et al 2010 ins Evolutionary History of the Monocot Flower T D E P e P B . 7 B e . . came sd iaa Ed d emos E Ed IE D — p ime d u p p — LI i p Ed —— L growth to gynoecium formation in Ledebouria Roth (A) and Petrosavia Becc. s on the left. Diagrams on the right illustrate schematic Diagrams on the left illustrate the LOOOOQOOO TITI TITITTTTIITI MTTTIT] Figure 9. Contribution of intercalary zonal (B). In all sections, the locule is on the right and the septum i rrespond to Figure 7G and C, respectively. i of Ledebouria, black areas indicate regions internalize the septal nectary. In the left-hand diagram of nding to the region Petrosavia, black areas indicate regions of future intercalary gro tamen bases jacent carpels; this future growth will form the outer wall of the inferior part of the ovary, septal nectary. In right-hand diagrams of both species, black areas indicate tissues prod i assumed that th fi l hf ing of ion of ng flower. The region of intercalary growth is not shown on the right-hand part of mh diagram, because it is impossible to draw a boundary between the product of zonal growth and the carpel wall. Future studies will investigate pollen-tube growth in these taxa. It is well known that septal nectary formation is correlated with postgenital or partially postgenital carpel fusion (e.g. Baum, 1948; Hartl & Severin, a cleistogamous, and pollen germination occurs within the unopened anther. It is interesting that an internal compitum is absent in some monocots with united carpels, even from species that possess a well- developed plicate zone (e.g., Metanarthecium Maxim., Nartheciaceae, Dioscoreales; Remizowa et al., 2008; 1981; van Heel, 1988; Endress, 1995). Vise pia Japonolirion and Petrosavia, Petrosaviales; Remizowa nectaries are absent, carpel fusion is usually completely et al., 2006b). This is also the case in some eudicots, congenital, without any contribution from peupe e.g., some Buxaceae (von Balthazar & Endress, 2002). fusion (e.g. van A Sie AO Rd, is ipn. Ru es ; ilocular in E, unilocular in F, and bilocular š n patterns ol stgenkal D AI e É uj = muc. In the upper part of the gynoecium (H), carpels are free with postgenitally closed ventral slits. Scale bars: A, E-H = um. Annals of Missouri Botanical Garden the Outgrups Intercarpellary fusion Acorales** Araceae* ali Tofieldia** Isidrogalvia** Alismataceae Figure 10. Maximum parsimony optimizations of features the monocots based on Angiosperm Azuma and Tobe (2005). In the first tree, an typ congruent with Takhtajan's (2009) f is considered; this (Nixon, 2002). S organs lost, but this d t affar de : : £h : Sinel flowers that co-occur with other substantially different types of flower groundplan As far as we know, the only exceptions to this occur in two sister genera of Tofieldiaceae (Azuma & Tobe, 2005), Isidrogalvia Ruiz & Pav. (Remizowa et al., HUYE Ju Ve. VAT - 1 D . ` ) 7 ( tal., in prep.), which differ from other Tofieldiaceae in the absence of septal nectaries. Carpel fusion in Isidrogal- via and Harperocallis is partially postgenital, but the basal regions of the carpels are congenitally united (Remizowa et al., 2007b, in prep.), in contrast with other Tofieldiaceae, where congenital carpel fusion is absent (e.g., van Heel, 1988; Remizowa et al., 2006b). Thus, in this respect, Tofieldiaceae show the same general evolutionary tendency to replace postgenital fusion with congenital fusion as other monocot groups in which septal nectaries are lost. The reasons for the correlation between septal nectaries and postgenital carpel fusion are unclear. In N a and Saruma, septal slits occur in gynoecia that lack postgenital fusion between adjacent carpels. A gynoecium with a triradiate nectary opening by three pores and carpels united above the nectary (as in Tofieldia or Borya Labill., Boryaceae, Asparagales) cannot develop without postgenital carpel fusion. T z J ) I py (coenocarpy). In the second tree, only ] deal is congruent with Leinfellner's (1950) concept of syncarpy. Optimizations are constructed using WinClada hal ha E Ed Sancho CEs ACE UE A dnl a: pr r---Outgroups Congenital intercarpellary fusion Acorales pa NS Butomaceae i LL Hydrocharitacose y == Scheuchzeriaceae Araceae (s Bea fieldia O D E dogs e7-7- Alismataceae heed t=- r---Aponogetonaceae t--4 -=-= Juncaginaceae E Potamogetonaceae PI Zosteraceae ie r---Ruppiaceae Cymodoceaceae (=> Posidoniaceae of gynoecium morphology onto a phylogenetic tree diagram of Phylogeny Group III (2009) and Stevens (2009); relationships in Tofieldiaceae follow y £f i n rÉ > sE 1/ + ced 1/, t M O o congenital intercarpellary fusion s rarely with some + `. (+) e ta SZ r x 7 However, if the septal nectaries do not meet in the center of the gynoecium (a more common condition than a single triradiate nectary), there is no obvious developmental constraint against gynoecium develop- ment exclusively by congenital fusion between carpels. For example, the gynoecium of Ledebouria Roth (Figs. 4, 7G), which has septal nectaries, develops through a combination of congenital and postgenital fusion between carpels, but in theory the same definitive shape and internal structure could be achieved if fusion was entirely congenital. | A possible explanation of the fact that postgenital and their monocots hypothesis implies multiple losses of septal nectaries. In well-investigated monocot groups, loss of septal nectaries is always associated with complete (e.g. Nartheciaceae, Iridaceae) or incomplete (Tofieldia- ceae) replacement of postgenital fusion by congenital fusion, suggesting that the presence of postgenital fusion is costly, since monocots switch to congenital correlation with postgenital fusion in extant md e one ancestor. This rPaAmmoan Volume 97, Number 4 ; Eno Remizowa et al. Evolutionary History of the Monocot Flower [eoe etait intercarpellary fusion .---Outgroups Septal nectaries : r=== Araceae ' [77 Acorales | ! : Pleea i i li rt Tofieldia 1 I í 1 CE isidrogaivia ' i avia quee atacea 4 i -Íg Butomaceae inn] = H Hyd ae ' wm : rides Scnelchzenacaso È te-4 r---Aponogetonaceae i Aponogetonaceae i i--d r=== Juncaginaceae Juncaginaceae k. te |=“ Potamogetonaceae E r T Qeloracoas Potamogetonaceae i=j _ —— Ruppiaceae Zosteraceae Cymodoceaceae Cymodoceaceae HL ¿eponolirion Posidoniaceae Posidoniaceae ' Petrosavia pi Petrosavia i Dioscorea Dioscorea | ripe as ae v ri VL Metanarthecium i d pe laceae Triuridaceae $T | ge--Stemonaceae L Ea Pandanaceae” ' r--- Liliales Liliales S; Orchidaceae D. aceae [0,1] Poales [0,1] Commelinales bist saan oe *-—- 0: absent Calamoideae ---- 0: absent ek ie Nypoideae . Dpto [Q1] —— t: present e [0,1] == Ambiguity Geroxyloideae == Ambiguity Fi fusion whenever possible. Why not switch to exclu- sively «tal faston in plante such s 2 seems likely that the early stages of epidermal cell differentiation are similar (i.e., share developmental Troera: X Su dd ° £ bos t sal fiar s Ledebouria? It future septal-nectary formation. There could be a po" large region of epidermal cells that later subdivides into two regions, one consisting of cells that will undergo fusion and the other that will differentiate into a nectary. Early in development, cells of these two types are often similar; before nectar production, adjacent epidermal layers in septal nectaries are in close contact with each other. This hypothesis is potentially testable through gene expression studies in epidermal cells of monocot carpels. The above evidence suggests that the hypothesis that the typical condition is the primitive one is plausible for monocot flowers. Otherwise, it is difficult to rationalize a correlation between the trimerous- pentacyclic groundplan, postgenital carpel fusion, and the presence of septal nectaries in any other way than that it is inherited from a common ancestor of all monocots. It is highly unlikely that septal nectaries tha evolved multiple times in plants that exclusively congenitally united ngenital : gure 11. Maximum parsimony optimizations of features of gynoecium morphology (postgenital intercarpellary fusion and occurrence of septal nectaries) onto a phylogenetic tree of the ots. monocots. optimizations discussed above. Figure 12 shows another parsimonious optimization, with three char- acter states: (0) carpels free; (1) carpels united, septal nectaries present; and (2) carpels united, septal nectaries absent. The character states are o to reject the transition from (2) to (1), as outlined above. Placement of Acorus as sister to all other monocots does not necessarily require that all of its morpho- resemble ancestral states, because can be highly specialized. In fact, among the extant early divergent monocots, the flower ascidiate zone in the carpel, which is pronounced in many early divergent angiosperms (Endress, 2001, a likely feature of the ancestral monocots. earlier observations (Remizowa et al., 2006b) ed that carpels of Petrosaviaceae are entirely nonpeltate, but detailed anatomical investigation of xtensive material has shown the presence of a in both J irion and Petrosavia (Remizowa, in press). Flowers of Tofieldia and Triantha (Nutt.) Baker (Tofieldiaceae sensu Takhtajan, 1997) those of Japonolirion, but the presence of a calyculus in Tofieldiaceae resem- bling a third perianth whorl (Remizowa & Sokoloff, 2003) represents a specialized feature. 640 Annals of the Missouri Botanical Garden Outgroups sss + Acorales sa: Araceae Pleea Tofieldia ' *" Isidrogalvia === Alismataceae Butomaceae s Hydrocharitaceae "a sa Scheuchzeriaceae === Aponogetonaceae = g=== Juncaginaceae tow aafaa Potamogetonaceae bas 1 i Zosteraceae -— '--Ruppiaceae ba Cymodoceaceae t Posidoniaceae Japonolirion Petrosavia Dioscorea s... Tacca s... Narthecium Metanarthecium === Triuridaceae Velloziaceae Stemonaceae J... 2" * Cyclanthaceae “1. Pandanaceae ' 111 [ iliales core-Asparagales == == Orchidaceae == Dasypogonaceae [1,2] .=== 0: carpels free or == Poales [1,2] united only via floral Commelinales Zingiberales —— 1: carpels united, with e s : == Nypoide pM nectaries Ñ == Coryphoideae [0,1] sean 2 carpels united, without .... Ceroxyloideae septal nectaries Arecoideae — MY. re 12. Maxim Figu SEO š states: (0) c ls f x 5) ae baa, w. or united dud via the floral center; (1) T ad with septal nectaries | present; and (2) carpels rd d eharacter Volume 97, Number 4 Remizowa et al 2010 Evolutionary History of the Monocot Flower " Possible evolutionary ee Sticky margins of free developing carpels transformations == P ostgenital fusion Mb ip sa igure 13. Possible evolutionary transformations of pathways of gynoecium development in monocots. Finally, it is important to note that parsimonious character optimization can be highly sensitive to tree topology, so that even minor changes in topology can result in major changes in optimization. For example, if we accept a basal placement for Tofieldiaceae (rather than Araceae) within Alismatales (S. W. Graham, pers. It is likely that the free-carpellate condition evolved several times during the course of monocot evolution, in groups where the stability of the floral developmental program was broken in various re- spects. A reversal to a free-carpellate condition was probably a relatively easy transformation in taxa with postgenital fusion between carpels. As Remizowa et comm.), optimization of congenital intercarpellary al. (2006b) noted, the process of postgenital fusion fusion wi as unambiguous as in Figure 10 between carpels in the ventral region closely i with ACCTRAN optimization, presence resembles the process of postgenital closure of fusion would be ancestral in monocots, individual carpels in the plicate zone. We speculate whereas with DELTRAN optimization, the ancestral that a switeh from one process to the other ean occur monocot condition would be postgenital carpel fusion. relatively easily (Fig. 13). Indeed, it can take place Additional sources of data, including character within a single gynoecium (Fig. 8E-H); different correlations, functional interpretations of character patterns of postgenital fusion can be seen in and the fossil postgenitally united styles (Fig. 4G, H). Three other record, can prov monocot groups with extensive floral variation lack of paro — : polymerous apocarpy (Araceae, wind-pollinated distribution along terminal groups in a phylogenetic Poales, Trilliaceae), but it is significant that in these ‘Tee and hence introduction e ee oa sach _ carpel fusion is exclusively congenital. It is as those expressed in Figures Me n. possible that evolutionary transformations from post- genital to congenital fusion between carpels are irreversible in monocots (Fig. 13), making a reversal to polymerous apocarpy unlikely. developmental constraints, states, ide evidence that allows amendment Literature Cited eev, Y. E. 1996. Sedges (Morphology. 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The development of ovule and embryo sac in Nuphar lutea jag ceae). .. Zhurn. (Moscow & Leningrad) 76: 378-3 ———, ]991b. Megasporogenesis and embryo lopment in representatives of the genera Nym- de do Vici oria (Nymphaeaceae). Bot. Zhurn. (Moscow & inal 76: 1716-1728. Choob. Types of flower Yurtsera, O. V. & V. V. 2005. Types structure es of their morp! cal transforma: tion in n : The preliminary data for the sid development. Byull. Moskovsk. Obshch. Isp. Prir., of Otd. Biol. 110: 40.32. a š "e . 1996. The Trilliaceae in the southeastern Zomlefer, W. E United Mio Harvard Pap. Bot THE EPICHLOAE, SYMBIONTS OF Christopher L. SchardP THE GRASS SUBFAMILY POOIDEAE! ABSTRACT oses of grasses (Poaceae) with fungi of family Clavicipitaceae vay widely | in SM benefits and detriments to = dra ind include mutualisms characterized by against verti (P) Tul. & C. Td i oi TE > epichloid fungi are are turni, und chemical classes: lolines, ne, ergot fruiting of Epichloë species chokes host inflorescences, pre Epichloé symbiont. Vertical. transmission provides the m or sole me MM grass subfamily, with considerable co y complex process of menpeci hybridizations, which can p ion, by and invertebrate herbivores. „This review focuses o on the epichloae, à pop o Neotyphodiu m A EU many produce seconde, 5 and indole-diterpenes logenetic evolution since then. rovide ise clonal symbionts. Evolution of the Poiidese-epichloae symbioses e fungus ees its me within ile Epichloë nan, C. W. Bacon & R. E * Hanlin). Mos antiherbivore alkaloids belonging to any of four distinct plant-associated Clavici means of dissemination fer asexual epichloae.. Molecular ost asexual púbica arose fro: alta and counteract accumulated abe Gen in i evolutionary o eterious mu link between viralen a seeds and D Key words: Alkaloids, aee res coevolution, cophylogeny, Epichloë, Hypocreales, mutualism, Neotyphodium, Poaceae, Podideae, Among the mechanisms that plants deploy against beber chemical defenses are widespread, varied, and important (Schardl € Chen, 2010). However, plants do not produce all of their own defensive metabolites; some are produced by plant symbionts (Bush et al., 1997; Markert et al., 2008; Ralphs et al., 2008). Among these are fungi jo the genus Epichloë (Fr. Tul. & C. Tul. (order Hypocreales) and their asexual derivatives in form eotyphodium A. E. Glenn, C. W. Bacon & R. T. Hanlin, which form symbioses with grasses (Poaceae) in the subfamily Povideae (Schardl et al., 2008) (Table 1). For conve- nience, and in recognition of the close relationship of Epichloë and Neotyphodium species, 1 refer to these fungi collectively as epichloae (adjective, epichloid). The Poói ichloae symbioses are systemic, in that the are present in most aboveground host tissues (but with little or no colonization of roots). ermore, they are constitutive symbioses because they are maintained throughout the life of the host plant. Most Epichloé species and all asexual Neoty- phodium species are vertically transmissible. The ‘ Lam grateful for reviews by Victoria C. Hollowell University, Palmerston, New Zealand), and and Adrian Dd M sequence analysis m ie ETE, iie A. McDonald and Adrian Leuchtmann. Satin, Gump with mM vertical transmission process is especially interesting because it involves extensive colonization of the host ovary, ovule, and embryo, without causing any damage or symptoms (Freeman, 1904). Although vertical transmission via seeds is an important RO pa mechanism for most epi- chloae, in the sexual state they cause a replacement disease called iska” whereby they actually suppress maturation and prevent seed production on the affected infloreseences. Choked culms instead manifest ectophytic proliferation of the fungus to form stromata bearing flask-shaped fruiting structures (perithecia), within which meiosis culminates in t neighboring plants (Chung & Schardl, 1997a; Brem & Leuchtmann, 1999). Most host-Epichloé symbiota exhibit choke disease on only some of the flowering tillers, while the other tillers bear the same fun genet in a completely asymptomatic association. Thus, the interaction of a single host individual with a single Epichloé species individual simultaneously exhibits and Peter F. Stevens (Missouri Botanical Garden), Barry Scott (Massey Leuchtmann : , Zürich, Switzerland). Epichloë typhina population ` Switzerland, and conducted i in the laboratories of y Agricultural Experiment director. de. x pom Plant Pathology, University of Kentucky, Lexington, Kentucky 40546-0312, U.S.A. schardl@uky.edu. Ñ M Missouri Bor. Ganp. 97: 646-665. PUBLISHED ON 27 DecemBer 2010. Volume 97, Number 4 2010 Schardl Epichloae, Symbionts of the Podideae very different phenotypes on different tillers, allowing for both horizontal transmission of sexually derived spores and vertical transmission of clonally derived hyphae (Sampson, 1933). Vertical transmissibility is one of the characteris- tics of the epichloae that predisposes them to evolve into forms that are strongly beneficial to the host. In particular, the asexual derivatives (Neotyphodium cause no choke disease (with occasional exceptions) and are entirely dependent on vertical transmission for their dissemination. Significant host benefits, particularly against insect herbivory, have been documented for N. coenophialum (Morgan-Jones & W. Gams) A. E. Glenn, C. W. Bacon & R. T. Hanlin (cf. Table 1 for attributions and isolates of epichloae) in Lolium arundinaceum (Schreb.) Darbysh [= Schedonorus arundinaceus (Schreb.) Dumort., = Festuca arundinacea Schreb.], N. lolii (Latch, M. J. Chr. & Samuels) A. E. Glenn, C. W. Bacon & R. T. Hanlin in L. perenne L., N. uncinatum (W. Gams, Petrini & D. Schmidt) A. E. Glenn, C. W. Bacon & R. T in in L. pratense (Huds.) Darbysh. [= S. — & M. R. Siegel in F. rubra L. (Clay et al., 1993; Wilkinson et al., 2000; Tanaka et al, 2005). Enhanced drought tolerance is another documented characteristic of N. coenophialum (Mal- inowski & Belesky, 2000), as well as N. uncinatum in L. pratense (Malinowski et al., 1997). Reported effects of N. lolii on drought tolerance of L. perenne are more variable, probably due to selection for adaptation to different habitats (Hesse et al., 2005). Antinematode activity and several additional host benefits have also been documented in the Lolium arundinaceum- Neotyphodium coenophialum system (Malinowski & Belesky, 2000; Timper et al., 2005). These symbioses, where the fungus is mainly or exclusively dissemi- nated by systemically colonizing host seeds, fit well with the prediction that vertical transmission selects for mutualism (Ewald, 1987). Epicniom ALKALOIDS AND Host PROTECTION Several classes of alkaloids produced by epichloae (Fig. 2) deter or kill insects and, in some cases, vertebrate herbivores. Protective roles of lolines and peramine against insects have been demonstrated by genetic and molecular genetic tests, respectively (Wilkinson et al., 2000; Tanaka et al., 2005). Other epichloid alkaloids act against both mammalian grazers and insects. A recent genetic test demonstrat- ed that ergot alkaloids contribute antifeedant and toxic effects against the insect Agrotis ipsilon (Potter et al, 2008). In mammalian systems, neurotropre activities of the ergot alkaloids in general, and ergopeptines in particular, have been known for a very long time (reviewed in Schardl et al., 2006). Likewise, the toxic effects of the indole-diterpenes, also referred to as tremorgens, are well established (Knaus et al., 1994; Parker & Scott, 2004). The anti- mammalian alkaloids produced by epichloae symbi- otic with temperate forage grasses cause significant losses to livestock productivity. This economic impact ESTIS. Š E Sab tie 1 2 + of epichloae in cultivated forage grasses as in Lolium and Festuca L. The claim that the protective effects have arisen by selective breeding (Faeth, 2002) ignores the fact that potent antiherbi alkaloids and anti-insect activities characterize wild popula- tions of these (Christensen et al., 1993), as well as uncultivated grasses such as Agrostis hyemalis (Walter) Britton, Sterns & Poggenb., Achnatherum inebrians (Hance) Keng, Bromus benekenii (Lange Glyceria striata (Lam.) Hit he., Poa autumnalis M ex Elliot, and others (Cheplick & Clay, 1988; Leuchtmann et al., 2000; Schardl et al., 2006, 2007; Gonthier et al., 2008). The epichloae have been shown to affect food web structure (Omacini et al., 2001) and ecological succession. À long-term study has compared plant Lolium arundinaceum with succession in stands of high or low frequencies of Neotyphodium coenoph lum infection (Clay et al., 2005). The highly infested plots showed considerably less plant diversity and dramatically succession to woody plants compared to those with low infection frequency. Experimental exclusion of s and insects indicated that both had a role in this phenomenon. Voles in particular would tend to eat the grass in preference to woody plants unless the grass was infected with the endophyte. This endophyte produces lolines and peramine, neither of which appears to eter mammals, and ergot alkaloids (Siegel et al., 1990) (Fig. 2). In a genetic experiment with a ryegrass endophyte, ergot alkaloids appeared to be a signifi- cant deterrent to feeding by rabbits (Panaccione et al., . Furthermore, grasses with very high levels of ergonovine and lysergic acid amide appear to deter common and suffer stupor due to the ergot alkaloids, they avoid those grasses thereafter. It is the endophytes of these grasses that produce the deterrent ergot alkaloids (Petroski et al., 1992; Miles et al., 1996). Some epichloae also impart or induce potent antinematode activities, although it is unclear if any 648 Annals of the Missouri Botanical Garden Table 1. Relationships of Epichloë and Neotyphodium species. Multiple clades are indicated for interspecific hybrids (ef; Fig 4. Host geographic e Fungal species’ Host grass species Host tribe origin? relationships? Epichloé amarillans J. F. White Agrostis L. spp., Sphenopholis Poeae N. America Eam Scribn. spp. E. baconii J. F. White Agrostis spp., — Poeae Europe Eba villosa J. F E. brachyelytri Schardl & Bachem er erectum (Schreb.) Brachyelytreae N. America Ebe Leuchtm. E. bromicola Leuchtm. & iln vos (Lange) Trimen, Bromeae Europe EbcC Schardl B. erectus Huds., B. ramosus Huds. E. bromicola Hordelymus europaeus (L.) Harz Triticeae Europe EbcC E. clarkii J. F. White Holcus lanatus L. Poeae urope EtC E. elymi Schardl € Leuchtm. Bromus kalmii A. Gray N. America Eel E. elymi Elymus L. spp. Triticeae N. America Eel E. festucae Leuchtm., Schardl & Festuca L. spp., Lolium L. spp- Poeae Europe Efe M. R. Siegel E. festucae Koeleria pyramidata (Lam.) P. Beau Poeae “gasas Efe E. glyceriae Schardl & Leuchtm. Glyceria striata (Lam.) Hitchc. Meliceae N. America Egl E. sylvatica Leuchtm. & Schardl — Brach sylvaticum (Hu Brachypodieae Europe, Asia EtC P. Beauv. E. typhina (Fr.) Tul. & C. Tul. Anthoxanthum odoratum L., Dactylis Poeae Europe EtC glomerata L., Lolium perenne L., Poa nemoralis L., P. pratensis L., P. Guss., P. trivialis i Puccinellia distans (Jacq.) P. : typhina Brachypodium pinnatum (L.) P. n Brachypodieae Europe FC Phleum pratense Poeae Europe EtC š yangzii Wei Li & Roegneria kamoji (Ohwi) Keng & Bromeae Asia EbcC Zhi Wei Wang S. L. Chen E Ç > Holcus mollis L. Poeae urope EHm Neotyphodium aotearoae C. D. Echinopogon ovatus (G. Forst.) Poeae Australia, Nao Moon, C. O. Miles & Schardl P. Beauv. New Pe nse C. D. Moon & Echinopogon ovatus Poeae Australia Efe, EtC N. chisosum (J. F. White & Achnatherum eminens (Cav.) Stipeae N. America Eam, EbcC, Morgan-Jones) A. E. Glenn, Barkworth EXC C. W. Bacon & R. T. Hanlin N. coenophialum (Morgan-Jones — Lolium arundinaceum P Poeae Europe, N. Efe, EIC, Eba & W. Gams) A. E. Glenn. Darbysh. [= Schedono Africa C. W. Bacon & R. T. Hanlin arundinaceus (Schreb) D Dumort., i = Festuca arundinacea Schreb.] N. jen K. D. Craven & " robustum (Vasey) Stipeae N. America Eel, Efe x hardl wo N. E x T: Nan Achnatherum inebrians (Hance) Keng — Stipeae Asia NgC as ac. na omin, Melica ciliata L. Meliceae N. Africa EtC, NgC N. huerfanum š n EFOR : F. White, Festuca arizonica Vasey Poeae N. America EtC A. E. Glenn, C. W. Bacon & R. T. Hanlin N. lolii (Latch, à S Is) A. ex J. Chr. & Lolium perenne Poeae N. Africa Efe x C. W. Bacon & R. T. Hanlin loli X : E. typhina " indet, Lolium perenne Poeae Europe Efe, EtC — N melicicola C. D. Moon i E e a de Melica decumbens Thunb. x Meliceae S. Africa Efe, Ñao EOS NS NISI AT eda NEUSS AUR e Volume 97, Number 4 Schardl 649 2010 Epichloae, Symbionts of the Poóideae Table 1. Continued. ost geographic Clade Fungal species! Host grass species Host tribe origin? relationships? N. occultans C. D. pes Lolium, annual species Poeae N. Africa EbcC, Eba B. Scott & M p d & Cabral Bromus auleticus Trin. ex N Bromeae S. America Efe, EtC N. siegelii K. D. Craven, Lolium pratense (Huds.) Darbysh. P N. Africa EbcC, Efe Leuchtm. & Schardl [= Schedonorus pratensis (Huds.) P. Beauv., = Festuca pratensis Huds.] N. sinicum Z. W. Wang, Roegneria K. Koch spp. Triticeae Asia EbeC, EtC Y. L. Ji & Y. Kang N. sinofestucae Y. Chen, Festuca parvigluma Steud. Poeae Asia EbeC, EtC Y. Ji & Z. W. Wang N. stromatolongum Y. L. Ji, Calamagrostis epigejos (L.) Roth Poeae Asia Nst L Zhan & Z. W. Wang N. dildo Cabral $ Festuca arizonica Poeae N. America Efe, EtC J. F. White N. tembladerae Bromus auleticus, B. setifolius J. Presl Bromeae S. America Efe, EtC N. tembladerae Festuca argentina (Speg.) Parodi, Poeae S. America Efe, EtC F. hieronymi Hack., F. magellanica Lam., : m Parodi ex Türpe, Poa Parodi, P. rigidifolia bee N. ene Melica stuckertii Hack. Meliceae S. America Efe, EtC N. tembla Phleum commutatum Gaudin Poeae S. America Efe, EtC N. EM (e ee & Poa ampla Merr., P. sylvestris Poeae N. America — EC W. Gams) A. E. Glenn, A. Gray C. W. Bacon & R. T. Hanlin N. typhinum var. canariense C. D. Lolium edwardii H. Scholz, Poeae Europe EC Moon, B. Scott & M. J. Chr. Stierst. & Gaisberg N. uncinatum (W. Gams, Petrini Lolium pratense Poeae Europe Ebc, EXC & D. Schmidt) A. E. Glenn, C. W. Bacon & R. T. Hanlin N. sp. indet., FaTG-2 Lolium sp. FW Pee TaT Africa Eba N. sp. indet., FaTG-3 Lolium sp. Poeae Europe, N. ExC, Africa C, FC N. sp. indet., FalTG-1 Festuca altissima All. “hagi N a ie N. sp. indet., FobTG-1 Festuca obtusa (Pers.) E. B. Alexeev — Poeae : oeae N. America Eam, EtC N. sp. indet., FpaTG-1 Festuca paradoxa Desv f Triticeae Europe EbeC, EXC N. sp. indet., HeuTG-2 ?Hordel xs Europe Eam, Eel N. sp. indet., HboTG-1 Hordeum bogdanit Wilensky Ta Europe EbcC, EtC N. sp. indet., HboTG-2 Hordeum bogdanii Vieni Link Triticeae Europe EbcC N. sp. indet., HbrTG-1 Hordeum brevisubulatum (Trin.) ; : Triticeae Europe EbeC, EXC N. sp. indet., HbrTG-2 ordeum brevisub p N. America Ed, N. sp. indet., PauTG-1 Poa autumnalis Muhl. ex F Poeae S. America Efe, Eba, Eam N. sp. indet., PheTG-2 A Roe EI IU) by he gree tenn forest x > - ITEC h y the gr t n for first ! Undescri Dd of Epichlo and ^ T x isolates, according to the convention of Christensen et al. (1993). 3 ae EE scheme of Barkw Major clades are identified by their described i brid s species. iiis EbeC, E. bromicola complex; Ebe, E A pat elymi; Oe eh indet. from Holcus mollis; EtC, E. typhina complex; Nao , abbreviated as follows: Eam, E. amarillans; Eba, E. clade; Nst, N. stromatolongum _ festucae; Egl, E. glyceriae; EHm, Epichloë s sp. N. gansuense of the alkaloids contribute. In a study of an endophyte (Panaccione et al of perennial ryegrass and its effect against the root- parasitic nematode Pratylenc seribneri, alkaloids were ruled out as the main factors ergot lolines can have ., 2006b), and lolines were not expressed in that system. Other studies show that affects on nemat as attractants at lower concentrations, bi as inns at Annals of the Missouri Botanical Garden infection of pit $ me host ovule p in seed EN V s hyphae sexual cycle/ transmission horizontal spermatia to stroma AGE. ame moan inflorescence mating type flag-leaf sheath and arrests its karyogamy À development & meiosis > Figure 1. Life cycles of Epichloë species in relationship to the life cycles of their host grasses. Some Epichloë gu simultaneously undergo sexual and asexual life cycles on different tillers of infected host grasses, as shown here. € y sexual Epichloë species transmit only horizontally and tend to suppress almost all seed production by the infected hosts. OH bal 1 : AE (N. E J: s du 1 1 stromata and are vertically transmitted. The micrograph ME r JE r 2 T t at left shows an ovule infected with E. festucae expressing a gene for cyan fluorescent protein. higher concentrations (Bacetty et al., 2009). Whether ts are relevant to plant-nematode interac- tions in the field remains to be determined. Another intriguing possibility is the effect of lolines on foliar ns C. D. Moon, B. Scott € M. J. Chr., and plants with this endophyte usually have lolines (TePaske et al., 1993). Annual ryegrass forage (e.g., Lolium rigidum Gaudin and L. multiflorum Lam.) can sometimes be toxic to livestock when infected with Clavibacter toxicus, which is in turn infected with a bacteriophage believed to encode a toxin (McKay & Ophel, 1993). The bacterium is vectored by the foliar nematode Anguina funesta. It is unknown whether the ryegrass stands that c toxicosis possessed or lacked the endophyte. Con- ceivably, the fact that annual ryegrass toxicosis is a rare phenomenon may relate at least partly to antinematode activity of this endophyte alkaloid. Thus, the effects of the alkaloids on foliar nematodes would be interesting to investigate. Among the species of epichloae, there is consider- able diversity in the alkaloid profiles, and even diversity within some species. For example, Epichloë festucae, which has been studied more extensively at this level than have any of the other sexual species, includes strains that produce various combinations of all four classes of alkaloids (Schardl, 2001) (Table 2). The chemotypic diversity of E. festucae is particularly interesting considering that phylogenetic analysis on intron sequences of housekeeping genes indicates exceptionally low sequence variation for this species (Moon et al., 2004). In contrast, E. typhina (Fr) Tul. & C. Tul has much greater sequence diversity, but very little chemotypic variation: no loline-, indole-diterpene-, or ergot-alkaloid-produc- ing strains of E. typhina or its close relatives, E. sylvatica Leuchtm. € Schardl and E. clarkii J. F. White, having been identified to date (Leuchtmann et al., 2000; Young et al., 2009). Anti-insect activity attributed to strains of E. sylvatica indicates that additional fungal metabolites or protective effects on host plants remain to be identified (Brem & Leuchtmann, 1) RELATIONSHIPS AMONG PLANT-ASSOCIATED CLAVICIPITACEAE Although the fungal order Hypocreales is dominat- ed by plant parasites and symbionts, the family Clavicipitaceae s.l. comprises primarily insect para- sites. Recently, this family has been reassessed based on multiple gene sequences, erecting the families Cordycipitaceae and Ophiocordycipitaceae (Sung et al., 2007), both of which are mainly insect parasites- Volume 97, Number 4 Scl 2010 : 651 Epichloae, Symbionts of the Podideae HN | Ergovaline Ergonovine 2 Spe 1 = eagles of alkaloids produced by ue. Loi B B is th bundant indole diterpene produced by of N. coenophialum n arundinaceum. Pe l ] 11 Epichloë and + L and N. N. lolis, whereas the Ergovaline is the lominan dipe ergot alkaloid, ergonovine, is produced b deterrent to grazers Clavicipitaceae s. str. includes insect parasites (such as Hypocrella and Metarhizium spp.) as well as a clade of plant parasites and plant symbionts. These plant- associated Clavicipitaceae include the genera Clavi- ceps Tul., a Speg., Epichloé, and Myriogeno- spora G. F. . Based on phylogenetic studies of ribosomal bg genes (rDNA) (Kuldau et al., 1997; White & Reddy, 1998; Sullivan et al., 2001) and the gene for acetaldehyde dehydrogenase ALDH1-1 (Tanaka 2008), this clade probably also includes the genera Aciculosporium I. Miyake, Atkin- sonella Diehl, Balansiopsis Höhn, Heteroepichloë E. Tanaka, C. Tanaka, Gafur & Teuda, Neoclaniceps .F. White, Bills, S. C. Alderman & Spatafora, Parepichloé J. F. White & P. V. Reddy, and Ustilaginoidea Bref. ‘Soe produced by, for pete ag N. gansuense in Achnatherum i discleriuins didus boss grass) as a major Most of the plant-associated Clavicipitaceae infect Poaceae (Diehl, 1950; Bischoff & White, 2003). Some Turbina Raf. species (Convolvulaceae) has recently been identified (though not yet described and named) me etal., -ANO With the nm of the Claviceps plant —— | der boat plants. Specifically, they grow prar within, or epibiotically upon, the aerial tissues of the plant, without obvious signs or symptoms in most of the colonised tissues. Their tie preet is or only by ds which form on i edic organs or locations such as | de florets, Annals of the Missouri Botanical Garden Table 2. Alkaloid profiles of grass species symbiotic with Epichloë festucae. Data are from Siegel et al. (1990). Host Lolines Peramine Ergot alkaloids Indole-diterpenes Lolium giganteum (L.) Darbysh. + + _ = Festuca ovina L. _ J $ = F. longifolia Thuill m + + = F. rubra L. subsp. = A S * F. rubra subsp. rubra = 5S * = F. rubra subsp. commutata Gaudin = + + n = inflorescences, nodes, or segments of the leaves (Diehl, 1950; Bischoff & White, 2003). More extensive study is required to determine if the aon gra Clavicipitaceae, together with Clavi- ceps and eps species, constitute a monophy- letic a n addition to more comprehensive ps R further characterization of host interactions or several related Clavicipita- ceae that are eas fruiting on plants; e.g., Dussiella tuberiformis (Berk. & Ravenel) Pat. on Arundinaria tecta (Walter) Muhl. (Poaceae), Shimizuomyces para- of Smilax M Miq. of plant- associated Clavicipitaceae (Bischoff & Y White, 2003). Some of these may first infect sucking insects on the plant and then access plant nutrients via the insect stylet. Such appears to be the case for Hyperdermium bertonii (Speg.) J. F. White, R. F. Sullivan, Bills & ywel-Jones, found in association with a scale insect on an unidentified Asteraceae (Sullivan et al., is observation fuels speculation that para- sitism of plant-associated invertebrates provided an evolutionary link to plant-symbiotic fungi in this family (Sullivan et al ; tafora et al., 200 7. Effects of the clavicipitaceous fungi on their host plants suggest that they alter the balance of plant growth regulators. Aciculosporium take 1. Miyake, Heteroepichloé sasae (Hara) E. Tanaka, C. Tanaka, Gafur & Tsuda, and H. bambusae (Pat.) E. Tanaka, C. Tanaka, Gafur & Tsuda cause witches’ broom of bamboos (Tanaka et al., 2002; Tanaka € Tanaka, 2008). Many of the other fungi suppress host flowering. As described above, Epichloë species can fruit on immature inflorescences and halt their further maturation. Balansia epichloé (Weese) Diehl, B. henningsiana (Müller) Diehl, and Myriogenospora atramentosa (Berk. & M. A. Curtis) Diehl form their stromata on leaves, but nevertheless also partially or completely suppress host flowering (Clay et al., 1989; Glenn et al., 1998). Thus, these plant parasites alter declan in a way that appears to redirect resources away from host seed production to support Many fungal species allied with the Clavicipitaceae lack a known sexual state, either because they never form stromata or, more rarely, because their stromata have not been observed to progress past the production of mitotic spores (conidia) to produce meiotic spores. These fungi are described as either eotyphodium or Ephelis Fr. species depending on the ontogeny and morphology of their conidia. Use of these genus names conforms to the International Code of Botanical Nomenclature (cf. Art. 59; McNeill et al., 2006), requiring that any fungi of phyla Ascomycota and Basidiomycota that lack a known sexual state (teleomorph) be given distinct form names tha e asexual state (anamorph). Arguably, lie availability of facile molecular techniques to establish relationships of isolates should obviate the need for this arcane system, but the requirement remains entrenched in the Code. The implication for the plant- associated Clavicipitaceae is that those fungi classi- fied in form genus Neotyphodium are (with the exception of Acremonium chilense J. F. White & Morgan-Jones, = N. chilense (J. F. White & Morgan- Jones) A. E. Glenn, C. W. Bacon & R. T. Hanlin) molecular congeners of Epichloé species (Glenn et al., 1996). Also, the Ephelis anamorph that is usually associated with Balansia and related genera has also been described without an associated teleomorph (Christensen et al., 2000b). Interestingly, Atkinsonella species actually produce two mitotic spore states, one ling the Neotyphodium anamorph, and the other resembling the Ephelis anamorph (Leuchtmann & Clay, 1988) EPICHLOË SPECIES The Epichloë species are members of the fungal phylum Ascomycota, order Hypocreales, and are characterized by systemic, intercellular growth in a host grass (Poaceae) and production of a brightly colored stroma (fruiting body) that envelops the host leaf sheath and subtending immature inflorescence of the young flowering culm (Ellis & Everhart, 1886). Upon emergence, the initially unpigmented stroma produces palisades of conidiogenous cells giving rise Volume 97, Number 4 2010 Schardl 653 Epichloae, Symbionts of the Podideae to conidia that serve as spermatia. Cross-fertilization is most often mediated by female dipteran flies of genus Botanophila Lioy. (Anthomyiidae), which lay one to several eggs on each stroma, and for which the maturing stroma provides nutrition for their larvae (Bultman et al., 1998). Fertilized stromata mature to form flask-shaped perithecia within which spore sacs (asci) develop. Each ascus bears eight meiotically derived spores (ascospores) which are filamentous and contain numerous haploid nuclei. In some species, these spores tend to break up into part- spores on maturation (White, 1993). As perithecia mature, they accumulate yellow to orange carotenoid pigments. This bright coloration is distinct from the , dark brown, or black pigmentation in stromata or sclerotia (resting structures) of most other plant- associated Clavicipitaceae. Mature ascospores are ejected through the apical pore of the ascus and the ostiole of the perithecium, and mediate infection of new plants or developing seeds on neighboring plants (Chung & Schardl, 1997a). Host SPECIFICITY As currently defined, and consistent with man molecular — analyses (Kuldau et al., 1997; Bischoff & White, 2003; Sung et al., 2007; Tanaka & Tanaka, ZUM. Epichloë species and Neotyphodium tribes of the Poöideae. The only other Clavicipitaceae known to infect pooid grasses are some Claviceps species and Balansia texensis (Diehl) P. V. Reddy, Clay & J. F. White [= Atkinsonella texensis (Diehl) Leuchtm. & Clay], which systemically infects and chokes inflorescences on Nassella leucotricha (Trin. & Rupr.) R. W. Pohl (Morgan-Jones & White, 1989). Although Epichloë species are found in a broad phylogenetic range of the Podideae, most described species of Epichloé are apparently restricted to a single host genus or closely related genera within a tribe (Table 1). However, the possibility must be considered that species are sometimes described on the assumption of restricted host range. Therefore, species represent populations of interfertile geno- types, and phylogenetic analyses of intron — in genes for B-tubulin (tubB), y-actin (actG), and translation elongation factor 1-X (tefA) (Fig. 3) indicate that most described Epichloé species corre- spond to unique clades (ignoring the asexual species and groups, which I discuss later). Thus, there is a close correspondence between host range, interfertility, and phylogenetic relationships of E. amarillans J. F. White, E. brachyelytri Schardl $ Leuchtm., E. bromicola Other relationships are intriguingly more complex (Fig. 3). Epichloé festucae constitutes a clade with extremely low sequence variation, and mainly associ- ated with Festuca and Lolium species (Leuchtmann et Pers., nom. illeg.; Craven et al., 2001b). Chloroplast DNA phylogeny places K. on a well- supported clade ene from the eee See Pus oem ts (Schardl et al., the tucae 2008). pentes attempted matings between an isolate from K. pyramidata and E. festucae stromata on Festuca rubra failed to yield viable ascospores (Craven et al., 2001b). This situation is not unique. Many isolates of E. typhina on Brac hypodium pinnatum (L.) P. Beauv. (tribe Brachypodieae) appear to be very close phylogenetically to E. sylvatica, which has only been identified on B. sylvaticum (Huds.) P. Beauv. (Fig. 3). However, test matings indicate that E. sylvatica is incompatible with E. typhina on B. pinndium um (Lench dues & Som. 1998). In contrast, eral host genera and tribes are interfer. These findings illustrate that pre- phylogenetic iw and that rent hosts sometimes have strong prezygotic ssolation. As currently circumscribed, Epichloé typhina has a broad host range including several grass genera in tribe Poeae, as well as in Brachypodium pinnatum (Brachypodieae). However, a population genetic study suggests that .E. typhina is a complex of genetically isolated populations associated with different hosts Schardl et al., unpublished). Isolates were surveyed — haplotypes were found in association with more than one host, indicating strong genetic isolation between host-specific groups. The possibility of similar host- based subdivisions of Epichloé species remains to be investigated in the cases of E. baconii J. F. White and amarillans. Possible underlying mechanisms could iecinde host phenology (particularly flowering time), genetic determinants ost specificity, or specific preferences of Botanophila flies for stromata on each 654 Annals of the Missouri Botanical Garden Epichloë/Neotyphodium tefA gene tree (nj) Host: Fungus: 5 l Dactylis glomerata 7 Hs EL. E. typhina L8 — bot m 4 Anthoxanthum odoratum T tolum perenne Dactylis glomerata Holcus lanatus E. clarkii ikea a mays (PhyMI joined tefA intro mam tn ema allele sequence askama represented d ipa terminals, des ignating the two v VER ceil and N. occultans are sepse T y . Exceptions are E. uen which e each of these Volume 97, Number 4 2010 Schardl Epichloae, Symbionts of the Podideae host. Published studies (Chung et al, 1997) and personal observations of the author suggest that all of these factors may be involved, but that none of them constitutes an absolute isolation mechanism. Epichloé stromata are hermaphroditic, expressing both spermatia and ascogenous (female) hyphae (White et al., 1991). The sexual cycle has not been reproduced in culture, but conidia produced in culture can serve as spermatia when transferred to a stroma of opposite mating type in the same interfer- tility group (Schardl & Tsai, 1992). For this reason, many isolates that do not produce stromata can be checked for mating compatibility with stroma-forming strains. For example, E. bromicola is known several Bromus L. species and produces stromata on us ., but not on B. benekenii or B. ramosus Hads, Isolates Roi the latter two hosts were cultured interfertile (Brem & Leuchtmann, 2003). This finding extended the known host range of E. bromicola and demonstrated that an Epichloë species may fruit on only some of its host species. Several other epichloae also appear to have arisen from Epichloë species infecting new host species (host jumps), losing their ability to fruit, and becoming strictly seed transmitted (Fig. 4). These are the nonhybrid Neotyphodium species (the hybrids are discussed later) Some arose by jumps between species in the same grass genus, as in the aforemen- tioned case of E. bromicola. Other apparent jumps are broader, between host genera or tribes. In three instances of jumps between host tribes, the fungus has retained the ability to mate with its ancestral Epichloë species if conidia from culture are used as spermatia. Thus, an isolate from Hordelymus europaeus (L.) Harz (tribe Triticeae) is compatible with E. bromicola on Bromus erectus (Bromeae), an isolate from Elymus virginicus L. (Triticeae) is compatible with Epichloé amarillans on Agrostis perennans (Walter) Tuck. (Poeae), and an isolate from B. kalmii A. Gray (Bromeae) is compatible with Epichloë elymi on Elymus virginicus (Triticeae) (Moon et al., 2004). These results establish clear relationships to sexual ancestors for epichloae that lack a sexual state in nature. In contrast, other epichloae arising from host jumps seem to have lost male fertility as well as fruiting ability. The overall pattern emerges that each Epichloé species forms stromata mainly on hosts of a single species, genus, or group of related genera in a tribe, and that a strain that has colonized a more distantly related host does not fruit on that host. So far, this I + + apply t 1 + y | Epichl se species and host-specific population of E. typhina, the sole exception being E. festucae, which infects and fruits on Festuca and Lolium species as well as the more distantly related Koeleria pattern suggests that most Epichloë species can inb fruit on a host with which it has coevolved. I propose a Been mee hypothesis that, when an Epichloé species infects a host with which it has not coevolved, it may not express stromata in the new host and thereby becomes trapped in vertical transmission mode. This particular h is has not been sufficiently tested because it is n io difficult to move an Epichloë or Neotyphodium isolate from one grass host into a host that does not naturally harbor the same species (Christensen, 1995). There is one reported case in which Epichloë elymi from Elymus virginicus was successfully moved to Brachy- elytrum erectum (Schreb.) P. Beauv. and then appar- ently produced stromata on the artificially infected B. erectum plants (Leuchtmann & Clay, 1993). However, failure to reproduce this result (Schardl, unpublished) leaves some doubt about the identity of the observed stroma-forming plants. Another study that bears relevance to the trapped endophyte hypothesis is that of Brem and Leuchtmann (2003), who observed that natural associations of Epichloë bromicola with Bromus erectus produced stromata, and those with B. benekenii or B. ramosus did not; yet when isolates of E. bromicola from B. erectus were decet into A +. benekenii or B. ramosus in the new associations. This maki is unsupportive of my trapped-endophyte hypothesis, with the caveats that the stromata on B. benekenii and B. ramosus caused atypical development of the host tillers (suppressing stem elongation), and that the new associations were unstable. Brem and Leuchtmann (2003) suggest that such instability provided selection favoring the strict vertical transmission that charac- terizes na bromicola symbioses with B benekenii and B. ramosus. Therefore, although it is conceivable that some host jumps immediately trap the symbiont and render it unable to fruit, others may A iei é- appears to " Lasa and E. ijina, except E. fest 273 isolates of E. eine from four sympatric host species rent host spec which appears to be paraphyletic to E. clarkii and E on atica. In every species us, a survey of "indicated that no haplotypes were shared between isolates from 656 Annals of the Missouri Botanical Garden A tubB gene tree: Host: Fungus: Clade rel.: 2905, Neotyphodium sp. NgC N. guerinii NgC, EtC N. gansuense NgC N. occultans EbcC, Eba EbcC, EtC E. yangzii EbcC EbcC, Efe Eel, EtC Eel, Efe Eel, Eam Egl N. stromatolongum Nst Eba, EtC Eba N. coenophialum Eba, Efe EtC Eba, Efe Eba, EtC EbcC, Eba N. coenophialum Eba, Efe, EtC Efe Efe, Nao EbcC, Efe Efe, EtC Efe, Nao Remaining tree on panel B Figure 4. Ph logeneti based on Md RR NN M Weis asexual epichloae (Neotyphodium Spp.) with sexual T: (Epichloë spp) cpi (EtC) clade. —B. Se a 4 = of iion Spiren intron sequences. —A. ences outside the E. typhina relationships of the fungal tubB Ben ized s are host species, fungal species (if vigens and the clade RE OEC UA HERES qe Ner eb S Em HR E e TU Pm AREE, VIO EUR Mr o Eo Volume 97, Number 4 657 Schardl Epichloae, Symbionts of the Poóideae B tubB gene tree: Host: Fungus: Clade rel.: 0.005 F1 1 Figure 4 (Continued). The number on each terminal leaf of the tree indicates the ee am — ord same allele sequence. Numbers on branches are bootstrap support values. All haploids have only Due e dl i bandi whereas i oia amaltiple alleles are inferred to be conis e Td "Een D oes - "e a d "i es 3 clades are abbreviated T 2 L P 0342, and estimated gamma shape parameter (= 0.891) assuming four rate categories. Annals of the Missouri Botanical Garden Or TAPAT TD for greater stability and mutual benefit. Up to this point, I have implied that loss of fruiting (either by mutation and selection, or by host effects) confines the epichloid fungus to vertical transmission mode, but such an assertion needs critical assessment. Ascospores form in the stromata, and studies under natural or near-natural conditions have indicated that ascospores mediate horizontal transmission (Chung & Schardl, 1997a; Brem & Leuchtmann, 1999; Leyronas & Raynal, 2008). Conidia appear less likely to be involved in horizontal transmission, and in any case are mainly associated with the newly emerged stromata. Conidia produced on asymptomatic plant surfaces might conceivably mediate horizontal transmission (Tadych et al., 2007), but epiphyllous conidia are very sparse compared with the stroma. With these consid- erations, it seems apparent that without stroma production an epichloid lineage is highly, but perhaps not entirely, dependent on vertical transmission for its persistence. With the exception of asexual epichloae (Neoty- phodium species), stroma production (either borne on the plant or arising from a sclerotium) is a feature shared by all plant-associated Clavicipitaceae. There- fore, it is likely that the stroma is required for these fungi to complete their life cycle and transmit to new host individuals. What sets the Epichloë species apart is their highly efficient vertical transmission, which obviates any requirement for fruiting and the sexual cycle, at least on short evolutionary time scales (Selosse & Schardl, 2007). Balansia hypoxylon (Peck) G. F. Atk. [= Atkinsonella hypoxylon (Peck) Diehl] also oe vertically via cleistogamous seeds of grass species within Danthonia DC., but a aaa genetic study indicated that asco- spore-mediated horizontal transmission is much more important for B. hypoxylon (Kover et al., 1997). Considering that vertical transmission is very common in Epichloë, that many Epichloë and N Neotyphodium species provide fitness enhancements and protection to their hosts, and that hosts for epichloae are broadly ra in subfamily Podideae, the evolutionary origi the Povideae-epichloae symbioses is ra to consider. EVOLUTION AND COPHYLOGENY OF POÓIDEAE- EPICHLOAE SYMBIOSES of grass subfamily Podideae known to tribes missing from this list are certainly under- studied, so it would not be surprising to find that they also include hosts of epichloae. Known hosts represent the entire phylogenetic range of Povideae, from Sine erectum to Poa pratensis L., but ere are none documented outside of the Poóideae. Rather, members of other grass subfamilies and more rarely, other monocot and even dicot families) host other Clavicipitaceae. This pattern of host and symbiont dr suggests that the genus Epichloé evolved at approximately the same time as the Podideae, perhaps as cospeciation events. Some of the relationships within the epichloae suggest that cospeciation, or a more diffuse process of cophylogeny, has been common, but not universal, throughout the evolution of the Podideae and Epichloé species (Schardl et al., 1997). The pattern seems to be obscured somewhat by the large number of interspe- cific hybrids as well as the apparently broad host- e E. typhina complex. If these are removed from consideration, then the major clades of the remaining epichloae reflect major clades of the grasses (Figs. 3, 4). The speciose tribe Poeae hosts several related species, E. baconii, E. amarillans, and E. D well as Neotyphodium | stromatolongu undescribed species associated with Holcus mollis L Similarly, E. elymi, E. yangzii, and E. bromicola are symbionts of grasses in the sister tribes Triticeae and Bromeae. Deep branches in the Epichloé-Neotypho- dium gene trees correspond with deep divergences of host tribes Brachyelytreae, Stipeae, and Meliceae (Schardl et al., 2008). The topologies of the tefA and tubB gene trees are not identical (Figs. 3, 4), and there remains ambiguity in the topology of the Povideae tree, making any precise topological com- parison impossible. An alternative method to assess use this approach heavily weights deeper nodes (older divergences) relative to shallower nodes (recent divergences), we modified the method ds correct for this disparity (Schardl et al., method takes account of topology, but tests for stall significant correspondence of ages of corresponding nodes in the host and symbiont gene trees. Applying this method to fungal tefA and tubB nt of epichloae and host grasses suggests at the genus Epichloé originated approximately K. M s ideae. years ago. If so, the common ancestors of host and symbiont probably interacted much like the current- day Brachyelytrum-Epichloé brachyelytri, Festuca— Epichloé festucae, and most other Povideae-Epichloé Volume 97, Number 4 2010 Schardl Epichloae, Symbionts of the Podideae 659 symbioses with mixed horizontal and vertical symbi- ont transmission. Poóideae—Epichloé symbioses are unique among the interactions of Poaceae with Clavicipitaceae in that both the plant and the symbiont are fully capable of both asexual and sexual reproduction, and the symbiont is efficiently transmitted in the host seed ny. Although most other Poaceae-Clavicipita- ceae symbioses lack vertical transmissibility, the Danthonia a hypoxylon s ce most close- ly resemble the Potidese-Epish loé symbioses in this respect (Clay, 1994; Kover & Clay, 1998). In Danthonia species, B. hypoxylon transmits vertically in cleistogamous (self-fertilized) seeds, but almost always chokes the chasmogamous (open-pollinated) inflorescences. Sometimes, particularly when B. hypoxylon strains are moved between d Danthonia s ch us infloresc are incompletely choked and re venia seeds, some of which transmit the fun pparently, there is a trade-off between Vind and vertical transmissibility to chasmogamous, as well as cleis- togamous, seed progeny in the Danthonia—Balansia hypoxylon system (Kover & Clay, 1998). In contrast, the Podideae-Epichloé system exhibits no such trade- off. In those cases where an Epichloé strain infre- quently chokes its host, vertical transmission to seed progeny is highly efficient, whereas some, more virulent Epichloë strains are apparently incapable of oim transmission in their hosts (Chung ; 997a). Thus, the key advance in the evolution of the that link broken, hosts can reward relatively benign symbionts by providing highly efficient vertical dissemination and can deny this benefit to highly virulent strains. ASEXUAL EPICHLOAE, THE NEOTYPHODIUM SPECIES Given that Poóideae vertically transmit the epi- chloae at very high efficiency and that the symbionts have the potential to be highly beneficial by, for le, combating herbivores, the most favorable situation for the host may be a symbiosis without choke. Such a symbiosis relegates the symbiont to strictly clonal reproduction; that is, the fungus is asexual. Due to Article 59 of the International Code Botanical Nomenclature (McNeill et al., 2006), such asexual fungi are artificially placed in a separate genus from their sexual relatives, so in a formal sense the asexual epichloae are classified as Neotyphodium species, although they are clear phylogenetic conge- of the sexual Epichloé species (Kuldau et al., 1997; Moon et al., 2004). Although the asexual Neotyphodium species fail to produce stromata, some can be experimentally mated to compatible Epichloé strains because conidia produced in culture can serve as spermatia. Most Neot ies, however, seem truly to be asexual. Such species disseminate mainly—indeed, perhaps exclusively—by vertical transmission, which is accomplished when they invade the ovule and eventually the developing embryo without any negative effects on the host tissues (Freeman, 1904). When the seed germinates, e fungus continues to colonize the shoot apical meristems. As plant cells emerge from the meriste- atic zone into the expansion zone, the fungal symbiont keeps pace apparently by intercalary growth of its hyphal strands (Christensen et al., 2008). Colonization of new tillers tends to be highly efficient, and once floral primordia are initiated they are also colonized, allowing for vertical transmission in the next host generation. Considering that this same process of vertical transmission is exemplified by many Epichloé spe- ci t species interactions, the simple scenario for evolution of Neotyphodium species would be that loss of the sexual state, for example by loss of key genes for stroma production, would generate an asexu fungus. This fungus would remain fit and persist in nature by virtue of its very efficient vertical trans- mission, and because this would remain more likely to enhance than degrade host fitness, selection would favor host compatibility. This simple scenario, however, appears not to apply to most ual epichloae, which have more complex evolutionary origins; most have the genetic footprints of interspe- cific hybrid origins. A major difference between the genomes of the sexual and asexual epichloae is that the sexual species are generally haploid, whereas most (but by no means all) of the asexual species are heteroploid; that is, they possess more than a single complement of chromosomes. Evidence for this includes the detection of multiple alleles in asexual isolates for genes that are singly present in each sexual isolate (Leuchtmann & Clay, 1989; Moon et al., 2004). Further evidence is the difference in genome sizes. Quantitative Southern- ven analysis and electrophoretic karyotyping indicate Neotyphodium u. and a N. loli X rper typhina hybrid (an undescribed taxon identified as LpTG-2) have approximately twice the - DNA content as isolates of the sexual species E. festucae, E. typhina, and the nonhybrid asexual species N. lolii (Kuldau et al., 1999). The E. festucae genome has been sequenced and subjected to optical mapping (Schardl, unpublished), and the results indicate a genome size of 27-30 (Mb), almost precisely the size estimated by Kuldau et al. Annals of the Missouri Botanical Garden (1999). The estimated 57-Mb genome size of N. coenophialum is likely, therefore, to be similarly accurate. Most Neotyphodium species have multiple (two or sometimes three) alleles of genes for which only a single allele is detectable in sexual Epichloë species. Phylogenetic analyses of tubB, tefA, and actG sequences have been conducted to distinguish the possibilities that the multiple alleles in heteroploid ichloae arose by gene duplications, or alternatively were contributed by different ancestors (Schardl et al., 1994; Moon et al., 2004; Gentile et al., 2005; Moon et al., 2007; Iannone et al., 2009; Yan et al., 2009). In each case, the different alleles in an isolate showed relationships to those of different sexual species (Fig. 4). Each Epichloë species occupies a distinct clade in the phylogeny, although there are some cases of paraphyly. The relationships among multiple alleles in each asexual species are much more divergent than the relationships among alleles within any population of sexual species. Furthermore, most of the alleles to alleles in Epichloë species, making it possible to assign ancestry of the hybrid endophytes. In F igure 4, each hybrid has ancestors from the two or three distinct species or clades indicated. These ancestors are apparent from the relationships of their two or three tubB alleles, except in the case of N. uncinatum, which has only one detectable tubB allele from the E. typhina clade. However, the single tefA allele of N, uncinatum is related to that of E. bromicola, and this fungus has two actG alleles related to those of E. typhina and E. bromicola (Craven et al., 2001a). The hybridization events giving rise to asexual epichloae were most lkely parasexual (somatic) rather than sexual. Extensive attempts to generate sexual hybrids almost all failed, with the excepti. an Epichloë festucae X E. baconii mating (Leucht- mann & Schardl, 1998). The resulting progeny was haploid, with parental alleles that had segregated in Mendelian fashion. Thus, this sexual hybridization failed to generate progeny with the typical heteroploid constitution. Also, two asexual epichloae, dium coenophialum (Tsai et al, 1994) and N. chisosum (Moon et al., 2007), have three ancestral species each. Considering that sexual isolates are consistently haploid, a sexual origin is difficult to imagine for these three-ancestor hybrids. Ney less, the sexual state was likely involved in hybridization events because a hori sion event was required to move an ancestral Epichloë strain into a host in which the other ancestor resided (Fig. 5). Neot coenophialum and other Neotyphodium Initially, evidence of interspecific hybrid origins of yphodium Selosse & Schardl, 2007). species (Schardl et al., 1994; Tsai et al., 1994) was surprising in light of a widespread belief that all ilamentous ascomycetes possess systems of vegeta- tive incompatibility, which require identical alleles at several vegetative incompatibility (vic) loci in order for the fungi to maintain heterokaryons after fusing hyphae during plasmogamy (Glass et al., 2000). Vegetatively incompatible strains produce a barrage reaction upon plasmogamy, killing the heterokaryotic hyphae. Somatic origin of hybrid Neotyphodium species required plasmogamy without a_ barrage response, and the chance that two different species would have identical alleles at several vic loci seemed remote. An investigation of vegetative compatibility between Epichloë species indicated that this classical vegetative compatibility system does not operate in the genus (Chung & Schardl, 1997b). Therefore, heterokaryons could form and represent the first step in hybridization. However, subsequent fusion of nuclei (karyogamy) was also required to give the heteroploid nuclear genotypes that typify hybrid epichloae, and no such events were detected. Furthermore, experimental coinfections of host grass- es with two different epichloae have not yet yielded demonstrable hybrids. Instead, the typical observation is that the fungal strains segregate from one another in different tillers of the plant (Wille et al, 1999; Christensen et al., 2000). The difficulty in producing interspecific hybrids experimentally begs the question, why are such hybrid epichloae so common? One possibility is that they occur in circumstances that are atypical of the experimental conditions. For example, perhaps they occur only in the developing seed when it becomes superinfected by two epichloae, one from the maternal parent, and the other from an ascospore that infected the floret. It may be that some unknown peculiarity of development in the seed makes plasmogamy more likely there than in other plant tissues. Alternatively, the hybridizations may be extremely rare, but hybrids are strongly selected. It is worth considering that as host plants evolve, their symbionts may also need to evolve in response, or otherwise lost. The evolutionary potential of a clonal fungus is far less than that of a sexual fungus, so the parasexual process of hybridization may be necessary to facilitate sufficiently rapid evolution of the otherwise clonal fungus. It is also noteworthy that many of the associated are polyploids that arose by grasses interspecific hybridization, though there is no clear association of polyploid hosts and hybrid epichloae- Finally, the parasexual cycle might counteract the progression of deleterious mutations, which is expect- ed on the basis of Muller's ratchet (Moon et al., 2004; Volume 97, Number 4 Schardl 2010 i - Epichloae, Symbionts of the Podideae uninfected Lo L eS VB nec v r y Vite " | == zt | infected Wes plan Cian cohabit plant tissue fungus species 2 Et fertilized stroma ^ Y hybrid of ' species 1 x species 2 Figure 5. Proposed scenario for the origin of hybrid epichloae. Ascospores produced by an Epichloë species may infect I A 1 e 4 x ts (left) p z ls p 1 J pl i. E t epichloé sy is t (right). In this scenario, hybridization is assumed to occur early in the superinfection before the symbionts can segregate from one lers. n h another in different host tillers There are three curious but unexplained patterns in one species of vertically transmissible epichloae, but at relationships of epichloae and their hosts. One is that most one of these is nonhybrid and the others are interspecific hybrids. So, for example, Festuca arizonica Vasey is a host for the hybrid N. tembladerae Cabral € J. F. White and the nonhybrid N. huerfanum (J. F. White, G. T. Cole & Morgan-Jones) A. E. Glenn, C. W. Bacon & R. T. Hanlin (Moon et al., 2004; Sullivan & t species may possess either vertically transmissi- ble epichloae or the more pathogenic strains that are not vertically transmitted, but rarely both. Hence, the Epichloé strains infecting Anthoxanthum odoratum L; Brachypodium pinnatum, Bromus erectus, Dactylis glomerata, Glyceria striata, Holcus lanatus L., Phleum Faeth, 2008) (Fig. 4). Finally, the two or three pratense L., Poa sylvicola Guss., and Poa trivialis almost identifiable anc of each hybrid Neotyphodium completely prevent seed production on infected plants; species are from different, well-separated phylogenetic their vertical transmission has not been observed; and clades (Fig. 4). As more isolates are surveyed, more no vertically transmitted Epichloë or Neotyphodium exceptions to these pattems may be found, but the species have been observed in any of these hosts (aside fact that they are evident among the many epichloae from Acremonium chilense, which may be vertically studied to date suggests that these patterns reflect transmissible in D. glomerata [Morgan-Jones et al., biological phenomena. Although these phenomena 1990] but is not closely related to Epichloé species). The have yet to be fully elucidated, it seems likely that exception is Lolium perenne, in which N. lolii isa they must reflect aspects of selection on the systems. common, vertically transmitted symbiont, whereas E. For example, I speculate that the highly pathogenic typhina is much rarer and not vertically seed Epichloë species select for a form of resistance in a transmissible in this host (Leuchtmann & Schardl, their hosts such that the plants cannot support verti- a 1998). Second, host grass species | x. cal transmission, whereas less pathogenic epichloae Annals of the Missouri Botanical Garden provide less selection against, or even selection favoring, vertical transmission. CONCLUDING REMARKS The plant-associated Clavicipitaceae present a rich variety of experimental material to investigate the mechanisms and evolution across an ecological mem ier. SERU ämadonistic symbiosea, y sim ple caesia, because they vary in relative bein or capabilities of the clavicipitaceous fungi to produce toxins that deter or kill - These characteristics appear key to the evolution of mutualism commonly, grass symbioses asexual epichloae Me species), vertical transmission is highly efficient and is the ec rtically transmitted symbionts favors host benefits (Ewald, 1987). Such protective mutualisms have evolved more than once in the Clavicipitaceae, which also include vertically transmitted, ergot alkaloid— ucing symbionts of Ipomoea and Turbina species (Convolvulaceae). Many other Clavicipitaceae share characte eristics of the epichloae in that they infect plants me ater but cause no damage to most infected ti —. empezo Nd d estu d vicipitaceae, including the verti transmis- sible Balansia hypoxylon, most eis as the symbionts of Ipomoea and Turbina ina species can transmit — without AUN host development. 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Tul. Trans. Brit. mera Soc. x Schardl, C. L. 2001. —— eie mutualistic of grasses. Fung. Genet. B 33: 69-82. » London, doi: 10.1002/ Shap onlinelibrary wiley wiley accessed 22 22 September 2010. TE — A. Leuchtmann, H. F. Tsai, M. A. Collen , D. M. Watt & D. B. Scott. 1994. Origin of a f ungal symbiont of perennial a by interspecific hybridizatio of à typhina. eT 136: 1307-1317. o : K-R. Chung, D. Penny & M. R. Siegel. 1997. 9T80470015902.0001: 324, Sullivan, T. J. & D. Craven, S. Speakman, A. Strombe i e & R. Yoshida. 2008. A novel test for host- simia codivergence we pon ancient origin of fungal ndophytes in grasses. Syst. B 7: 483—498. See, M. A. & C. L. Schardl. 2007. Fungal endophytes of Hybrids rescued by vertical transmission? An ends perspective. eg Phytol. 173: 452 G , L. P. Bush, F. F. Fannin, lid ade mulation and aphid response. J. Chin. Ecol. 16: 1-3315. e R. J. & J. I. Davis. 1998. Phylogenetics and ter evolution in the grass family (Poaceae): Sila taneous analysis of morphological and chloroplast DNA restriction site character sets. Bot. Rev. 64: 1- 85 Spatafora, J. W., G. H. Sung, J. M. Sung, N. L. Hywel-Jones & J. F. T 2007. Phylogenetic evidence for an animal gin of — and the grass endophytes. Molec. Ecol. 16: 1701- 174 Steiner, U., M. A. A A. Markert, S. Kucht, d GroB, N. Kauf. a aie. € EET of a seed vanemited deii pitaceou. urring on dicotyl s plants (Convolvulaceas) Plasa 224: 533—544 ivan, R., M. S. Bergen, R. Patel, G. F. Bills, S. C. Alderman, J. W. Spatafora & J. F. White. 2001. Features and phylogenetic status of an enigmatic d: fungus Neoclaviceps monostipa gen. et sp nov. Mycologi 93: Sullivan, R. F., G. F. Bills, N. L. Hywel-Jones & J. F. White Jr. 2000. Hyperdermium: A new clavicipitalean genus for some apical epibionts of donde plants. Mycolo- gia 92: 908-918. S. H. Faeth. 2008. Local adaptation in Festuca arizonica infected by hybrid and nonhybrid eotyphodium endophytes. Microbial Ecol. 55: 697—704. Sung, G. H., N. L. oe J. M. Sung, J. J. Luangsa- lora & J. W. Spatafora. 2007. Phylogenetic classification of f Cordyeeps id the clavicipitaceous fungi. Stud. Mycol. 57(1): 5— an & J. F. White. e le of water in spre conidia of the Neotyphodium endophyte of Poa Mycol. Res. 111: 466-472 Tanaka, A., B. A. Tapper, A. Ner E. J. Parker & B. Scott. A symbiosis expressed non-riboso peptide from a mutualistic fungal endophyte " perennial ryegrass confers protection to the symbiotu LM insect ipid Molec. Microbiol. 57: 1036-1050. Tanaka, E. & C. 2008. Phylogenetic study of clavicipitaceous c using —À € dehydrogenase sequences. Wie 49- 115-125. » — ———, À. Gafur & M. Tsuda. 2002. Heteroepichloë, et nov. (arapiscese: Ascomycotina) on bamboo ia. Mycoscience 43: 87— TePaske, M. R., R G. Powell & S. L. Clement. 1993. yses of selected oS ow for the and ergot-type alkaloids. J. Agric- H. Bouton. 2005. Response of atylenchus spp. in tall fescue infected with different strains of the fungal endop yte Neotyphodium coenophia - Nematology 7: 105—110. Volume 97, Number 4 2010 Schardl Epichloae, Symbionts of the Poóideae 665 . F., J. S. Liu, C. Staben, M. J. Christensen, G. Latch, R. Siegel & C. L. Schardl. 1994. “ses nisi dreiit cation of fungal endupkiytes of tall fi by h D "o Epichloë species. Proc. Natl. bu. ‘US. 2546. Tsai, H White, J. F. i As] Endophyte-host associations in XIX. A systematic study of some — patric species of p. in Uu. ior lo & P. V 1996. Examination ui structure ond ] lar iilii in genera Epichloë and Porepichlos. Mycologia 90: saaw orrow, G. Morgan-Jones & D.A. € - 1991. Enh host Primary stromata formation and seed transmission in Epichloé "E Developmental and regulatory aspects. Mycologia 83: 72-81. Wilkinson, H. H., M. R. Siegel, J. D. Blankenship, A. x Malam LN Bush & C. L. Schardl. 2000 2000. Cor im. e mutualism. Molec. Pl.-Microbe niin 13: 1027-1033. Wille, P. A., R. A. Aeschbacher & kbd didi oio sedile b bab infected host grasses. Plant J. 18: 349-358. Yan, K., J. Yanling, S. Xianghui, Z. Lihui, L. Wei, Y. Hodie & W. Zhiwei. 2000. Tax axonomy of Neot Sy terc 101: 211-219. Je aor. MN P MA E TN NN GL Schardl & : Indole-diterpene — capability of ' Epichlot endophytes as predicted by lim gene analysis. Appl. Environm. Microbiol. 75: 2200- 2211. ANNALS OF THE MISSOURI BOTANICAL GARDEN VOLUME 97 2010 Volume 97, Number 4 667 Colophon This volume of the ANNAIS of the Missouri Botanical Garden has been set in APS Bodoni. The text is set in 9-point type while the figure legends and literature cited sections are set in 8-point type. This volume has been printed on 60# Opus Gloss Reeycled No. 2. This is an acid-free paper designed to have a shelf-life of over 100 years. Sra ao used in the ANNALS are reproduced using 300 line screen halftones. 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L] Maps include reference to D and longitude and are bounded by a fine bo C] Scanning electron uo x: are free of conspicu- ous c ing. C] Axes on graphs are all labeled. L] Captions provide all explanatory text. Captions are separate from other text, one paragraph for each group of figures, and following the style in current issues of the Annals. CJ Symbols on maps are e and reduction has been taken into consideration Author Index: Annals of the Missouri Botanical Garden Vol. 97! A Albert, V. A. see Scheen et al. 191-217 Ames, M. see Givnish et al. 584—616 Armesto, J. J. see Salinas et al. 117-127 Arroyo, M. T. K. see Salinas et al. 117-127 B Baeza, M. see Linder et al. 306—364 Barker, N. P. see Linder et al. 306—364 Bell, C. D. see Soltis et al. 514—526 Bendiksby, M. see Scheen et al. 191-217 Beseda, L. see Mayer & Beseda. 106-116 Bove, C. P. see Philbrick et al. 425—456 Boyce, C. K., J.-E. Lee, T. S. Feild, T. J. Brodribb & M. A. Zwieniecki. Angiosperms Helped Put the Rain in Rainforest: The Impact of Plant oe Evolution on Tropical Biodiversity, 5 Briggs, B. G. see Givnish et al. ae Brodribb, T. J. see Boyce et al. 527—540 Burleigh, J. G. see Soltis et al. 514—526 6 Chiapella, J. & F. O. Zuloaga. A Revision of Deschampsia Avenella, and Vahlodea (Poaceae, Poeae, Airinae) in South America, 141—162 Chung, K.-F., H. van der Werff & C.-I Peng. Observations on the Floral Morphology of Sassafras ra (Laur- aceae), 1-10 Crayn, D. M. see Wagstaff et al. 235-258 D Dawson, M. I. see Wagstaff et al. 235-258 , S. S., O. Morrone & F. O. Zuloaga. Estudios en el unta Paspalum (Poaceae, Panicoideae, Paniceae): Paspalum m y Especies Afines, 11-33 dePamphilis, C. W. see qu et al. 584-616 Ding, B.-Y. see Jin et al. 1 Duvall, M. R. see Givnish et 584-616 E Endress, P. K. Flower Structure and Trends of Evolution in Eudicots and Their n eee 541-583 Escobar, A. see Sede et al F Feild, T. S. see Boyce et al. 527-540 Fine, P. V. A., R. García-Villacorta, N. C. A. Pitman, I. Mesones & S. W. Kembel. A Floristic Study of the White-sand Forests of Peru, 283-305 1 97(1) pp. 1-140, 97(2) pp. 141-282, 97(3) pp. 283—468, G Galley, C. see Linder et al. 306-364 Garcia-Villacorta, R. see Fine Givnish, T. J., M. Ames, J. R. McNeal, M. R. McKain, P. R. ilis, S. W. Graham, J. C. Pires, Duvall, M. J. Moore, J. M. rH D. E. Soltis, P. S. (Iytkeabeask, Including Haitia from Hispaniola, 34-90 Graham, S. W. see Givnish et al. 584-616 H Heaney, J. M. see Givnish et al. 584-616 Hong, D.-Y. see Jin et al. 163-190 Humphreys, A. M. see Linder et al. 306-364 Jin, X.-F., B.-Y. Ding, Y.-J. Zhang & D.-Y. Hong. A Taxonomic Revision of Rhododendron subg. T: sect. yx (Ericaceae), 163-190 K Kelly, D. L. see Ulloa Ulloa et al. 457-467 Kembel, S. W. see Fine et ue Kiehn, M. of Neotropical Rubiaceae. I: Rubioideae, 91-105 E Labandeira, C. e n edi bene 469-513 Lee, J.-E. see Boyce et al. 527-540 Leebens-Mack, J. H. see Givnish et al. 584-616 K. L. see vera x ea H. P., M. Baeza, N. P. Barker, C. Galley, A umphreys, K. M. Tug A. Orlovich, M. D. an B. K. Simon, N. Walsh & G- A. V Verboom. A Generic of the Danthonioideae (Poaceae), 306- 364 Lindqvist, C. see Scheen et al. 191-217 Lloyd, K. M. see Linder et al. C. see Scheen et al. 191-217 Mayer, M. S. & L Reconciling Taxonomy and Phylogeny in the glandulosus Complex (Brassicaceae), 106-116 97(4) pp. 469-677. 672 Annals of the Missouri Botanical Garden McKain, M. R. see Givnish et al. 584—616 McNeal, J. R. see Givnish et al. 584—616 , L see Fine et Moore, M. J. see Soltis et al. 514—526 Moore, M. J. see Givnish et al. 584—616 Morrone, O. Morton, C. M. és Vinee et al. ee Máúlgura, M. E. see O'Leary et al Munzinger, J. see Wagstaff et et al. 235 N Nickrent, D. L. see Ulloa Ulloa et al. 457-467 0 O'Leary, N. M. E. Múlgura & O. Morrone. Revisión ro Verbena (V Orlovich, D. A. see Linder et al. 306-364 P Peng, C.-I see Chung et al. 1-10 Philbrick, C. T., C. P. Bove & H. I. Stevens. Endemism in Neotropi 425—456 Prance, G. T. see Yakandawala et al. 259-281 R Remizowa, M. V., D. D. Sokoloff & P. J. E Evolutionary History of the Monocot Flower, 617-64. Rudall, P. J. see Remizowa et al. 617-645 Ryding, O. see Scheen et al. 191-217 3 Salinas, M. F., M. T. K. Arroyo & J. J. Armesto. Epiphytic Growth Habits of Chilean Gesneriaceae and the Evolution of Epiphytes Within the Tribe Coronanther- eae, 117-127 Schardl, C. L. ue Epichloae, Symbionts of the Grass Scheen, A-C., ^ Bendiksby, O. Ryding, C. Mathiesen, v. A. Albert & C. Lindqvist. Molecular Phylogeneti and ric Classifi Betis e a A. Escobar, O. Morrone & F. O. Zuloaga. Studies in American Paniceae (Poaceae, aura 128-138 Simon, B. K. see Linder et al. 306-364 Sokoloff, D. D. see Remizowa et al. 617-645 Soltis, D. E., M. J. Moore, J. G. rene C. D. Bell & P. M. Soltis. E the Angiosperm Tree of Life: uture uber Lo Soltis, D. E. see vidua et al. 584—6 Soltis, P. S. see Soltis et al. om Soltis, P. S. see Givnish et al. 584—616 eane, D. A. see Wagstaff et al. 235-258 Steele, P. R. see a et al. 584—616 Stevens, H. I. see Philbrick et al. 425—456 Stevenson, D. W. see Givnish et al. 584—616 T Thiele, K. see Givnish et al. 584—616 U Ulloa Ulloa, C., D. L. Nickrent, C. Whitefoord & D. L. Kelly. Hondurodendron, a New Monotypic Genus of Aptan- draceae from Honduras, 457—467 van der Werff, H. see Chung et al. 1-10 Venter, S. see d et al. 235-258 Verboom, . see Linder et al. 306-364 Wagstaff, S. J., M. I. Dawson, S. Venter, ES D D. M. yn, D. A. Steane & Origin, Diversification, and e el of pia Ta Genus Dracophyllum (Richeeae, Ericaceae), 235— Walsh, N. see Linder et al. 364 Welzen, P. C. van. Revision d the Asian Genus Koilodepas erica 218- Whitefoord, C. see Ulloa i et al. 457-467 x. Yakandawala, D., C. M. Morton & G. T. Prance. Phylogenetic Relationships of the Chrysobalanaceae Inferred from Chloroplast, Nuclear, and Morphological Data, 259- 281 Zhang, Y.-J. see Jin et al. 163-190 Zomlefer, W. B. see Givnish et al. 584-616 28-138 Zuloaga, F. O. see Chiapella . Zuloaga. 141-162 Zwieniecki, M. A. see Boyce et al. 527-540 Subject Index: Annals of the Missouri Botanical Garden Vol. 9712 caceae, 61 Argentina, 141-162 Asia. see also specific countries 90 Axonopus andinus, 128-1 Axonopus iridifolius, 128-138 B A par nica, 191-217 e neige 62 Borneo, 218-234 Bracteosae, 365—424 Brassicaceae, 106—116 Brazil, 141-162, 425-456 Bromeliaceae, 584-616 C . 306—364 Copochiia. arundinacea, 306-364 Capeochloa cincta, 306-364 s . sericea, Capeochloa setacea, 306-364 Caribbean, 34-90 1 97(1) pp. 1-140, 97(2) pp. 141-282, 97(3) pp. 283-468, 97(4) "The ject index was compiled from volume 97 abstrac Caytonia, 469-513 Centrolepidaceae, 584-616 Ci 1 457—467 Chile, 117-127, 141-162 Andes, 141- Chiloé Island, 117-127 Chimaerochloa, 906-364. China, 163-190, 218-234, 469-513 Chry , 259-281 oel , 218-234 Coronanthereae, 117—127 Cortaderia, 306-364 Cortaderia hieronymi, 306-364 i iana, 306-364 Dracophyllum milliganii, 235-258 E Ecdeiocoleaceae, props Echinochloa, 128— Epacridaceae. pp- 469-677. words. ts and key 674 Annals of the Missouri Botanical Garden G Latin America, 425—456. see also specific countries Lauraceae, Geochloa decora, 306—364 Lawsonia, 34—90 Geochloa lupulina, 306-364 Leonureae, 191-217 rufa, Leucadeae, 191-217 Gesneriaceae, 117—127 Leucas, 191-217 Gesnerioideae, 117-127 Lythraceae, 34-90 34-90 sect. Discospermum, 34—90 M Ginoria americana Malesia, 218-234 var. spinosa, H- Marrubieae, 191-217 Ginoria buchii, 34-90 Mayacaceae, 584-616 Ginoria curvispina, 34-90 Merxmuellera, Ginoria davisii, 34-90 Merxmuellera grandiflora, 306-364 Ginoria jimenezii, 34-90 ospermae, 51 ia lanceolata, Mexico, 34— Ginoria pulchra, 34-90 Mitraria, 117-127 Ginoria spinosa, 34-90 Mitraria coccinea, 117-127 Gomphostemmateae, 191—217 Mo N Haitia, 34—90 Harmandia, 451—467 Hirtelleae, 259-28] Hispaniola, 34-90 Honduras, 457-467 457-467 n urceolatum, 457-467 Hymenachne, 128-138 I India, 218—234 Indochina, 218-234 Neotropics, 91-105 Neotyphodium, 646-665 Nesaea, New Caledonia, 235-258 New Guinea, Olacaceae, 457-467 Ongokea, 457-467 Paniceae, 11-33, 128-138 Panicoideae, 11-33, 128-138 Volume 97, Number 4 2010 675 Pentameris atroides Pentameris caulescens, 306—364 Pentameris chispindallide. 306—364 Pentameris chrysurus, 306—364 Pentameris clavata, Pentameris colorata, 306—364 ris insularis, fuut juncifolia, 306—364 Pentameris ipes, 306-364 Pentameris malouinensis, 306-364 Pentameris microphylla, 306-364 entameris pusilla, 306—364 Pentameris pyrophila, 306—364 Pentameris reflexa, viac 6 Phlomideae, 191-2 Poaceae, 11—33, T 141-162, 306—364, 646-665 Podostemaceae, Poeae, 141— P Pogostemoneae, 191-217 Pogostemonoideae, 191-217 646-665 R Rapateaceae, 584-616 Restionaceae, 584-616 ndron Rhodode sect. Brachycalyx, 163-190 subg. Ts i Rhododendron dilatatum var. leucotric 190 Rhododendron mariesii, 163—190 Rhododendron 163-190 n 163-190 Richea, 258 sect. Cystanthe, 235—258 sect. ides, 235-258 Richeeae, 235— Rosaceae, 259-281 Rosidae, 514—526 676 Annals of the Missouri Botanical Garden Setaria tenacissima, 128-138 Sideritis, 191-217 th America, 117-127, 141-162. see also specific countries , 235-258 Stachydeae, 191-217 Stachys, 191-217 Streptanthus, 1 peramoenus, 106—116 Sumatra, 218-234 Synandreae, 191-217 ibolium, 306—364 Tribolium curvum, 306—364. Tribolium pleuropogon, 306—364 Typhaceae, 584—616 U United States California, 106—116 Urochlaena, 306—364 V Vahlodea, 141—162 s 24 ser. Pachystachyae, 365—424 V. , 365-424 ser. Ve Verbena teata, 365—424 var. brevibracteata, 24 Verbena carolina, 365—424 Verbena domingensis Verbena ehrenbergiana, 365-424 Verbena gracilescens var. swiftiana, 2 Verbena hastata, 365-424. Verbena hirsuta, 4 Verbena lasiostachys, 365—424 Verbena officinalis, 24 var. gracilescens Verbena riparia, Verbena roemeriana, 365—42. Virgin Islands, 34-90 X Xyridaceae, 584-616 Volume 97, Number 1, pp. 1-140 of ANNALS OF THE MISSOURI BOTANICAL GARDEN was published on 31 March 2010. Volume 97, Number 2, pp. 141-282 of ANNALS OF THE MISSOURI BOTANICAL GARDEN was published on 9 July 2010. Volume 97, Number 3, pp. 283-468 of ANNALS OF THE MISSOURI BOTANICAL GARDEN blished Volume 97, Number 4, pp. 469-677 of ANNALS oF on 8 October 2010. THE MissOUR1 BOTANICAL GARDEN was published on 27 December 2010. t WERT . 9 1753 www.mbgpress.org sz s ae Sa DUE OR aad TS oh qus d. EX "E