MUNnruBRAAY lit MRffU. HALL f^Bo 71995 UNlvtRSITY OF ILLINOIS LIBRARY AT URBANA-CHAMPAIGN BIOLOGY H8 01^995 V t lale External Genitalia of Non-Prehensile ailed South rican Monkeys. irt I. Suhfamilv PithoHinae, Fam^Kr r'pbidae 'tlvc FIELDIANA Zoology NEW SERIES, NO. 73 Male External Genitalia of Non-Prehensile Tailed South American Monkeys. Part I. Subfamily Pitheciinae, Family Cebidae Philip Hershkovitz Curator Emeritus Division of Mammals Department of Zoology Field Museum of Natural History Chicago. Illinois 60605-2496 Accepted March 30, 1993 Published September 30, 1993 Publication 1451 PUBLISHED BY FIELD MUSEUM OF NATURAL HISTORY © 1993 Field Museum of Natural History ISSN 0015-0754 PRINTED IN THE UNITED STATES OF AMERICA Table of Contents List of Illustrations Abstract I Introduction 1 Material 1 Measurements 2 Abbreviations 2 PiTHECiiNE Characters 2 Generic Characters 2 Pithecia Desmarest (Sakis) 2 Chiropotes Lesson (Bearded Sakis) 2 Cacajao Lesson (Uacaries) 2 Species Descriptions 3 Pithecia pithecia Linnaeus 3 Pithecia monachus E. Geoffroy 4 Pithecia irrorata Gray 6 Pithecia aequatorialis Hershkovitz 6 Pithecia albicans Gray 6 Chiropotes albinasus \. Geoffroy 6 Chiropotes satanas Hoffmannsegg 6 Cacajao melanocephalus ouakary Spix .... 9 Cacajao calvus \. Geoffroy 9 Cacajao calvus rubicundus \. Geoffroy and Deville 12 Morphology and Phylogeny 13 Baculum 13 Penile Shaft 13 Scrotum 14 Spines 14 Sexual Behavior 14 Conclusions 15 Acknowledgments 16 Literature Cited 16 1 . External genitalia of Pithecia pithecia 4 2. Bacula of three species of P/7Aeaa 5 3. Penis of Chiropotes albinasus 7 4. External genitalia of Chiropotes satanas . . 8 5. Penis of Cacajao melanocephalus 10 6. External genitalia of Cacajao calvus 11 List of Tables 1. List of described external genitalia 3 2. Pitheciine penile forms 3 ui Male External Genitalia of Non-Prehensile Tailed South American Monkeys. Part I. Subfamily Pitheciinae, Family Cebidae Philip Hershkovitz Abstract External male genitalia of the three pitheciine genera appear to be uniquely designed for direct delivery of sjjerm into the uterus. Described is the gross anatomy of five of the six sjjecies of Pithecia and the two each of Cacajao and Chiropotes. The shaft in pitheciines is evenly tap)ered to tip, subtriangular in cross section, curved upward in some, downward in others with cant to right or left, labile glans undifferentiated from shaft, meatus bordered by erectile lappets. Penile shape, curvatures and glans accessories facilitate coupling of the meatus with the uterine cervix and possible direct transfer of SF>erm into the uterus. The baculum of each SF>ecies of Pithecia is distinctive, the penile spines minute. Remaining pitheciines lack a baculum but have large, hooked p)enile spines. Hypertrophied penile spines of Chiropotes and Cacajao may lock into the vagina after in- tromission and/or open a passage through ejaculates of previous multimale copulations. The little that is known of pitheciine sexual and social behavior is recorded. Introduction Material External male genitalia of pitheciines (Pitheci- inae, Cebidae) are among the least studied of pri- mate reproductive organs. Known heretofore are descriptions of the external genitalia of one sj^ec- imen each of a Pithecia pithecia and a Cacajao rubicundus by Hill (1958, p. 645, 1960, pp. 184, 226, 227 with figure) and of Cacajao calvus by Fontaine and Du Mond (1977, pp. 201, 203). The present account describes the male external genitalia of all but one (Pithecia albicans) of the nine known species of the three genera of Pithe- ciinae, and the system that seems to have evolved for direct sperm transfer from penis into uterus. Notes on social organizations are included. Most recent taxonomic revisions of the genera are by Hershkovitz. They are those of bearded sakis, ge- nus Chiropotes (1985), uacaries, genus Cacajao (1987a), and sakis, genus Pithecia (1987b). Gen- italia and sexual behavior were not considered in these revisions. Thirty-eight male external genitalia are de- scribed (table 1 ). Of these, 1 2 are entire, that is, with intact penis, scrotum, and surrounding in- tegument, fixed in formalin, and preserved in al- cohol. The remaining 26 arc terminal ends of Ire- nes excised from dry museum skins, hydrated, cleared in 2—4% potassium hydroxide (KOH), and stained with alizarin to reveal the baculum, if any. The cleared penes are gelatinous in texture, tu- mescent as in erection, but often bloated. Adorn- ments such as lappets surrounding the urinary me- atus are usually swollen as in erection. Furrows— The integument of nearly all penes examined is evenly furrowed all around. In con- trast, penile skin of the live or freshly killed animal is loose, wrinkled, or folded without suggestion of furrows or corrugations or indication of tendency toward their formation. Perhaps the differential responses of skin and underlying tissues to fixation and/or chemical clearing combine to produce fur- HELDIANA: ZOOLOGY, N.S., NO. 73, SEPTEMBER 30, 1993, PP. 1-17 rows. In a casual inspection, furrows were noted in similarly prepared and preserved penes of Ateles, Cebus, and Macaca. Measurements Intact and extended penes were measured from base at scrotal margin to tip of glans. Full length of a completely erect penis in the live animal is conjectural but may be approximated by those of some cleared specimens. However, most de- tached, cleared penes, including glandes, used in this study are less than half of full length. Their measurements are included nevertheless in the de- scriptions. Greatest length of each baculum is giv- en. Body size dimensions given for species and specimens examined serve as bases for estimates of proportional size of external genitalia. The di- mensions used are means and extremes of com- bined head and body length (HB), greatest skull length (GSL), and weight in grams (W). Measure- ments for the species are from Hershkovitz (1985, 1987a,b). Those of individual animals are from the original data sheets. Abbreviations side of midline; glans undifferentiated from shaft by nonexpansion or nonconstriction at neck; uri- nary meatus a vertical or medioventral slit, its borders swollen with an extensile or erectile lappet distally, another proximally; p>enile spines minute in Pithecia, large in Cacajao and Chiropotes. Body size of each of the five species of Pithecia is approximately equal. Size of each of the two species of Cacajao average larger, and that of each of the two species of Chiropotes is largest. Generic Characters Pithecia Desmarest (Sakis) (figs. 1, 2; tables 1, 2) Genitalia of 4 available of the 5 known species appear to be similar. Scrotal sac is pigmented, skin glandular, the glands not always visible to the unaided eye, testes descended, penis arising from anterior scrotal margin curved downward or pos- teriad, longitudinal axis of shaft convex or concave dorsally, concave or convex ventrally, cross sec- tion subtriangular with apex dorsal, shaft canted right or left, spines extremely minute. Baculum present in 2 of 4 cleared penes of P. pithecia, 1 of 2 P. monachus, the single P. aequatorialis, and absent in the single P. irrorata (table 2). AMNH American Museum of Natural History, New York FMNH Field Museum of Natural History, Chi- cago MPEG Museu Paraense Emilio Goeldi, Belem RNHMS Royal Natural History Museum, Stock- holm Pitheciine Characters Male external genitalia of the three genera of Pitheciinae exhibit increasing specialization from those of Pithecia to those of Cacajao and Chiro- potes. Shared characters include scrotum sessile, parapenial, skin glandular with thin covering of pale hairs; testes subequal in size, descended in young and adults, retractable in both; baculum small, or absent in Pithecia, absent in Chiropotes and Cacajao; penis tapered to tip, subtriangular in cross section and more or less canted to either Chiropotes Lesson (Bearded Sakis) (figs. 3, 4; tables 1, 2) Scrotum almost entirely unpigmented, skin vis- ibly glandular; testes descended but presumed re- tractable in all 8 available specimens including those of 5 young; longitudinal penile axis of Chi- ropotes satanas usually concave dorsally, convex ventrally as in Cacajao calvus, subtriangular in cross section with apex dorsal; penile shaft curved or canted left or right touching scrotum; shaft of C albinasus with convexity and apex of cross sec- tion dorsal as in Pithecia pithecia; baculum absent in both species. Cacajao Lesson (Uacaries) (figs. 5, 6; tables 1, 2) The single available scrotum of a mature C. cal- vus calvus is entirely pigmented, the skin without macroscopically detectable glands; penis projected FIELDIANA: ZOOLOGY Table 1. Male external genitalia described in this study. Intact genitalia include scrotum, penis, and part of perineum. Taxon Cleared penis Bacuium Intact only (mm) Pithecia pithecia Pithecia monachus Pithecia irroratus Pithecia aequatorialis Chiropotes albinasus Chiropotes satanas Cacajao calvus Cacajao melanocephalus 2 4 1.5; 3.0 2 2 1 1 2.5 1.5 8 1 10 — 3 _ — 4* _ * Three decomposed. from inguinal border of scrotum curved upward or anteriad, with a 30° twist or cant to right; lon- gitudinal axis of shaft variable, cross section sub- triangular with apex ventral; curvature of two cleared partial penes of C. calvus equivocal; penis and prepuce invested with large, grappling spines; bacuium absent in cleared penes, not palpable in untreated specimens. Cleared shaft of Cacajao melanocephalus (fig. 5) is convex dorsally, concave ventrally as in Pi- thecia, subtriangular in cross section, apex dorsal; spines larger and thicker than those of C calvus, but this may be individually variable; bacuium absent. Species Descriptions Noteworthy interspecific differences among adult genitalia of congeneric species, bacula excepted. are not apparent. Because of the fragmentary na- ture of most of the cleared penes used to increase sample size, the description of parts of one spec- imen may be applied to missing parts of other specimens of the same species. Body size dimen- sions are given under each species heading; mea- surements of individual animals follow their reg- istry number. Pithecia pithecia Linnaeus (figs. la,b) SiZE-HB = 363(330-395)9; GSL = 80.6(77.4- 82.7)16; W = 1.740(1,380-1,866)9. Specimens— Six, including two intact external genitalia and four partial penes detached from dry museum skins, cleared, stained, and preserved in glycerine. FMNH 95504 (HB = 348; GSL = 79.4) -Scro- tum pear-shaped, greatest transverse diameter about 2 1 mm, wrinkled skin pigmented except the broadly distributed unpigmented or mottled ovate skin glands each with a triad of long brown hairs projecting from a minute pore; penis, issuing from anterior scrotal margin, mottled brownish except unpigmented borders of meatus; longitudinal axis of shaft slightly convex dorsally, concave ventral- ly, inclined or canted left; rounded glans undiffer- entiated from shaft but slightly wider on ventral than dorsal surface; meatus a 3-mm medioventral slit, its expanded ventral border with swollen tri- angular lappet, dorsal border with conical lappet, each lateral border with paired Iapp)ets; minute spines of shaft or glans not detectable macroscop- ically; bacuium if present not palpable. FMNH 95505 (HB = 349; GSL 79.6) (figs. Ia,b)- Scrotum more or less pear-shaped, greatest trans- Table 2. Pitheciine penile forms of shaft (not all features completely determinable in some specimens). I^ength wise N dorsal surface Apex Cant Taxon Convex Concave Dorsal Ventral Left Right Pithecia pithecia 6 4 2 3 Pithecia monachus 4 2 1 1 — — 3 Pithecia irrorata 1 1 — 1 — 1 — Pithecia aequatorialis 1 — 1 1 — 1 — Chiropotes albinasus 1 1 — I — 1 — Chiropotes satanas 18 l*;3t 8 8 — 4 9 Cacajao calvus 3 1* 1 — 3 — 3 Cacajao melanocephalus 4 1 - 1 — 1 — Totals 38 14 11 15 3 11 15 * Glans twisted, t Juvenals. HERSHKOVITZ: SOUTH AMERICAN MONKEYS PITHECIA PITHECIA =2min evident macroscopically; baculum if present not palpable. FMNH 93251 (HB = 375; GSL = 78.7) (fig. 2c)- Cleared unpigmented glans with fully developed tenpin-shaped baculum imbedded above meatus, its base subtriangular, greatest length, ca. 1.5 mm. FMNH 93232 (HB = 360; GSL = 81.6)-aeared unpigmented penile fragment 5-6 mm long, sur- face furrowed, covered with nodular based minute spines; baculum in dorsal portion of tip 3 mm long, shape not clearly defined but seemingly like preceding; dorsum of shaft convex, cant left. FMNH 50882 —Cleared unpigmented penile fragment about 1 7 mm long, shaft with dorsal sur- face convex, narrower than concave ventral sur- face; swollen horseshoe-shaped meatal borders as in preceding; shaft furrowed, with minute nodules each with spine; cant right; baculum absent. FMNH 95507 (HB = 345; GSL = 76.7) -Skin of cleared pigmented glans and fragment of furrowed shaft with minute nodules each with macroscop- ically invisible spines; dorsal surface convex, broader ventral surface concave, cant left; meatal borders swollen; baculum absent. Hill (1958, I960)— The description of external genitalia of an undetermined species of Pithecia does not mention a baculum. A subsequent report of the genitalia by Hill (1960, p. 184, fig. 34) de- scribes the baculum o^ Pithecia pithecia as a "short (2.0 mm) pyramidal nodule, 1.75 mm in diameter at base, triangular in dorsal view, with a medial dorsal keel, and a pair of alai directed downwards and lateral enclosing a ventral concavity which encloses the fossa navicularis of the urethra." The accompanying figure is unlike adult bacula of Pi- thecia pithecia at hand, but the description in text suggests an incompletely developed or abnormal bone. 1 =4mm Fig. 1 . Pithecia pithecia, external genitalia; a, intact, anteroventral aspect (fmnh 95505); b, glans of same, meatal aspect. verse diameter about 19 mm, skin less glandular than that of preceding; completely extruded penis tapered, particolored, length about 20 mm, cant left, ventral raphe continued as frenulum at base of glans; shaft with dorsal surface narrower than ventral; meatus as in preceding but with ventral lappet extruded, dorsal lapp)et receded; spines not Pithecia monachus E. GeofTroy (figs. 2a,b) SiZE-HB = 418(398^80)15; GSL = 87.2(82.1- 92.7)40; W = 2,697(2,177-3,100)8. Specimens— Four, including two intact external genitalia and two penes detached from dry mu- seum skins, reconstituted, cleared, stained, and preserved in glycerine. FMNH 122796 (HB = 405; GSL = 83.0; W = 3,000)— Pigmented scrotum with testes retracted, skin puckered, hairy cutaneous glands pro- nounced; furrowed shaft about 1 4 mm long, pig- mented, slightly tapered, spines hardly evident un- FIELDIANA: ZOOLOGY a,' •a •c .<3 I '5. a; J- 8 U UJ X ^ o ■u 3 tr (U nj UJ 0 0) x; •u is? . .. (0 I/) u c 2 HERSHKOVITZ: SOUTH AMERICAN MONKEYS der magnification, dorsum convex, cant right; baculum, if present, not palpable. FMNH 122798 (HB = 409; GSL = 84.5; W = 2,500) — Subadult, globular scrotum hardened, shrunken, its greatest diameter about 23 mm, puckered skin pigmented, triad of brown hair pro- jecting from each glandular pore; shaft nearly en- tirely pigmented, dorsum slightly convex, cant right; meatus as in P. pithecia, ventral lappet ex- truded, dorsal lappet exposed; spines not evident macroscopically; baculum if present not palpable. FMNH 25321 (GSL = 88.7)— Cleared penis ta- pered, entire length about 15 mm; width at base 6 mm, of glans 4 mm, dorsal surface convex or concave, ventral surface concave or convex, shaft subtriangular in cross section with apex dorsal, cant right; ventral and dorsal lappets swollen; mi- nute spines evident; baculum absent. FMNH 87001 (HB = 434; GSL = 81.5) (figs. 2a,b)— Cleared, partially disintegrated glans with dorsal and ventral lappets; spines if present not detectable macroscopically; club-shaped baculum near tip of dorsal lappet about 2.5 mm long (fig. 2a). Pithecia irrorata Gray SiZE-HB = 428(375^90)13; GSL = 89.4(86.1- 94.3)19; W = 2,920(1). Specimen— Cleared penis, excised from dry mu- seum skin, reconstituted, cleared, stained, and pre- served in glycerine. FMNH 98040 (HB = 419; GSL = 89.0) -Penile fragment 10 mm long, furrowed, pigmented; shaft with longitudinal axis of dorsal surface convex, ventral concave, subtriangular in cross section with apex dorsal, cant left; dorsal and ventral lappets well defined; minute spines weakly defined; bac- ulum absent. Pithecia aequatorialis Hershkovitz (figs. 2d-g) SiZE-HB = 417(394-440)4; GSL = 86.0(81.5- 89.8)4. Specimen— Cleared penile fragment from dry museum skin, reconstituted, cleared, stained, and preserved in glycerine. FMNH 86995 (HB = 394; GSL = 81.5) (fig. 2d)- Pigmented penile fragment 13 mm long consid- erably distorted, flattened, nodular skin pigment- ed, indistinctly furrowed; shaft with dorsal surface concave, ventral convex, subtriangular in cross section with apex dorsal, cant left; spines if present not detectable; dorsal and ventral lappets hardly defined in distorted, partially disintegrated glans; baculum about 1.5 mm long, subglobular with lat- eral borders redoubled forming a longitudinal sul- cus (figs. 2d-g). Pithecia albicans Gray Size-HB 465(404-560)10; GSL = 85.4(83.3- 89.2)12. Specimens— None. Dixson (1987b, p. 52) gives 1.5 mm for baculum length of the single specimen examined. Chiropotes albinasus I. Geoffrey (figs. 3a-c) SiZE-HB = 431(390-470)8; GSL = 93(90.0- 97.1)12; W = 2,487(2,200-2,720)7. Specimen— One partial penis removed from dry museum skin, cleared, stained, and preserved in glycerine. MPEG 8151 (skin without data, skull missing)— Longitudinal axis of shaft slightly convex dorsally, plane ventrally, the surface with median crest, cross section subtriangular with apex dorsal, cant left; spines large, their orientation in all directions ap- pears normal but may be an artifact of preparation and preservation (figs. 3a-c); baculum absent; fur- rows not distinct. Chiropotes satanas HofTmannsegg' (figs. 4a-d) Sizes- C. 5. chiropotes: HB = 423(370-507)20; GSL = 91.4(84.3-94.9)23; W = 2,904(2,200- 4,000)20. C. s. satanas: HB = 382(335^24)15; GSL = 86.2(80.5-92.4)16. C s. satanas: HB = 390, 440; W = 2,510, 3,000. Specimens— Eighteen, of which 8 are intact ex- ternal genitalia fixed in formalin and preserved in alcohol, the organs hard, shrunken; 10 penes ex- cised from dry museum skins, cleared, and pre- served in glycerine. FMNH 57691 (adult)— Subovate scrotum infest- ed with cuterebrid larvae, width 55 mm, skin un- pigmented except dark brown triangular patch of anterodorsal section, thinly hirsute; scrotal and perineal skin crimped, puckered; penis partially ' The name Chiropotes satanas utahicki Hershkovije (1985, p. 17) for Uta Hick (now Uta Ruempler) must take the feminine ending. It is herewith emended to Chi- ropotes satanas utahickae. FIELDIANA: ZOOLOGY 'W. w .':■•? M ^i^:^\■■'<■'■■■■^?r.''■■^■M K-d (^n ^f::^m -Dt&:V' •:•■;■:•;•.:•.■■•. 9 - >:■• ■.^'v.'.oVii =3niin CHIROPOTES ALBINASUS Fig. 3. Chiropotes albinasus (mpeg 8151; KOH preparation); a, ventral surface of shaft; b, same, right side; c, same, spines enlarged. destroyed by parasites, completely sheathed, shaft with longitudinal axis of dorsal surface concave, of ventral convex, unfurrowed circumferentially; cross section subtriangular with apex dorsal, spines large, baculum absent. FMNH 95786 (HB = 406; GSL = 93.5) -Di- ameter of scrotum about 55 mm, skin less puck- ered than that of preceding, dark brown triangular hirsute patch more extensive; greatest length of extended penis, 20 mm, exposed shaft tap)ered, furrowed, glans undifferentiated from shaft; shaft with longitudinal axis of dorsal surface deeply con- cave, ventral surface convex, cross section sub- triangular, apex dorsal; penis sharply canted left, nearly touching scrotum; longitudinal slit of me- atus about 3 mm, lateral borders swollen, ventral lappet small, dorsal lappet bulbous, protrusion about 3 mm; prepuce spiny; baculum absent. FMNH 95512 (HB = 407; GSL = 91.8) (figs. 4a- d)— Scrotum ovate, wider than long, greatest di- ameter about 45 mm, skin unpigmented except eumelanin speckling of dorsal surface proximal to p)enis, skin puckered, wrinkled, thinly covered with triads of long blond hairs each issuing from a glan- dular pore; long dark guard hairs uniformly dis- persed; anterodorsal surface of scrotum with tri- angular patch of dark brown hair, the skin speckled; scrotum divided by moderately deep sulcus an- teriad to base of penis; perineum broad, smooth, unpigmented; penis projecting from midscrotum, length about 30 mm, basal half sheathed, exposed terminal half corrugate and furrowed, cant left, the shaft nearly touching scrotum, glans pointed up- ward; hooked spines prominent, the longest about 0.6 mm; longitudinal axis of dorsal surface of shaft concave, ventral convex, subtriangular in cross section with ap)ex dorsal; baculum if present not palpable. FMNH 57692 (juv.)— Scrotal halves spread, greatest transverse diameter about 45 mm, indi- vidual testis smaller than that of preceding spec- imen; length of preputial or sheathed portion of HERSHKOVITZ: SOUTH AMERICAN MONKEYS CHIROPOTES SATANAS =10iiim =3mm y ^ *j Fig. 4. Chiropotes satanas, external genitalia of mature male; a, intact, anteroventral aspect (FM^fH 95512); b, distal portion of shaft (KOH preparation), right side (amnh 518225); c, same, ventral surface; d, same, penile spine enlarged. penis about 9 mm, curvature indeterminable but longitudinal axis of dorsal surface possibly convex; spines if present not evident, baculum not pal- pable. FMNH 93256 (no individual measurements)— Transverse diameter of scrotum 35 mm, unpig- mented skin puckered, thinly covered with blond hair; penis emerging from lower anterior third of scrotum completely ensheathed within spinous prepuce, penile shape and curvature not precisely determinable. FMNH 95348 (juv.)— Greatest transverse scrotal width about 34 mm; length of sheathed shaft with small portion of glans visible about 18 mm; shaft with longitudinal axis of dorsal surface convex; spines not evident; baculum not palpable. FMNH 57690 (juv.)— Right testis missing; length of nearly entirely sheathed penis about 1 8 mm; dorsal curvature of shaft convex; spines not evi- dent; baculum not palpable. FMNH 57689 (juv.)— Greatest transverse diam- eter of unpigmented scrotum 37 mm, testes small; length of sheathed portion of p>enis 7 mm; spines not evident, baculum not palpable. MPEG 6936 (HB = 440; W = 3,000) - Length of cleared penile fragment about 40 mm, base 10 mm, distal constriction 5 mm; long axis of dorsal and ventral surfaces plane, shaft tajjered, fur- rowed, cross section subtriangular, apex dorsal, cant right; spines present; ventral meatal lappet enlarged, dorsal lappet smaller; baculum absent. MPEG 6915 (HB = 430; GSL = 94.3) -Length of cleared p)enile fragment 30 mm, base 12 mm; furrowed shaft with surface concave, ventral con- vex, subtriangular in cross section, apex dorsal, cant right, spines prominent, baculum absent. MPEG 6921 (GSL = 90.2) -Length of cleared p)enile fragment 30 mm, shaft furrowed, dorsal surface concave, ventral convex, subtriangular in cross section, apex dorsal; cant right; spines pres- ent, baculum absent. MPEG 8848 (HB = 410; GSL = 87.9)- Length of cleared penile fragment 25 mm, 1 1 mm wide at prepuce; dorsal surface of furrowed shaft con- vex, ventral slightly concave, cant right, spines present, baculum absent. MPEG 6935 (HB = 428)— Length of cleared sec- tion of furrowed penis 21 mm; dorsum of shaft concave, cant right; spines present, baculum ab- sent. MPEG 6933 (HB = 430)— Length of cleared fur- rowed penile fragment 16 mm, strongly concave dorsally with apical crest; cant left; spines present; baculum absent. MPEG 6914 (HB = 430; GSL = 91.3)-Cleared terminal penile fragment, the furrowed basal bor- der with spines; shaft with dorsal contour concave, ventral convex, subtriangular in cross section with apex dorsal; cant left; baculum absent. AMNH 518225 (HB = 380; GSL = 89.2; W = 2,500)— Length of cleared, slender, furrowed penis 20 mm long; shaft with dorsum concave, cant right, spines present, baculum absent (figs. 4b-d). FMNH 57685 (HB = 260) -Cleared fragment of glans with vestige of baculum, original no. 93, no original data, labeled identification questionable. FMNH 57686 (original no. 108)— Cleared frag- ment of glans without original data, baculum ab- sent; labeled identification questionable. Cacajao melanocephalus ouakary Spix (figs. 5a-d) Size- HB = 4 1 4(3 1 0-500) 1 7; GSL = 99.9(9 1 .2- 108.8)21. Specimens— Four penes excised from dry mu- seum skins, cleared, stained for bone, and pre- served in glycerine; three of them nearly entirely decomposed. FMNH 78567 (HB = 415; GSL = 99.5) (figs. 5a- d) — Length of cleared tapered penile fragment 42 mm, diameter at base 10 mm, distal diameter be- low meatus 5 mm; shaft with dorsal surface convex longitudinally, concave ventrally, cross section subtriangular, apex dorsal, cant left, the raphe keeled; entire organ thickly vested with mostly large grappler spines, some nearly 1 mm long, most directed forward (distad), others back, still others at right angle to longitudinal axis, the orientation appears normal but may be an artifact of prepa- ration and preservation; meatus longitudinal with lips swollen, terminal lappet approximately as long as meatus, its tip pigmented; baculum absent. FMNH 78562-3, 78566— All without penis bones, remaining fragments were presumably like com- parable parts of preceding. Cacajao cahus I. Geoff roy (figs. 6a-e) SiZES-HB = 456(380-560)14; GSL = 100.1(96.8-103.8)14. HB = 400; W = 3,450. Specimens— Three, including intact external genitalia of one fully mature C. c. calvus and two partial p)enes of C. c. (subspecies?) detached from dry museum skins, cleared, stained for bone, and preserved in glycerine. HERSHKOVITZ: SOUTH AMERICAN MONKEYS JiifJi-..- fc; .:-.•• • *\ ■■■■"■■■; ^%--. 'ij-' t^- ■:;/■:■■ ^ Vv^ V j.^a CACAJAO MEtANOCEPHALUS Fig. 5. Cacajao melanocephalus (fmnh 78567; KOH preparation); a, ventral surface of shaft; b, same, right side; c, same, cross section (apex dorsal); d, same, spines enlarged. FMNH 60292 (no data) (fig. 6a)— Scrotum ovate, entirely pigmented, the testes withdrawn, greatest stretched transverse diameter about 55 mm, skin puckered and convoluted, thinly hirsute, nearly nude in appearance, covered with small glands opening to surface; perineum pigmented, the per- ianal portion with short spines; penis tapered, pre- puce pigmented basally, unpigmented distally, shaft unpigmented, base to tip about 50 mm, diameter at base of prepuce about 10 mm, transverse width of glans 6 mm, length 8 or 9 mm; meatus 4 or 5 mm, lateral borders swollen, the ventral with swol- len lappet about 4 mm transversally; penis in- cluding prepuce and glans studded with large grap- FiG. 6. Cacajao calvus, external genitalia of mature male; a, intact, anteroventral aspect, testicles retracted, right sac partially stuffed with cotton, left sac relaxed (fmnh 60292); b, distal portion of shaft, right side (mpeg 8990, KOH preparation); c, same, ventral aspect; d, same, cross section of shaft, narrow side (apex), ventral; e, same, spines enlarged; the several directions of spines appear to be natural but may be artifacts of preparation and preservation. Sample figured is the only one available. 10 FIELDIANA: ZOOLOGY CACAJAO CALVUS =lC)rara HERSHKOVITZ: SOUTH AMERICAN MONKEYS 11 pling spines each with expanded base; longitudinal axis of staff slightly concave dorsally, moderately convex ventrally, subtriangular in cross section, the apex ventral, cant right, the shaft twisted about 30° to right of scrotal raphe; baculum not palpable. MPEG 8990 Guv.) (figs. 6b-e)— Length of cleared penile fragment with tapered shaft 23 mm, di- ameter at base 10 mm, distally behind meatus, 5 mm; shaft with longitudinal axis of dorsal surface slightly convex, crested, ventral surface concave, staff subtriangular in cross section, apex ventral, cant right; prominent spines recurved, each rising from swollen base; meatus bordered by swollen lips on sides, lappet below protruded; baculum absent. Cacajao calvus rubicundus I. GeofTroy and Deville RNHMS 630142 (GSL = 102.1) -Cleared penile fragment about 25 mm long, shaft with dorsal cur- vature plane, ventral convex, cross section sub- triangular, apex ventral, cant right; spines and glans as in preceding; baculum absent. Hill (1958, p. 645, 1960, p. 227, figs. 48, 49)- The 1958 description of the genitalia of an un- named species could apply to adults of either or neither of the two species of Cacajao but more likely to either an immature Cacajao calvus rubi- cundus or C. c. ucayalii. The crudely figured glans appears asymmetrical but it may be the lateral aspect that is shown. The detailed description of developing and ma- ture genitalia of Cacajao calvus ucayalii observed by Fontaine and Du Mond (1977, pp. 201, 203) in the seminatural environment of The Monkey Jungle, in Goulds, Florida, follows. Examination of the external genitalia of Ca- cajao allows easy sexual identification of adults while providing uncertain clues as to the sex- ual identity of younger animals. The most probable basis for this condition is the oc- currence in the male of a developmental stage of several years duration in which the external genitalia and other characteristics of the male approach the adult female in form. Female red ouakaris lack this developmental stage which begins in the male's fourth year. Their development proceeds directly from the ju- venile condition to adulthood in the fourth year. Thus, the external genitalia of infants and juveniles appear similar in both sexes be- cause these young ouakaris are in the process of developing the apparently similar external genitalia of adult females and subadult males. In the adult male the testes are fully de- scended. The scrotum is a black p)endulous[!], flaccid, asymmetrical bilobed sac. ... It is en- tirely hairless[!] as described by Kinzey (1971). The penis of the adult male appears large in proportion to other perineal structures. The prepuce encloses the proximal half of the body while tiny spicules cover the exposed distal portion of the body. The glans is poorly dif- ferentiated from the body and, as mentioned by Hill (1960), the penis is laterally com- pressed along its length. With the exception of a ring of black pigmentation around the external urethral meatus, the distal portion of the penis is entirely unpigmented. The external genitalia of the subadult male red ouakari presents a marked contrast with the adult male condition. The subadult male scrotum consists of a pair of rugose, black, hairless, symmetrical, parapenial scrotal alae that superficially resemble the adult female labia. Roughly triangular, and broadly at- tached to the pubic region, each pendulous scrotal lobe is distinct from its opposite mem- ber, but connected by a bridge of apparently similar tissue postpenially. The testes appear undescended at this level of development. The prepuce covers the entire length of the sub- adult's glans penis which only becomes visible during erection. Hill (1960) provides a detailed account of the external genitalia of C. rubicundus ucayali [= C c. rubicundus]. In comparison with males observed in the "Rainforest," his description conforms to a transitional stage between the adult and the subadult. The sexual identification of juvenile and infant ouakaris on the basis of field charac- teristics is problematical. Male and female ex- ternal genitalia do not have obvious differ- entiating characteristics during the first two years of life. ... In these animals, the external genitalia consist of three hillocks in the pubic region that are more darkly pigmented than the surrounding regions. During vigorous lo- comotor play in the male, erection of the penis occurs allowing the unpigmented penis to pro- trude beyond the preputal [sic] anlage. The absence of visible erection characterizes the young female. The external genitalia of the adult female 12 FIELDIANA: ZOOLOGY resemble those of the subadult male. The glans clitoridis and preputium clitoridis of adult fe- males in the seminatural environment form a dusky hillock anterior to the rima pudendi. To each side of the rima pudendi lie black, rugose, p)endulous labia. These structures su- perficially resemble the scrotum of the sub- adult male; however, their relatively uniform lateral thickness, their relatively gracile char- acter, and their tendency to form an acute angle anteriorly allow discrimination of the adult female labia and the subadult male scro- tum. A constriction of the labia about halfway along their ventral extent which may corre- spond to a demarcation between the labia mi- nora and the labia majora provides another characteristic facilitating the identification of adult females. Hill's description of the female genitalia of a specimen of C. ruhicundus [= C. c. ucayalii] probably represents a female about 3 years of age that was in the process of acquiring adult characteristics. The pendulous character of the labia was not developed in this specimen. Hill's (1960) account suggests that the pen- dulous labia of the adult female ouakari may represent fusion of the labia minora and the labia majora with the portion homologous with the labia majora extending most ven- trally. Morphology and Phylogeny Baculum Pitheciine bacula are in the process of disap- pearing in the wake of differentiation of an osten- sibly unique system of sperm delivery within the group. The baculum has been lost in Cacajao and Chiropotes except for scattered vestiges of disin- tegrated embryonic bacula detectable in the cleared and stained glandes of a few adult specimens (table 1). The baculum in Pithecia is dorsomedian, the urinary meatus ventromedian directly behind the anteromedian lappet. The lobes on each side of the opening are symmetrical. Hershkovitz (1977, p. 119) observed that the meatus of the Callitri- chidae, Callimiconidae, most cebids, nearly all cercopithecids, and some anthropoids is skewed to the right with the left lobe of the glans containing the baculum larger than the right. The asymmetry p>ersists in atelines and Aotus with baculum lost or vestigial. An Aotus [sp.?] in the British Museum (Natural History) with baculum 2.2 mm long was reported by Dixson (1987a, p. 52). Evidently, loss of baculum in the symmetrical glans of pitheciines. Homo, Tarsius, and the asym- metrical glans of atelines and Aotus, are parallel- isms. Correlations between baculum length and body weight in 74 adult primates representing 46 species were described as positive by Dixson ( 1 987a). The length of the baculum also appeared to be corre- lated with copulatory behavior in 34 species for which detailed information was available. The study animals included Pithecia albicans, with baculum length 1.5 mm and copulatory behavior and weight unknown. The small baculum, how- ever, does correlate with small body size as de- termined by Dixson (1987a, table on p. 53). The same is true of other individuals of Pithecia with baculum intact. All other pitheciine genera are much larger and lack bacula. In their case, Dix- son's correlations do not apply. Penile Shaft Pitheciine penes have departed from the hy- pothetical ancestral, subcylindriform organ to a small, tapered, bluntly pointed glans, the shaft with dorsal longitudinal axis either convex (p)enis point- ed down or distally) or concave (p)enis pointed up or proximally), sides compressed, the organ in cross section subtriangular with ap)ex dorsal or ventral, the shaft curved or canted to left or right. Penile cant in Pithecia monachus, as in Cacajao calvus, is to the right; that of the remaining pithe- ciines is to the left except in Chiropotes satanas where it may be right or left. The single cleared mature penis available of Chiropotes albinasus re- sembles those of Chiropotes satanas except pos- sibly by its dorsal longitudinal convexity. The pe- nis of Cacajao calvus differs primarily from all others by the narrow or apical aspect of its ventral surface (table 2). More samples of each sp)ecies may reveal variation not apparent in the single or few available samples. Observations— In his study of primate geni- talia and behavior, Dixson (1987b, p. 439) noted that penile morphology and copulatory patterns "tend to be more specialized in sfjecies which have a multimale or dispersed (non-gregarious) mating system. The penis may be longer and more com- plex morphologically in such species." Among the HERSHKOVITZ: SOUTH AMERICAN MONKEYS 13 1 30 species Dixson examined, the pitheciine Ca- cajao calvus (two specimens) was listed among the multimale societies, its penis indicated as mod- erately complex. Attribution of a baculum to the SE)ecies, however, may be questioned. Included among primates with a monogamous mating sys- tem were the comparatively unspecialized Pithecia pithecia and P. albicans. Present data indicate that correlations drawn by Dixson between baculum, penile complexity, spines, body size, and copulatory behavior could be the same with or without the baculum. Scrotum All pitheciine scrota are sessile and parapenial, ovate in Cacajao and Chiropotes, pear-shaped in Pithecia; skin in preserved condition puckered in parts, sulcate, convoluted or corrugated in others, the sebaceous glands showing as pitted welts, the long pigmented hairs arranged in triads each emerging from a pore; a short hair flanks each side of each triad. The eight available scrota o{ Chiropotes satanas are mostly asymmetrical without evident polarity. In Pithecia, the pigmented perineum is hairy, the raphe extending nearly to proximal border of glans; in Chiropotes, the bare, pigmented raphe contin- ues well defined to the scrotal base and continues almost imperceptibly to base of prepuce. The pig- mented perineum is beset with short, thick spines. Spines The conical recurved spines are formed of over- lapping scales of keratinized epidermis. Worn, broken, or cast-off'spines are renewed as evidenced by spines of all sizes and in all formative stages. Spines of monogamous Pithecia are minuscule, each with a nodular base and altogether too small for effective hooking or grappling. They may, how- ever, provide stimulation during intercourse. Spines of so-called multimale groups Chiropotes and Cacajao are large and hooked. Those of Ca- cajao attain a length of nearly 1.0 mm. Those of the tumescent penis of both genera can be erected, possibly for heightened sensitivity during prein- tromittent probing. During intromittent thrusting, spines may assist in the disintegration of vaginal plugs formed from prior multimale ejaculates or may hook into the vaginal mucosa to form a lock. Penes of juvenals and subadults have no need to lock. They lack spines. Effects of penile spines on the copulatory be- havior in primates were tested by Dixson (1991) on the common, generally monogamous mar- moset, Callithrix jacchus. Sixteen sexually expe- rienced captive-bom males and 10 females with similar histories were used. "The major effect of spine removal," Dixson (1991, p. 561) found, "is to increase the duration of pelvic thrusting re- quired to attain intromission, with some effect also upon the duration of intra vaginal pelvic thrusting. Spine removal has no effect upon penile erection or upon the ability of males to orientate correctly when mounting females. However, the ability to locate the vaginal orifice during bouts of rapid preintromission pelvic thrusts is impaired in these animals." Sexual Behavior The sexual life of pitheciines is little known. A monogamous social system of certain, if not all, species of Pithecia is inferred from field observa- tions of paired or family group associations of P. pithecia (Buchanan et al., 198 1) and P. monachus (Moynihan, 1976; Izawa, 1976). My field obser- vations of both species confirm those reports. In- formation on the social system of remaining spe- cies {P. irrorata, P. albicans, and P. aequatorialis) is lacking. Observations of actual mating and cop- ulation among free-living sakis have not been re- corded. The two species of Chiropotes (C albinasus and C satanas) associate in so-called multimale groups, actually composed of both sexes of all ages (Ayres, 1981). Again, nothing is known of sexual play and copulatory behavior of either species. Each of the two species of Cacajao also form "multimale groups," correctly, multimale-female or cosexual congregations. Sexual behavior of wild-living Ca- cajao melanocephalus has not been recorded. That of C calvus rubicundus has been studied in the seminatural environment of The Monkey Jungle, Goulds, Florida, by Fontaine and Du Mond ( 1 977, pp. 207-209). Their account follows. Observations of the sexual behavior of Ca- cajao at Monkey Jungle have been largely con- fined to sexual relationships between juvenile males and adult females. The adult male's involvement in defensive responses to human 14 FIELDIANA: ZOOLOGY intruders interferes with his conduct of sexual relations in the presence of observers. Enough observations of adult male sexual behavior have been collected, however, to allow de- scription of the major elements of Cacajao's sexual behavior. The adult female displays some p>ostural variability during copulation. She may lie prone with all four limbs flexed under her body or she may allow her limbs to dangle freely beneath her. Less frequently, the female lowers her hindquarters and maintains them in flexion during copulation while raising the forequarters. During copulation, the male sits behind the female with the thighs abducted and flexed. In juvenile copulations, the males were observed to flex their hindlimbs at the knees allowing the feet to maintain a firm grip on the small of the female's back (Fig. 6). The latter aspect of juvenile copulation may have been overlooked in adult male copulation. However, since this feature of juvenile cop- ulation serves to "lock" the male into a secure position of dorsal-ventral contact with the fe- male, it may prove to be a typical aspect of copulation in Cacajao. Copulation in Cacajao requires several minutes. The typical copulation consists of a series of intromissions each accompanied by multiple pelvic thrusts by the male partner occasionally aided by complementary move- ments by the female partner. Periods of with- drawal alternate with periods of intromission. During these withdrawal periods, behavior is quite variable, ranging from general body contact to rapid travel to another location to continue copulation. . . . Postcoital behavior in the adult male usu- ally includes smelling of the female genitalia followed by a bout of mutual social grooming. The juvenile male, in contrast, usually leaves the female after a few cursory genital sniffs. Cacajao does not include patterns such as genital presenting, pelvic thrusting, etc. with- in its repertoire of non-sexual social signals. On the other hand, the ouakari's long mantled fur hinders the observation of intromission and ejaculation and the detection of copula- tion plugs. The large mixed sex and age associations or troops o{ Cacajao or C/;/>o;?o/c5 described by some (Ayres, 1981; Roosmalen et al., 1 98 1 ) as consisting of up to 30 individual and more, and by others as from 100 to 200 (Olalla, 1955), suggest a mating pattern of sexual promiscuity. Testis size, sperm quality and quantity, and sperm competition within and between multiple ejaculates have been discussed by Moller (1988). According to Gomendio and Roldan (1991), sperm length is longer in polyandrous species than in monogamous species and is positively correlated with maximum SF>erm velocity. Neither report mentions pitheciines with mating systems that en- compass monogamy, polyandry, and penes with or without baculum. Neither considers the prob- ability that among females hierarchical controls and physiological responses to sperm stimuli might enforce a degree of selectivity. Conclusions Evolution of pitheciine male genitalia has given rise to what could possibly be a unique system for direct sperm delivery into the uterus. The process involved reduction or elimination of the baculum, curvature of the shaft with lateral compression and taper to a small bluntly pointed labile glans, emer- gence of meatal erectile clasping bodies or lappets, and in Chiropotes and Cacajao hypertrophy of penile spines for clearing passage through the va- gina and locking. The penis such as that of Pithecia with a simple or nearly cylindrical form covered with minuscule spines could give rise to organs such as those of Chiropotes and Cacajao. The pigmented strongly tapered penis of Cacajao projects from near the inguinal border of the scrotum and curves upward with a sidewise twist of more than 30°. The lon- gitudinally concave curvature of the unpigmented ventral surface of the Chiropotes penis is like that of Cacajao, but the narrow side or apex is dorsal, not ventral as in Cacajao, the member itself turned sidewise to as much as 45° against the scrotum. The boneless, curved pitheciine shaft simulates or equates with the long terminally curved or hooked baculum possessed by many kinds of mammals (cf. Burt, 1960). In all cleared penes, the arrangement of the tu- mescent lappets surrounding the meatus take on the form of a gasket. In coitus, the glans likely penetrates to the level of the cervix. Conceivably, at that point the labile gasket-like meatus clamps onto the cervix and stimulates opening of the cer- vix for transfer of ejaculates into the uterus. In Cacajao and Chiropotes, the penis with its labile HERSHKOVITZ: SOUTH AMERICAN MONKEYS 15 glans is already curved and twisted upward toward the cervix. During coital convulsions, an extensile cervix might make the additional quarter turn to couple with the glans. Adhesion between cervix and meatus of a particular male most likely de- p)ends on selective responses of the female appa- ratus. Where meatus and cervix are normally not opposed as, presumably, in nearly all other pri- mates, the described maneuver would not be pos- sible. In a sperm delivery system, described by Fooden (1990, p. 63 1) for the bear macaque, Ma- caca arctoides, "the prominent vaginal collide, short vagina, and long exocervix in M. arctoides are apparently morphologically complementary to the long, tapering glans penis in this species. . . . These complementary specializations of the glans and female tract appear reciprocally adapted to permit the glans to pass ventral to the vaginal collide, through the short vagina, and into the long exocervix. Penetration of glans into cervix, as pos- tulated here, has not been previously reported in catarrhine primates." A baculum-stiffened glans as in perhaps 50% of Pithecia males might be less successful than the boneless glans in effecting embrace between me- atus and cervix. Baculum or not, males of mo- nogamous Pithecia are hardly if at all competitive with each other for insemination of the female. Spermatozoa of one saki, once delivered, presum- ably do not compete with those of other males as might be the case in multimale groups. Among primates, seminal vesicles, of impor- tance in the ejaculatory process, are reported ab- sent in the monogamous Pithecia and Callicebus (by Harrison and Lewis, 1986, table, without ref- erence to original sources) and in Daubentonia by Eckstein (1958, p. 554). In these genera, vaginal plugs would not be needed and may not be formed. According to Voss (1979), nearly all male rodents form vaginal plugs in the female vagina for chas- tity enforcement. Voss (1979, tables 3, 4) adds, however, that among the 24 murid species he ex- amined, the three that are monogamous form no vaginal plugs. These species were further distin- guished by highly modified or missing seminal vesicles and presence of a complete copulatory locking system. The locking system, according to Dewsbury (1972), has not been observed in pri- mates. It seems, rather, that it may exist at least among pitheciines (cf. p. 14), and some callitri- chids (Hershkovitz, 1977, p. 418). Acknowledgments Authorities of the Museu Paraense Emilio Goel- di, the American Museum of Natural History, and the Royal Natural History Museum, Stockholm, graciously permitted detachment and preparation of samples of penes from dry skin specimens of Cacajao and Chiropotes in their charge. Through the good offices of its then Curator of Mammals, Dr. Clyde A. Hill, bodies of pitheciines that had died in the San Diego Zoological Garden were donated in 1974 to the Field Museum of Natural History. The illustrations of genitalia were exe- cuted by Elizabeth Liebman and Kathleen Telfer. Former Technical Assistant Ron Edwards assisted in the preparation of the genitalia for study and all other aspects of the research. Research Assis- tant Barbara Brown helped in many ways. My thanks to all and particularly Dr. Bruce Patterson for a critical reading of the manuscript and valued suggestions. Literature Cited Ayres, J. M. 1981. Oserva96es sobre a ecologia e o comportamento dos cuxius {Chiropotes albinasus e Chiropotes satanas, Cebidae: Primates). Doctoral diss, privately published under auspices of the Conselho Nacional de Desenvolvimento Cientifico e Technolo- gico (CNPq), Instituto Nacional de Pesquisas da Ama- zonia (INPA), Manaus, Brazil, 142 pp. Buchanan, D. B., R. A. Mittermeier, and H. G. H. VAN RoosMALEN. 1981. The saki monkeys, genus Pithecia, pp. 391-417. In Coimbra-Filho, A. F., and R. A. Mittermeier, eds., Ecology and Behavior of Neo- tropical Primates, 1. Academia Brasileira de Ciencias, Rio de Janeiro. Burt, W. H. 1 960. Bacula of North American mam- mals. Miscellaneous Publications of the Museum of Zoology, University of Michigan, 13: 1-75. Dewsbury, D. A. 1972. Patterns of copulatory behav- ior in male mammals. Quarterly Review of Biology, 47(1): 1-33. DixsoN, A. F. 1987a. Baculum length and copulatory behavior in primates. American Journal of Primatol- ogy, 13:51-60. . 1987b. Observations on the evolution of the genitalia in copulatory behavior in male primates. Journal of Zoology, London, 213: 423-443. -. 1991. Penile spines affect copulatory behavior in a primate (Callithrix jacchus). Physiology and Be- havior, 49: 557-562. Eckstein, P. 1958. II Reproductive organs: A. Internal 16 FIELDIANA: ZOOLOGY reproductive organs. In Hofer, H.. A. H. Schultz, and D. Starck, eds., Primatologia III. (1): 543-629. S. Kar- ger, Basel. Fontaine, R., and F. V. Du Mond. 1977. The red uacari in a seminatural environment: Potentials for propagation and study, pp. 167-236. In Prince Ranier III of Monaco and G. H. Bourne, eds., Primate Con- servation. Academic Press, New York. FooDEN, J. 1990. The bear macaque ii/acac-a arc/o/V/^5: A systematic review. Journal of Human Evolution, 19: 607-686. GoMENDio, M., AND E. R. S. RoLDAN. 1991. Sperm competition influences sperm size in mammals. Pro- ceedings of the Royal Society of London, Series B, 243(199): 181-185. Harrison, R. H., and R. W. Lewis. 1986. The male reproductive tract and its fluids, pp. 101-148. In Du- kelow, W. R.,andJ. Erwin, eds.. Comparative Primate Biology, 3. Alan R. Liss, New York. Hershkovitz, p. 1977. Living New World Monkeys (Platyrrhini) with an Introduction to Primates. Uni- versity of Chicago Press, Chicago, xiv + 1,1 17 pp. . 1985. A preliminary taxonomic review of the South American bearded saki monkeys, genus Chi- ropotes (Cebidae, Platyrrhini), with the description of a new subspecies. Fieldiana: Zoology, n.s., 27: 1-46. 1 987a. New World monkeys of the genus Ca- co/ao (Cebidae, Platyrrhini): A preliminary taxonomic review with the description of a new subspecies. Amer- ican Journal of Primatology, 12: 1-53. 1987b. The taxonomy of South American sa- kis, genus Pilhecia (Cebidae, Platyrrhini): A prelimi- nary report and critical review with a description of a new species and a new subspecies. American Journal of Primatology, 12: 387^68. Hill, W. C. Osman. 1 958. External genitalia, pp. 630- 704. In Hofer. H., A. H. Schultz, and D. Starck, eds., Primatologia, 3(1). S. Karger, Basel. . 1960. Primates Comparative Anatomy and Taxonomy. IV, Cebidae, Part A. A Monograph. In- terscience Publishers, New York, xiii + 523 pp. IzAWA, K. 1976. Group sizes and composition of mon- keys in the upper Amazon basin. Primates, 17(3): 367- 399. KiNZEY, W. G. 1971. Male reproductive system and spermatogenesis, pp. 85-1 14. In Hafetz, E. S. E., ed.. Reproduction of Nonhuman Primates. Springfield, III. MoLLER. A. P. 1988. Ejaculate quality, testes size and sperm competition in primates. Journal of Human Evolution, 17(5): 479-488. MoYNiHAN, M. 1 976. The New World Primates. Adap- tive Radiation and the Evolution of Social Behavior, Languages and Intelligence. Princeton University Press, Princeton, N.J. Olalla, a. M. 1955. Notas biologicas sobre los uaca- ries. Geografica, Sao Paulo, 5(5): 1 7-23. ROOSMALEN, M. G. M., R. A. MiTTERMEIER, AND K. Milton. 1981. The bearded sakis, pp. 4 1 9-44 1 . /« Coimbra-Filho, A. F., and R. A. Mittermeier, eds.. Ecology and Behavior of Neotropical Primates, 1. Ac- ademia Brasileira de Ciencias, Rio de Janeiro. Voss, R. 1979. Male accessory glands and the evolution of copulatory plugs in rodents. Occasional Papers of the Museum of Zoology, University of Michigan, no. 689, pp. 1-29. HERSHKOVITZ: SOUTH AMERICAN MONKEYS 17 Dri