AVIAN SEED DISPERSAL OF NEOTROPICAL GAP-DEPENDENT PLANTS By KELVIN GREGORY MURRAY A DISSERTATION PRESENTED TO THE GRADUATE SCHOOL OF THE UNIVERSITY OF FLORIDA IN PARTIAL FULFILLMENT OF THE REQUIREMENTS FOR THE DEGREE OF DOCTOR OF PHILOSOPHY UNIVERSITY OF FLORIDA 1986 ACKNOWLEDGMENTS I am greatly indebted to many individuals for support and assistance in completing this project. Kathy Winnett- Murray was intimately involved in every phase of the project, providing assistance in the field work as well as valuable advice on planning, data analysis, and writing. That she was able to do all that, complete her own dissertation work, and still be a wonderful wife in the face of both our frustrations over the difficulties of field research, is truly amazing. Peter Feinsinger likewise provided advice, assistance, and humane editorial criticism from the earliest planning stages of the work. Without several of his well-timed pep-talks, the study would surely have suffered greatly and might never have been completed at all. I cannot overestimate his positive influence on this work, or on my graduate career in general. For this and for his friendship, I will always be grateful . I benefitted greatly from discussions with the other members of my supervisory committee, H. Jane Brockmann, Thomas Emmel, Walter Judd, and Francis Putz, who also provided valuable editorial advice on earlier drafts of the dissertation. Discussions with Nicholas Brokaw, Carmine Lanciani, Robert Lawton, Douglas Levey, Timothy O'Brien, Carlos Martinez del Rio, and Harry Tiebout III were also very helpful. My collegues at the University of Florida, and especially the other biologists who resided concurrently at Monteverde, were also invaluable. Willow Zuchowski-Pounds, Bill Busby, Rita Schuster, and Sarah Sargent provided assistance with field work. Jennifer Shopland kindly shared mist-netting and feeding observation data on frugivores. Advice on field technigues and data analysis were provided by these individuals as well as by Jim Beach, Martha Crump, Eric Dinerstein, Sharon Kinsman, Yan Linhart, David McDonald, Alan Pounds, Francis Putz, and Nat Wheelwright. I am especially grateful to all of these Monteverde biologists, and to members of the Monteverde community in general, for making my 27-month tenure there one of the most enjoyable periods of my life. Wolf Guindon, Gary Hartshorn, Joseph Tosi, Jr., Manuel Ramirez, and Giovanni Bello kindly facilitated my use of the Monteverde Cloud Forest Reserve. Logistical support in Costa Rica was provived by personnel of the Organization for Tropical Studies, especially Roxanna Diaz. Financial assistance was provided by the Jessie Smith Noyes Foundation (administered by the Organization for Tropical Studies), the University of Florida Department of Zoology, a Sigma Xi grant-in-aid, and NSF grants DEB 80-11008 and 80-11023 to Peter Feinsinger and Yan Linhart, respectively. Finally, I thank my family. My parents, Max W. Murray and Lorene M. Murray, and my sister, Gayle Fitchner, provided understanding and unwaivering encouragement throughout my educational career. My wife, Kathy, and my son, Dylan Winnett Murray, have taught me what is truly important, and help me to keep the various aspects of my life in their proper perspective. TABLE OF CONTENTS Page ACKNOWLEDGMENTS ABSTRACT INTRODUCTION STUDY AREA METHODS ll V 1 5 7 Crop Size, Fruiting Phenology, and Fruit Removal Rates 7 Seed Germination Experiments 8 Seed Dormancy Experiments 1° Gap Dynamics of the Monteverde Cloud Forest 1 1 Mist Netting and Analysis of Fecal Specimens 12 Fruit Handling, Seed Treatment, and Seed Passage Rates 13 Movement Patterns of Frugivores 14 RESULTS. 16 16 Natural History of the Plants 1 7 Fruit Consumers L Fruit Handling and Seed Treatment in the Gut 23 Spatial and Temporal Distribution of Suitable Colonization Sites Cl Seed Shadows Produced by Birds 41 Mediation of Plant Reproductive Success by Birds 59 DISCUSSION Effects of Fruit Handling and Gut Treatment. Effects of Dispersal 30 83 Limitations of the Model 92 Seasonal Constraints on Reproductive Success 94 Conclusions 97 APPENDIX ESTIMATION OF "SEED SHADOWS" FROM DATA ON SEED PASSAGE RATES AND BIRD MOVEMENT PATTERNS: A HYPOTHETICAL EXAMPLE 1°° LITERATURE CITED 109 BIOGRAPHICAL SKETCH 119 Abstract of Dissertation Presented to the Graduate School of the University of Florida in Partial Fulfillment of the Requirements for the Degree of Doctor of Philosophy AVIAN SEED DISPERSAL OF NEOTROPICAL GAP-DEPENDENT PLANTS By Kelvin Gregory Murray December 1986 Chairman: Peter Feins inger Major Department: Zoology In cloud forest at Monteverde, Costa Rica, I investigated reproductive consequences of avian seed dispersal for three species of gap-dependent plants: Phytolacca rivinoides (Phytolaccaceae) , Witheringia solanacea, and W_^ coccoloboides (Solanaceae). Of six bird species that consumed fruits of these plants, only three (Myadestes melanops (Muscicapidae) , Phainoptila melanoxantha (Ptilogonidae) , and Semnornis f rantzii (Capitonidae) dispersed seeds in viable condition. I estimated quality of dispersal service provided by these species by comparing the seed shadows they produced with spatial and temporal distributions of establishment sites for the plants. I estimated seed shadows from data on gut passage rates of seeds and on movement patterns of radio- tracked birds. Seed shadows produced by all three effective dispersers were extensive, with few seeds deposited near the parent plant, and some moved N 500 m. Seeds of the species examined germinate in forest gaps formed by treefalls or landslides. Germination success varies with gap size and age, but the relationship is different for each species,- both 2 Witheringia species germinate well in gaps as small as 15 m or as old 2 as 6 months, whereas P. rivinoides germinates well only in gaps > /0 m or < 4 months. Consequently, establishment sites for all three plants are both rare and ephemeral, but to differing degrees. Seeds that are not dispersed to suitable habitat patches can remain dormant in the soil until a gap is formed overhead. To determine consequences of dispersal and dormancy for plant reproductive success, I developed a simulation model that uses data on seed shadows, germination requirements, seed dormancy, and forest dynamic processes to estimate reproductive output (total offspring produced during an individual's lifetime) and relative "fitness" (an estimator that discounts the contribution of offspring produced after a long period of dormancy). Results show that (1) dispersal by any of the three effective dispersers increases reproductive output 16-36 times, even without seed dormancy. (2) dormancy capabilities up to two years greatly enhance both reproductive output and "fitness", but greater capabilities increase only reproductive output. (3) Without dispersal, dormancy has little effect on either reproductive output or fitness. Thus, both dispersal and dormancy ("dispersal" in time) are essential to these gap-dependent plants. INTRODUCTION Recent interest in the ecology and evolution of plant-f rugivore mutualisms focuses largely on the reproductive consequences, to plants, of fruit consumption by different animals (e.g., Snow 1965, 197 1; McKey 1975; Howe and Estabrook 1977; Howe and De Steven 1979; Howe and Vande Kerchove 1979, 1980, 1981; Thompson and Willson 1979; Howe 1980; Stiles 1980, 1982; Herrera 1981, 1984; Sorensen 1981, 1983; Thompson 1981; Stapanian 1982; Skeate 1985). Most studies deal with fruit removal or qualitative aspects of dispersal only: they distinguish between regular and occasional visitors to fruiting plants (e.g., Leek 1972, Howe and Primack 1975, McDiarmid et al. 1977, Howe 1977, 1980, Howe and De Steven 1979, Howe and Vande Kerchove 1979, Hilty 1980, Greenberg 1981), between animals that pass seeds in viable condition and those that destroy seeds (e.g., Howe 1980), or between animals that disperse seeds away from the parent plant and those that drop seeds directly beneath it (e.g., Howe 1977, 1980, 1982, Howe and Vande Kerchove 1979, 1981). However, few studies directly address the contributions to plant reproductive success resulting from the spatial distributions of seeds, or "seed shadows," produced by dispersers. This study deals with the reproductive consequences of avian seed dispersal in three gap-dependent plant species of neotropical cloud forest. Using data on the dynamics of gap formation and the seed germination requirements of plants, I first identify the spatial and temporal distributions of suitable habitat patches ("gaps" formed by 1 treefalls or landslides) within the forest. Second, I compare the distribution of suitable patches with the "seed shadows" produced by different frugivorous birds. Finally, I evaluate the impacts of fruiting phenology, plant longevity, seed dormancy, and other plant life history traits on plant reproductive success and on the ecology and evolution of plant-disperser interactions. In spite of the recent explosion of research on plant-f rugivore interactions (reviewed by Howe and Smallwood 1982, Janzen 1983a; see also Estrada and Fleming 1986), knowledge of their ecology and evolution lags behind that of plant-pollinator interactions (reviewed by Feinsinger 1983, Jones and Little 1983, and Real 1983). This discrepancy occurs because the reproductive consequences of pollen dispersal by animals are more easily quantified than the consequences of seed dispersal (Wheelwright and Orians 1982). In plant-pollinator systems, both the origin of, and "target" for, pollen grains are specific and easily recognized by dispersers and ecologists alike. Furthermore, pollinators are rewarded for delivering pollen grains to the target--the stigma of a conspecific flower. Thus, we can determine the relative advantages of pollen dispersal by different animals by determining which ones are most likely to deposit pollen grains on the stigma of a conspecific flower. In contrast, the only target for dispersed seeds is generally a patch of soil with a combination of physical, chemical, and biotic characteristics that make it a suitable site for germination and growth (i.e., a "safe site," sensu Harper 1977). Furthermore, no reward is offered to vectors that deposit seeds in such sites. For most plants, we lack detailed knowledge of the characteristics of suitable target sites for seeds, let alone their spatial and temporal distributions. As a result, we know little about the reproductive advantages of dispersal for most plants, and even less about the consequences of dispersal by particular animals. To understand plant-f rugivore relationships and the phenotypic traits associated with them, we must identify the spatial and temporal distributions of seed "targets" and evaluate the likelihood of dispersal to those sites by different animals. Howe and Smallwood (1982) proposed three alternative functions of seed dispersal. First, dispersal may result in decreased density- or distance-dependent mortality on seeds or seedlings near the parent plant (e.g., Howe and Primack 1975, Janzen et al. 1976, Piatt 1976, Salmonson 1978, Clark and Clark 1981, Augspurger 1983a, b, 1984a, b, Howe et al. 1985). Second, dispersal by certain means (e.g., by ants that carry seeds to rotting logs) may result in non- random seed movement to particular sites where the probability of survival is especially high (Docters van Leeuwen 1954, Handel 1978, Culver and Beattie 1980, Thompson 1980, Davidson and Morton 1981a, b). Third, widespread dispersal may allow colonization of ephemeral, spatially unpredictable patches of disturbed habitat (cf., Augspurger 1983a, b, 1984a, b, Piatt 1975, 1976). Although the three functions proposed by Howe and Estabrook are not mutually exclusive, the third may be most important for many plants. In most tropical and temperate forests, recruitment of many plant species occurs only in patches created by canopy disturbances such as treefalls and landslides (Richards 1952, Schultz 1960, Whitmore 1975, Hartshorn 1978, Brokaw 1980, Denslow 1980). Such gap-dependent or "pioneer" species typically germinate in forest gaps soon after formation, grow rapidly to reproductive size, and produce large numbers of seeds. They 4 often die out as the gap is closed by lateral growth of trees on the gap's border and by vertical growth of other plants within the gap. In most gap-dependent species, germination is stimulated by the increased red/far red ratio of incident light (e.g., Vazquez-Yanes 1977, 1980, Vazquez-Yanes and Smith 1982, Vazquez-Yanes and Orozco-Segovia 1984) or increasing soil temperature fluctuations (Aubreville and Leroy 1970, Vazquez-Yanes 1976, Vazquez-Yanes and Orozco-Segovia 1982, 1984) that characterize recent gaps (Schultz 1960). Such plants are ideal for studies on seed dispersal. The spatial and temporal distributions of suitable habitat patches can be determined by first establishing the range of gaps in which germination and establishment occur, and then measuring the distribution of those gaps over the landscape. STUDY AREA From June 1981 through July 1983, I studied the interactions between f rugivorous birds and Phytolacca rivinoides Kunth & Bouche (Phytolaccaceae), Witheringia solanacea L' Her, and W^_ coccoloboides (Damm.) Hunz. (Solanaceae) in the Monteverde Cloud Forest Reserve, Costa Rica (10°18'N, 84°48'W). Lawton and Dryer (1980) provide a thorough description of the geography, climate, and forest types of the Reserve. The Monteverde area lies on a gently sloping plateau, on the Pacific slope of the continental divide in the Cordillera de Tilaran. Local weather patterns and vegetation of the area are strongly influenced by the northeast trade winds. Blowing mist is a nearly constant source of water for plants near the continental divide, even during much of the dry season (January to early May). Forest types in the area range from Lower Montane Rain Forest (Holdridge life zone classification system, Holdridge 1967) near the continental divide, through Lower Montane Wet Forest to Lower Montane Moist Forest and Premontane Wet Forest zones along the lower edge of the plateau. Sites used in this study were all located between 1450 and 1650 m elevation, within either Lower Montane Rain Forest (oak ridge forest, windward cloud forest, and swamp forest, sensu Lawton and Dryer 1980), or within the Lower Montane Wet Forest - Rain Forest transition zone (leeward cloud forest, sensu Lawton and Dryer (1980)). Dominant overstory vegetation within the study area includes many species of Lauraceae, Moraceae, and Araliaceae, in addition to Meliosma sp., Sloanea megaphylla, Guarea spp., Hieronyma poasana, Ardisia palmana, and Clusia alata. The understory is dominated by Rubiaceae, Solanaceae, Acanthaceae, Gesneriaceae, Piperaceae, and Palraae. Many species occur most commonly in light gaps formed by falling branches or trees, including the "pioneer" trees Cecropia polyphlebia, Urera elata, Trema micrantha, Sapium pachystachys, Heliocarpus popayensis, Clibadium leiocarpum, and several species of Miconia and Conostegia. Several shrubs and large herbs also occur commonly in gaps, e.g., Solanum acerosum, S^ hispidum, Witheringia spp., Phytolacca rivinoides, Heliconia tortuosa, Bocconia f rutescens, and Eupatorium sexangulare. Seedlings of Phytolacca rivinoides, Witheringia solanacea, and W^ coccoloboides are very common in recent treefalls, especially on soils disturbed by uprooted trees. Within one month of formation, these "pits and mounds" (sensu Putz 1983) are generally covered by hundreds of seedlings of these and other species, especially Cecropia polyphlebia and Bocconia frutescens. A typical treefall examined approximately one month after formation contained 79 seedlings of P. rivinoides on the "mound" area alone (Murray, unpubl. data). Of the many gap-dependent species at Monteverde, I concentrated on P^ rivinoides, W. solanacea, and W. coccoloboides because they have similar fruits (small, multiple- seeded berries) and growth forms, but slightly different life history traits. By doing so, I hoped to evaluate the conseguences of dispersal by similar assemblages of frugivores to plants with different reproductive schedules, longevities, and germination reguirements. METHODS Crop Size, Fruiting Phenology, and Fruit Removal Rates I collected data on fruit crop sizes and fruiting phenology using monthly censuses of 8, 36, and 33 individuals of I\_ rivinoides, W^ solanacea, and W^_ coccoloboides, respectively. Plants occurred in several different building-phase (sensu Whitmore 1975) treefall plots and in larger, man-made clearings within the reserve. During each census, I counted all flowers, green fruits, and ripe fruits on each plant. Since most flowering and fruit development in both Witheringia species occurs well before ripening begins, I defined the total fruit crop in those species as the largest number of green fruits counted on that plant during any census in that fruiting episode. In Phytolacca, I estimated total fruit crop as the product of the number of inf ructescences formed and the average number of fruits per inf ructescence. I computed population-level fruiting phenology of each species (i.e., that of the "average" individual) by first determining the proportion of each individual's fruit crop that ripened each month (number of ripe fruits censused in each month divided by the sum of all ripe fruits censused on that plant over the fruiting season), and then averaging this proportion over all individuals censused. Thus, individuals with large fruit crops and those with small fruit crops were weighted egually in determining the fruiting phenology of the "average" individual . To determine rates of fruit removal from individual plants, I counted the number of ripe fruits on marked branches (Witheringia) or inf ructescences (Phytolacca) on each census plant on one day, and then counted those remaining 24-72 hours later. For purposes of the analyses reported here, each observation consisted of two such censuses on one plant. During the first count, I removed any damaged or desiccated fruits that might abscise spontaneously before the next census. In most cases (77% of all observations), I counted all ripe fruits on the plant. On very large plants or those with inaccessible fruits (23% of all observations), I marked and counted only a subsample of branches or inf ructescences. Plants were checked in this way for 2-4 consecutive days each month. Eighty-six percent of the observations were from plants re-censused after 24 hours. In those checked after 2 or 3 days, I divided the number of fruits removed by the number of days between censuses. All removal data are thus reported on a per day basis. I could not obtain information on removal rates by direct observation; the birds responsible for removing most fruits from these plants are extremely wary, and generally avoid feeding in the understory anywhere near an observer. Seed Germination Experiments I conducted experiments to determine germination success of P^ rivinoides, Witheringia solanacea, and W. coccoloboides in closed-canopy forest and in treefall gaps of various sizes and ages. Seeds used in all experiments were collected from several plants, mixed, and assigned to different treatments at random. Since many comparisons had to be made at different times of year, strict controls were not possible for all experiments. In such cases, I attempted to eliminate most of the obvious biases introduced by seasonal weather conditions. For example, during the driest months (March and April) when germinating seeds desiccate easily, I watered all seeds 1-2 times per week. Although this practice may result in an overestimate of seed and seedling survival in gaps during very dry periods, it provides unbiased data for answering the more immediate question of the relationships between germination success and gap size and age. To compare germination success in closed-canopy forest with that in large gaps, I planted 100 seeds of each species in cups of sterile soil in a large (ca. 2440 m2) man-made gap and 100 others (in like fashion) in adjacent forest. Gap seeds received full sunlight for most of the day, whereas canopy cover over forest seeds was greater than 98%, as determined by a canopy densiometer. Both groups of seeds were covered with a screened (ca. 1 mm mesh) enclosure to exclude herbivores and seed predators. Setups were checked for germination and seedling survival at 1-14 day intervals for 14 months. I measured the effects of smaller gaps on germination success by planting 50 seeds of each species in small cans of soil (10 seeds/can) near the centers of six recent treefall gaps of different sizes. Where necessary, I placed cans above any ground- layer vegetation so that shading was due solely to the crowns of trees bordering the gap. By thus eliminating shade from rapidly growing plants within gaps, effects of gap age (see below) on germination success were controlled. These setups were checked at weekly intervals for 2-3 months. I determined gap size using the formula for the area of an ellipse 10 (A = If' L • W / 4/ where L and W represent the lengths of the major and minor axes of the ellipse), since most gaps were roughly elliptical. Because light quality and intensity within a gap decrease over time as a result of shading from rapidly growing vegetation within it, I also determined the effects of gap age on germination success. Experiments were conducted in four gaps as they aged naturally. Three of the gaps were formed during a severe windstorm on 13-14 November 1982, the fourth during a storm on 11 January 1983. I planted fifty seeds of each species, in 5 groups of 10 seeds each, in small metal cans along transects running through the centers of the gaps. Setups were checked at weekly intervals for 1.5-2.5 months. The first run of this experiment was started 2-4 weeks after gap formation, and was repeated in each gap with 50 new seeds at 3-4 month intervals for one year. Seed Dormancy Experiments To estimate how long seeds of E^_ rivinoides, W. solanacea, and W. coccoloboides can remain dormant in the soil, I determined the viability of cohorts of seeds buried for different periods of time. In December 1981 I collected approximately 850 seeds from 5 to 20 individuals per species. After combining seeds taken from all individuals of a particular species, seeds were randomly assigned to treatments (burial for different periods of time) and then packed in small bags of mosquito netting or in microcentrifuge vials with mesh coverings. All seeds were then buried approximately 15 cm deep at a forest site with approximately 98% canopy cover. At one to two month intervals over the next 17 months, I recovered 50 seeds of each species from the burial site and planted them in 11 plastic cups of forest soil in the center of a large, man-made clearing 40 m away. Seeds were checked at least once every two days for germination. During the dry season, seeds were watered at least every other day. In March 1984, I recovered an additional 50-75 seeds of each species from the burial site and planted them in plastic cups of potting soil in a greenhouse on the University of Florida campus. These seeds, like those germinated in the field, were checked at least every two days until all seeds had germinated, or until no further germination had occurred for four weeks. Gap Dynamics of the Monteverde Cloud Forest From May to July 1983 I set up five permanent 500 m line transects through representative areas of the Lower Montane Wet Forest and Rain Forest zones in the reserve. For each "expanded" gap (the area bounded by lines connecting the trunks of trees bordering the canopy gap; see Runkle 1982) encountered along a transect, I measured the transect interval within the canopy gap (defined as the land area directly beneath the canopy opening), length and orientation of the major and minor axes of the canopy gap, and height of the surrounding canopy. I 2 sampled even the very small gaps (down to 1.6 m ) formed by single branches, because data from germination experiments suggested that even gaps of that size affected germination success in P^ rivinoides, W^ solanacea and W^ coccoloboides. I also subjectively estimated gap age in years. This was easily done for gaps formed in the previous year, because most still contained intact twigs and leaves of the fallen tree, as well as many epiphytes. The proportion of land area occupied by gaps 12 less than one year old was computed as the length of transect under those canopy gaps divided by the total transect length. Gap area was determined using methods described above. I censused the transects again in March 1984 to collect data on gaps formed since the previous July. Mist Netting and Analysis of Fecal Specimens From June 1981 through July 1983, I regularly mist-netted birds in 14 study plots: six in treefall gaps from 1.5 to 3.5 years old, four in large, man-made clearings (hereafter termed "cutover" plots), and four in mature forest with intact canopy. Plots were chosen primarily for another study, and are described in detail in Feinsinger et al. (in review). From June 1981 through July 1982, I netted for the first six hours of daylight (ca. 0515-1115) in two plots of each of the three habitat types each month. Plots used each month were alternated so that sampling effort was approximately equal in all forest and cutover plots, and most treefall plots, over the first 12-month period. From September 1982 through July 1983, I netted at least one day (i.e., for the first 6 hours of daylight) per month in each of three plots, one in each habitat type. For this 11-month period, the same three plots were sampled each month. Additional netting in these and other plots was conducted on an irregular basis. I also netted in one of these plots from 4 to 20 March 1984. All birds captured were weighed, measured, and checked for breeding condition and molt. Frugivores were marked with unique color combinations using plastic leg bands and then retained from 5 to 45 minutes in small holding cages (ca. 20x20x30 cm) to obtain fecal 13 specimens. I also collected samples from many, but not all, insectivorous species. Fecal specimens were stored in 70% ethanol. In the laboratory, I counted and identified all seeds in each sample using a reference collection made over the two-year study. I also visually estimated the percent arthropod composition of each sample to the nearest 10%. Fruit Handling, Gut Treatment, and Seed Passage Rates To determine the consequences to P^ rivinoides, W. solanacea, and W. coccoloboides of fruit consumption by different bird species, I conducted feeding experiments with captive individuals of six bird species observed to eat their fruits. Birds were captured in mist nets and maintained in a small (lxlxlm) cage during the experiments. Between trials, fruits other than the experimental species, as well as water, were provided ad libitum. In all but two cases, trials were completed and the bird was released on the same day. After introducing the experimental fruits into the cage, I noted whether or not birds consumed the fruits, how fruits were ingested (e.g., swallowed whole vs. eaten piecemeal), whether the ingested seeds were voided intact, and whether they were defecated or regurgitated. Recovered seeds, or a subset if many trials were run, were then planted in plastic cups of soil under a screened enclosure in a large clearing. I checked seeds at least once every two days for germination, and watered them when necessary. To determine gut passage rates, I conducted feeding trials in a similar fashion. Approximately 7-15 fruits of either P^ rivinoides, W. solanacea, or W. coccoloboides were introduced on the cage floor, and all other fruits were removed from the cage. I observed subsequent 14 events through a small hole cut in one opaque side of the cage. Birds usually descended from perches to feed within a few minutes after the test fruits were introduced. All uneaten fruits were removed 5 min. after the first fruit was consumed. The midpoint of the interval during which fruits were eaten was considered as the time of ingestion for all fruits in a particular trial. Each time a bird defecated, I recorded the time and the location of the fecal mass on the floor of the cage. After 3-5 fecal masses had accumulated, I removed the paper from the bottom of the cage and replaced it. At the end of the feeding trial, all fecal masses were recovered; seeds were later identified and counted. Successive feeding trials were done approximately 30 min apart; i.e., the next trial (with a different fruit species) began 30 min after the beginning of the previous trial. In this way, I could usually complete 1-2 feeding trials on each bird with each of the three fruit species before releasing it on the afternoon of the same day it was caught. After counting seeds in the fecal masses, I grouped the data into 5-min classes, recording the proportion of all seeds voided in each 5 min time segment following ingestion. Movement Patterns of Frugivores To determine the movement rates and patterns of birds taking P^ rivinoides, W^ solanacea, and W^ coccoloboides fruits in the field, I fitted mist-netted birds with small (ca. 3.5g) radio transmitters and followed their movements for 3-8 days. Transmitters used were homemade units similar to those available from a number of commercial telemetry 15 suppliers. I used an LA-12DS receiver (AVM Instrument Company, Dublin, CA) and a homemade 5-element yagi antenna. Transmitters were attached to the skin and feathers on a bird's back (just anterior to the synsacrum) with Super Glue . Birds fitted with transmitters were held in the field in a small cage for approximately 30 min to ensure that they were healthy when released. By using a carefully mapped network of trails, I could often remain within sight of radiotagged birds for long periods of time. Each time the bird moved to a new location, I simply recorded the time and the bird's location on a map of the study area. When I was out of visual contact with the bird, I determined its location by triangulation. I took compass bearings on the direction of the strongest signal from two points, separated by at least 50 m, on the mapped trail system. After taking the second bearing, I rechecked the first to ensure that the bird had not moved. I took new bearings as soon as the signal received indicated (by a change in signal strength or direction) that the bird had moved. In the absence of any such indication, I took two new bearings every 3-5 minutes to check the bird's location. RESULTS Natural History of the Plants Phytolacca rivinoides is a large herb ranging from Mexico to Bolivia (including the Antilles, Raeder 1961) at elevations from sea level to 3000 m (Standley 1937). Usually among the first colonists of treefalls and landslide edges, individuals commonly spread to cover approximately 25 m2 within 1-2 years of seedling establishment. Plants begin to ripen fruits at about one year of age, but most die (presumably as a result of shading and/or root competition) within 2.5 years of establishment. Of the eight individuals I monitored closely, the median age at death was 24 months (range 21 to 31 months). During the single, extended fruiting season, individuals produce 1,500-30,000 (median = 4700) fruits borne on axillary racemes containing ca. 30-100 fruits each. The fruits are purple-black, about 7.5 mm in diameter, and contain 5-12 (x=9.4, n=20) seeds in a watery pulp. Witheringia solanacea and W^ coccoloboides are both shrubs attaining heights of about 1.5-2.5 m. Witheringia solanacea ranges from Mexico to Brazil, including the Antilles (D'Arcy 1973), occurring from sea level to 2000 m (Standley 1937). Witheringia coccoloboides is typical of cloud forests from Costa Rica to Colombia at elevations from 300 to 2500 m (D'Arcy 1973). Both species grow much more slowly than does P. rivinoides; although seedlings are common in young gaps, they do not attain reproductive size for about 3-5 years, and they usually live for 8 or more years before being shaded out by the reestablishing 16 17 canopy. Fruits of both Witheringia species are red, ca. 10-12 mm in diameter, and are borne in axillary fascicles. Fruit crop size and seed number are highly variable in both species. Total seasonal fruit crops in W. solanacea ranged from 5 to 1084 (median=154, n=121), and seed number per fruit ranged from 6 to 39 (x=22.8, n=44). Seasonal fruit crops in W. coccoloboides ranged from 5 to 1150 (median=120, n=84), and seed number ranged from 46 to 73 (x=59.1, n = 17). Fruits of all three species show typical adaptations for bird dispersal (van der Pij 1 1972). Removal by animals other than birds is probably rare. Although rodents are known to eat fruits of some understory plants, including P^ rivinoides (Denslow and Moermond 1982), I found no evidence of removal by rodents at Monteverde. Early morning counts of fruits marked on the previous afternoon showed no evidence of nocturnal removal, and no fruits were removed from two plants each of W^ solanacea and W. coccoloboides from which birds, but not rodents, were excluded by screened enclosures left open at the bottom (Murray, unpubl. data). In addition, an intensive concurrent study of frugivorous bats revealed no evidence of these fruits in bat fecal specimens (E. Dinerstein, pers. comm.). Fruit Consumers The disperser assemblages for P^ rivinoides, W. solanacea and W. coccoloboides at Monteverde are surprisingly limited. Data from ca. 200 fecal samples collected from mist-netted frugivores, as well as extensive observations by several investigators (Wheelwright et al. 1984), suggest that only ten bird species commonly consume fruits of any of these plants in the Monteverde vicinity. The limited size of the disperser assemblage comes about because few species of frugivorous birds commonly descend to the forest understory or into treefall gaps; similar fruits of canopy trees and epiphytes are often taken by a much larger number of bird species (Wheelwright et al. 1984). The three major dispersers for all three plant species in cloud forest above 1500 m are Black-faced Solitaires (Myadestes melanops, Muscicapidae) , Black and Yellow Silky Flycatchers (Phainoptila melanoxantha, Ptilogonatidae) , and Prong-billed Barbets (Semnornis frantzii, Capitonidae). Of the 360 seeds of these three plant species recovered in fecal specimens from 196 frugivores, all were from these three bird species. Furthermore, these data also suggest that Myadestes is responsible for far more dispersal of these plants than are either Semnornis or Phainoptila: 84% of recovered seeds were from Myadestes alone. Although P. rivinoides, W. solanacea, and W_;_ coccoloboides are highly dependent upon a very few bird species for dispersal services, none of the birds is similarly dependent upon any of the three plant species. The known diets of Myadestes, Phainoptila, and Semnornis include fruits of 51, 14, and 30 species, respectively (Wheelwright et al. 1984; K. G. Murray, unpubl. data). In fact, fruits of the three plants are of relatively minor importance in the diets of these birds. Of the 154 fecal specimens collected from these three species, only 35% contained seeds of P^ rivinoides, W^ solanacea, or W^ coccoloboides. The ecological relationships between these three plants and their dispersers are thus highly asymmetrical. Seven other bird species removed fruits from at least one of the plant species. The tanagers Chlorospingus opthalmicus and Tangara dowii and the finch Pselliophorus tibialis occasionally removed fruits, but 19 failed to ingest most seeds (see below). Of the remaining four species recorded feeding on P^ rivinoides, W. solanacea and W^ coccoloboides, only one was a frequent visitor to any of these plants: at elevations below approximately 1420 m, seeds of W. solanacea were commonly found under display perches of Long-tailed Manakins (Chiroxiphia linearis, Wheelwright et al 1984). Data from mist net captures (Table 1) also suggest the unequal importance of these ten bird species as dispersers for P^ rivinoides, W^ solanacea, and W^ coccoloboides. Of the three primary dispersers, M. melanops was the most frequently captured in all three habitats. In fact, M. melanops may be the most important disperser for all understory plants with bird-disseminated seeds within the Monteverde Cloud Forest Reserve. Capture rates for Myadestes were highly variable over time, however (Fig. 1). While usually very common in the reserve from February through August, they were all but absent from late October through early January. The seasonal decline in capture rate was due to emigration of both adults and young following the breeding season. Visual and auditory censuses confirmed this seasonal pattern of abundance (K. G. Murray, unpubl. data). Where Solitaires go when they leave the Monteverde area remains somewhat a mystery, but D. J- Levey (personal communication) has caught several individuals during this season at Finca La Selva, at ca. 50 m elevation in the Atlantic lowlands. Although some other species of frugivorous birds at Monteverde are also altitudinal migrants (e.g., Three-wattled Bellbirds, Procnias tricarunculata, and Resplendant Quetzals, Pharomachrus moccino; Wheelwright 1983, and K. G. Murray, personal observation), I have no 20 Table 1. Capture data for bird species feeding at least occasionally on fruits of E\_ rivinoides, W. solanacea, and W^ coccoloboides at Monteverde. Total numbers of mist net hours in forest, treefall, and "cutover" (see text) plots were 1158, 1164, and 1449, respectively. Species forest treefalls "cutovers" Myadestes melanops 66 30 33 Phainoptila melanoxantha 1 0 4 Semnornis frantzii Chlorospingus opthalmicus Tangara dowii 0 0 1 Pselliophorus tibialis 1 0 2 6 30 1 0 0 0 0 9 0 0 1 0 2 Capture data from these unusually large (1155-2442 m ) man-made clearings are not included with those from natural treefalls. Plant and bird assemblages in the large clearings were more typical of early second growth habitats than those of natural forest or treefall gaps. .-, 3 5 s m 01 C 4J •fH T) 3 0) T5 0) rD U 0 0 C TJ ■H C T3 0) X! 22 o o o o UnOH-13N U3d Q3anidV0 sdisdpeAw CO 00 0) C\J CO 00 0) 23 evidence that any other disperser of P^ rivinoides, W^_ solanacea, and W^ coccoloboides undertakes such annual movements. Fruit Handling and Seed Treatment in the Gut Consumers of P. rivinoides, W. solanacea, and VL_ coccoloboides at Monteverde handled fruits by one of two methods. Myadestes, Phainoptila, and Semnornis invariably swallowed fruits whole, with little or no manipulation in the bill. In contrast, the tanagers Chlorospingus opthalmicus and Tangara dowii, and the finch Pselliophorus tibialis, mashed fruits extensively in the bill before swallowing. This behavior resulted in the fruit skin and many of the seeds being dropped before the pulp was ingested. Field observations of these and other tanager and finch species suggest that most handle fruits in this manner. As a result, these birds ingest and disperse few, if any, of the seeds they remove from most plants. The probability of seed ingestion in tanagers and finches seems to depend at least in part on seed size. In Pselliophorus, Chlorospingus, and Tangara, most seeds were discarded along with the fruit skin during handling (Table 2). Nevertheless, some W^ solanacea seeds (ca. 1.5 mm diameter) were ingested by all three species, especially by Pselliophorus. In contrast, none of the birds ingested any of the larger seeds of W. coccoloboides (ca. 2.4 mm diameter); all were discarded with the fruit skin. For seeds of a given size, the probability of ingestion increases with bird size. P^ tibialis (ca. 30.5 g; gape 10.3 mm) ingested 71% of the W^ solanacea seeds offered, whereas C. opthalmicus (ca. 20.0 g ; gape 9.1 mm) and T. dowii (ca. 20.0 g; gape 8.5 mm) ingested only 10.7% and 15.8%, respectively. 2 4 Apparently, Larger seeds are more easily separated from the fruit pulp during manipulation in the mandibles, especially by birds with smaller bills. Data on the seed loads recovered from mist-netted tanagers at Monteverde support this suggestion: feces of these birds generally contained only the minute (ca. 0.2-.06 mm diameter) seeds from species of Ericaceae, Melastomataceae, and Gesneriaceae (K. G. Murray, unpubl. data). Small tanagers such as Chlorospingus and Tangara may act as dispersers only for plants with such minute seeds. The effect of gut passage on seeds also varies among bird species. Data from feeding trials suggest that although many seeds of W^ solanacea may be ingested by Pselliophorus, very few survive passage through the gut (Table 2). Instead, most seeds were apparently ground up in the gut; feces of the individual used in this experiment contained large numbers of recognizable W^ solanacea seed fragments. Only two W. solanacea seeds emerged intact, and these were inviable (Table 3). The absence of seed fragments in feces of the same bird after feeding on W. coccoloboides fruits again strongly suggests that seeds of this species are not ingested by Pselliophorus. Data for Chlorospingus and Tangara suggest that the few W. solanacea seeds that are ingested pass through the gut intact (Table 2); no evidence of destruction in the gut (such as seed fragments in the feces) was found, and the few seeds recovered from feces were fully viable (Table 3). Seeds eaten by Myadestes, Phainoptila, and Semnornis were always voided intact. Although I found no evidence of either increased or decreased germination success (defined simply as the percent of seeds that germinated following gut passage) as a result of gut passage in any of these birds, the rate at which seeds of ail three plant species 25 Table 2. Fruit handling techniques and gut treatment effects on seeds eaten by captive individuals of six frugivore species. Bird Plant seed fruits seeds seeds voided species b species P.r. diao 2 :eter (mm) eaten dropped ingested intact M.m. 0 53 0 411 411 W.s. 1 5 69 0 1366 1366 W.c. 2 4 36 0 1206 1206 P.m. P.r. 17 0 168 168 W.s. 19 0 447 447 W.c. 18 0 524 524 S.f . P.r. 36 0 413 413 W.s. 7 0 145 145 W.c. 8 0 477 477 Co. W.s. 3 16 3 3 W.c. 4 36 0 _ T.d. W.s. 2 25 3 3 P.t. W.s. 9 38 95 2 W.c. 4 111 0 M.m.= Myadestes melanops , P.m.= Phainoptila melanoxantha, S.f.= Semnornis frantzii, C.o.= Chlorospingus opthalmicus, T.d. = Tangara dowii, P. t.= Pselliophorus tibialis P . r . = Phytolacca rivinoides , W . s . = Witheringia solanacea, W.c . = Witheringia coccoloboides Of seeds ingested 26 Table 3. Effects of gut passage on germination success and germination rate. Data on untreated controls taken from Table 4. percent germination (n) days to 95% germination Bird species Plant a species P.r. W.s. W.c. tre 78 73 ;ated untreated treated untreated M.m. (100) (100) d 89 86 86 (100) (100) (100) 22 45 31 49 56 56 P.m. P.r. W.s. W.c. 89 (100) d d 89 86 86 (100) (100) (100) 37 73 54 49 56 56 S.f . P.r. W.s. W.c. 75 (100) d d 89 86 86 (100) (100) (100) 26 19 19 49 56 56 Co. W.s. 100 (3) 86 (100) d d T.d. W.s. 100 (3) 86 (100) d d P.t. W.s. 0 (2) 86 (100) d d a M.m.* Myadestes melanops, P. m.= Phainoptila melanoxantha, .o.= Chlorospingus opthalmicus Pselliophorus tibialis S.f. T.d. = Semnornis frantzii, C = Tangara dowii, P.t.= b P.r.* = Phytolacca rivinoides, = Witheringia coccolobo W.s ides . = Witherin gia solanacea, W.c. c Of those that germinated d Insufficient number of seeds available for experiment 27 germinated was often enhanced by gut passage (Table 3). Thus, although treatment in a bird gut is not reguired for germination in any of these plants, seedlings from treated seeds may gain a competitive advantage through rapid germination in a newly created patch of suitable habitat. Spatial and Temporal Distribution of Suitable Colonization Sites Germination Reguirements Gap vs. understory comparisons. Results of forest vs. gap germination experiments (Table 4) show that after 60 days, all three species had significantly higher germination success under gap conditions than under closed canopy. Many Witheringia seeds did eventually germinate in the forest after more than a year. These seeds, however, were protected from litter fall by the screened enclosure. Ordinarily, seeds on the forest floor would be covered by leaf litter and incorporated into the soil seed bank in a dormant state long before they germinated. Germination success vs. gap size. Germination success increased with increasing gap size in all three species (Fig. 2). In fact, slopes of the regressions (on transformed variables; see Fig. 2 legend) of germination success on gap area do not differ significantly among the three species (F =1.550 with df=2,15, 0.1 < P < 0.25). Furthermore, analysis of covariance shows that the regression lines for the two Witheringia species are indistinguishable (Fs=0.07 with 1,17 df, P > .75), but that the adjusted mean germination success in P. rivinoides is less than that for the other two species (Fs=12.82 with 1,17 df, P < .005). Eguations for the adjusted (by analysis of covariance) regressions are y = 6.84x + 12.88 for both V^_ solanacea and W^ Table 4. Percent germination success in forest and large gap habitats. Sample size for all experiments was 100. Differences between gap and forest values were tested with a test for equality of two percentages (Sokal and Rohlf 1969: 608). gap Phytolacca rivinoides Witheringia coccoloboides forest after 60 days 0 <-001 Witheringia solanacea 86 14 <-001 Witheringia coccoloboides 86 <.001 after 410 days Phytolacca rivinoides 89 0 <.001 Witheringia solanacea 86 61 < . 001 17 >-5 29 coccoloboides, and y = 6.84x + 1.14 for P^ rivinoides, where y is the arcsin transform of the proportion of seeds germinating and x = ln(gap area + 1). Thus, germination success increases with gap size at the same rate in all three species, but for a given gap size, germination success in P. rivinoides is always less than for either species of Witheringia. Consequently, P^ rivinoides requires larger gaps than either species of Witheringia for germination. Such differences in the relationship between gap size and germination success translate directly into differences among species in the distribution of suitable germination sites over the landscape. Germination success vs. gap age. Seeds of P^ rivinoides, W. solanacea and W. coccoloboides also differ in the relationship between germination success and gap age (Fig. 3). Because the gaps used were of different sizes, data plotted in Figure 3 were adjusted to control for the effects of gap size, according to the relationships in Figure 2. To facilitate comparison among species, data were also scaled such that the highest germination success attained in each species was set at 100%. Germination success decreased with increasing gap age in all three species, presumably as a result of decreasing light intensity (or quality) as the understory vegetation within the gap grew and shaded more of the soil surface. The initial increase in germination success of P. rivinoides may have resulted from increased light intensity or quality in the first few months after gap formation, as the leaves and epiphytes on fallen trees and branches decayed and fell to the ground. Such an increase in light intensity or quality would be expected to have the greatest effect on an extremely shade-intolerant species such as Pj_ rivinoides . Figure 2. Germination success vs. gap area. Results from germination experiments in 6 recent gaps and 1 forest understory site (gap area=0). Curves shown are de-transformed linear regressions of the proportion of seeds germinating (arcsin transformed) on In (gap area + 1). Equations, F-values, and significance levels for P^ rivinoides, W. solanacea and W. coccoloboides are y = 6.99x + 0.54 (F = 71.8, p < .001), y = 5.15x + 20.08 (F=10.11, p < .05), and y = 8.36x + 6.35 (F=40.35, p < .002), respectively. 31 60-i Phytolacca rivinoides DC • ^-^ 4J 4°- H 2 2°- • o DC 111 i 80 "I Witheringia coccoloboides 60- 40- 100 200 300 400 GAP AREA (m2) Figure 3. Germination success vs. gap age. Results from germination experiments in 4 gaps as they aged naturally (see text). Missing data for W. solanacea at 3.5 months and for W^ coccoloboides at 1.5 and 3.5 months are due to a lack of sufficient seeds for those experiments. Different symbols indicate values for each of the 4 gaps. Lines connect mean germination success values at each gap age. 33 Phytolacca rivinoides i «g i — i — f — ' — f*- Witheringia solanacea 2 4 6 8 10 GAP AGE (months) 34 Following the initial increase in P^ rivinoides, germination success decreased with increasing gap age much more rapidly than in either species of Witheringia. In fact, germination success in P^ rivinoides was negligible by 7 months after gap formation, whereas some W. coccoloboides seeds germinated in gaps as old as 12 months. Germination success decreased least rapidly with increasing gap age in W. solanacea, although it reached zero by 10 months (Fig. 3). Thus, a given gap remains open for colonization by W^ coccoloboides and W^ solanacea for some time after it is no longer suitable for P^ rivinoides . Seed dormancy. In all three plant species, seeds buried for up to 27 months showed no significant decrease in viability (Figure 4). Mean germination success for all seeds was similar in all three species; values for P. rivinoides, W. solanacea, and W^ coccoloboides were 65%, 50%, and 55%, respectively. In a similar experiment (K.G. Murray, unpubl. data), I collected 100-200 seeds of each species at approximately two-month intervals for the same 27-month period and buried these seeds together in a similar forested site. These seeds were recovered in March 1984 and planted in the greenhouse. The results of this experiment were similar to those obtained in the previously described one: no decrease in seed viability was demonstrated in the first 27 months of burial. Spatial Distribution of "Safe Sites" New canopy gaps covered approximately 1.5% of the total land area sampled by forest transects each year. Percentages of the five forest transects under new canopy gaps (less than 1 year old) were 0.2, 3.1, Figure 4. Results of seed dormancy experiments with P^ rivinoides, W. solanacea, and W^ coccoloboides, and results of regression analyses on germination success vs. seed burial period. 36 90 -i 60- 30 - Phytolacca rivinoides (.25< p<.5) 90 -i E 60-. s '- M. Witheringia solanacea * ys-0.92 x + 55.8 (.05
400 m2. To determine the density and
coverage (proportion of land area) of gaps in each category that are
formed each year, I used a modification of the methods of Lucas and
Seber (1977) for line transect data. Because the gaps censused in this
study were actually formed over a period of several years, I weighted
the coverage estimates such that the total area in gaps (over all size
categories) eguals 1.5% of total land area. Density estimates were
weighted in a similar manner, so that all final values are expressed on
a per-year basis.
I used this analysis to approximate the availability of suitable
germination sites over the landscape. For purposes of illustration, let
us arbitrarily define a "safe site" with respect to gap size as any gap
in which germination success is at least 25%. My use of the term "safe
site" here is not exactly equivalent to that of Harper (1977), since one
gap could provide many germination sites, and each of these would be
termed a "safe site" by Harper's definition. Figure 6 shows the density
of safe sites and the proportion of land area they occupy as a function
of minimum safe site area, using the gap density and coverage estimates
derived above. Both density and land area covered decrease rapidly with
increasing minimum safe site area. For a plant that requires a gap of
at least 100 m2 (e.g., a circular gap of 11.3 m diameter) as a safe
site, for example, there is approximately 1.0 safe site per hectare, and
0.62% of the total land area is available for colonization. For a plant
2
whose seeds can germinate in a much smaller gap, however, say 10 m
(e.g., a circular gap of 3.6 m diameter), suitable patches for
40
colonization are much more common: 6.0 "safe sites" per hectare,
representing 1.32% of the total land area.
Similar analyses demonstrate that suitable germination sites are
indeed distributed differently for the species in this study. Minimun
gap sizes in which germination success is at least 25% (based on the
2
regression lines in Figure 1) are 66.7, 5.9, and 15.9 m for P.
rivinoides, W. solanacea, and W. coccoloboides, respectively. Thus,
from Fig. 6, we can estimate approximately 1.6, 8.8, and 4.3 suitable
patches per hectare, representing 0.8, 1.4, 1.2% of the total land area.
The foregoing discussion treated the availability of suitable
patches only on the basis of gap size and its effect on germination
success; i.e., it assumes that all gaps formed in a particular year are
equally suitable for colonization at any time. Since germination
success varies among the species with respect to gap age as well as to
gap size, however, the availability of suitable colonization sites
varies among species temporally as well as spatially. If we again
arbitrarily define the length of time a gap remains open for
colonization as the length of time during which germination success
remains at least 25%, then for P^ rivinoides, W. solanacea, and W.
coccoloboides gaps remain open for colonization for approximately 4.5,
8.0, and 5.5 months, respectively. Figure 7 shows the density of safe
sites and the proportion of land area they contain as a function of time
of year, for plants that can colonize gaps up to 4, 6, and 8 months old.
The figure was generated by multiplying both the canopy disturbance rate
of 1.5% / year or the overall gap density of 17.5 gaps / hectare / year
by the estimated proportion of gaps occurring in each month. The result
(the line labelled "0 months") is the density of gaps formed that month,
41
or the proportion of land area they occupy. Other lines in the figure
were generated by including, for each month, the density of new gaps or
the proportion of land area disturbed in the 4, 6, or 8 previous months.
For species capable of invading only very young gaps, suitable
colonization sites are available for only a short period of time each
year (Fig. 7). For species capable of colonizing older gaps, however,
the availability of suitable colonization sites remains high for a much
longer period of time. For example, suitable colonization sites for W^
solanacea are relatively common for 9 months of the year, while those
for P. rivinoides are common for only 5 months.
Although these analyses are useful for gaining a gualitative
impression of the relationship between germination reguirements and the
availability of suitable habitat patches over the landscape, data
presented in Figures 6 and 7 clearly show that applying the concept of
"safe site" to treefall gaps oversimplifies the relationship between
germination reguirements and availability of suitable patches over the
landscape. The effects of gap size and age on germination are not
threshold effects, in which germination success in gaps below a certain
size or above a certain age is zero and that in younger or larger gaps
is 100%. Instead, germination success is a continuous function of both
gap size and age, and each gap size has an associated germination
probability for each plant species.
Seed Shadows Produced by Birds
Seed Passage Rates
Most birds fed on fruits placed in the experimental cage soon after
the fruits were introduced. In most cases, birds ate 4-10 fruits
43
(1V101 dO %)
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44
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MINUTES AFTER INGESTION
Figure 8 -- continued
<
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Figure 8 -- continued
49
Table 5. Summary of differences among median seed retention times, (A)
among bird species within plant species, and (B) among plant
species within bird species. Based on multisample median tests
(Zar 1984:179-180) and subdivisions of the multisample
contingency tables (Zar 1984: 69-70).
A. plant species comparisons
Phytolacca rivinoides
Witheringia solanacea
Witheringia coccoloboides
**
St
> Mm
Pm
**
St
= Mm
> Pm
**
St
Mm
> Pm
B. bird species comparisons
* * **
Phainoptila melanoxantha Pr > ^ Wc > ^^ Ws
Myadestes melanops Pr >++ Wc >^ Ws
Semnornis frantzii Pr > Wc > Ws
p < .05
p < .005
50
be about equally easily extracted from the pulp. In fact, P^ rivinoides
fruits are slightly smaller than those of either Witheringia species and
have a more watery, amorphous pulp. It would seem that seeds would be
most easily separated from this pulp, yet retention times were
consistently longer in P. rivinoides than in the two Witheringia
species. Fruits of W^ solanacea and W^ coccoloboides may contain a
compound with laxative properties, or perhaps P. rivinoides contains a
compound having the opposite effect.
Median passage times vary systematically among bird species as
well. For seeds of all three plant species, passage times are longer in
Semnornis than in Phainoptila (Table 5). Median passage times in
Myadestes were generally intermediate between those in Semnornis and
Phainoptila, but were statistically indistinguishable from those of one
or the other bird species for seeds of each plant.
Several features of the seed retention distributions in Figure 8
are important to the relationship between gut passage times and the
spatial patterns of seeds produced by an actively foraging bird. First,
seeds ingested at one point in time do not emerge from the gut together;
in these experiments, the last seeds emerged more than 7 5 minutes after
the first-emerging seeds ingested at the same time. Second, the
distributions of retention times are not symmetrical, but instead are
skewed to the right. As a result, neither the length of time for the
appearance of the first-voided seeds, pulp, or marker stain (e.g.,
Herrera 1984, Holthuijzen and Adkisson 1984, Sorensen 1984) nor the
mean seed retention time (e.g., Walsberg 1975) is likely to provide
complete information for inferring seed dispersal patterns. Third,
although retention times are variable in all cases, the variation is
51
greater in some bird species than in others. For example, coefficients
of variation for P. rivinoides passage times in Myadestes, Semnornis,
and Phainoptila were 44.5, 35.9, and 9.2, respectively. Clearly, any
inferences about the seed shadows produced by animals must be based on a
consideration of the entire frequency distribution of retention times,
rather than on a descriptive statistic (e.g., mean, median, mode, etc.)
derived from it.
Movement Patterns of Frugivorous Birds
A total of 195.7 hours of data on movement patterns was collected
from 8 birds of three species. Totals for Myadestes melanops,
Phainoptila melanoxantha, and Semnornis f rantzii, respectively, were 4
individuals for 96.2 total hours, 3 individuals for 90.3 hours, and 1
individual for 9.3 hours. I also attached transmitters to eight other
individual Myadestes, one Phainoptila, and one Semnornis, but I was
unable to collect enough data on these birds to include here.
Transmitters fell off two of these birds less than one day after the
birds' release. In five other cases, the tagged individual moved out of
the area before I could begin tracking it. These five individuals were
non- territorial birds that foraged over very large areas of the forest.
The few hours of data collected from two of these birds indicate that
they did not move more rapidly through the forest than those on well-
defined home ranges; rather, their movements were simply more linear
than those of other individuals of the same species, which turned more
often. Seeds dispersed by a particular widely foraging bird are thus
unlikely to travel much farther from their source than those dispersed
by birds with more restricted home ranges.
52
Birds fitted with transmitters generally showed no adverse effects
of carrying the 3.5 g package. Within 2 hours of release, most
individuals had begun foraging actively and chasing territory intruders.
Data from two individuals that did not adjust quickly to carrying the
transmitter were not used in the analysis.
Foraging behavior of the primarily frugivorous Myadestes,
Phainoptila, and Semnornis resulted in very different movement patterns
than those of primarily insectivorous birds. Whereas most insectivores
seem to move through the forest almost continuously while feeding, the
frugivores studied here punctuated brief episodes of rapid movement with
relatively long stationary periods. Radio tracking data indicate that
birds generally spent 7 to 1 2 minutes in one location (Table 6),
presumably consuming and processing fruits, and then moved rapidly to
another location without feeding along the way. Not surprisingly, this
pattern corresponds well with the patchy distribution of fruiting
plants. In addition, the mean times between successive movements in
Table 6 correspond closely with behavior I noted during feeding
experiments with captive birds: after eating a number of fruits, most
birds perched nearly motionless for approximately 10 minutes before
moving about the cage in search of more fruit. The fact that data from
remotely monitored birds correspond well with the behavior of closely
observed individuals again suggests that the transmitters did not
interfere with normal foraging activity.
Movement patterns of radio-tracked birds did not suggest any
tendency for gap-to-gap movement. Rather, birds seemed to travel
rapidly between well-defined fruit sources, regardless of where they
occurred. Locations to which birds returned frequently were always
53
found to be large fruiting plants such as trees, rather than gaps.
Furthermore, data from mist-net captures and analysis of fecal specimens
suggest no tendency for pref errential foraging in gaps. First, none of
the frugivore species was captured more freguently in gaps than in
forest (Table 1). Indeed, one species (Myadestes melanopsj was captured
significantly more often in forest (X2 = 12.942, p < .001; expected
values corrected for differences in sampling effort). Second, over 82%
of the fecal specimens from mist-netted Myadestes, Phainoptila, and
Semnornis contained seeds of canopy or subcanopy trees and epiphytes,
suggesting that these birds concentrate much of their foraging outside
gaps. Thus, although these three bird species are the primary
dispersers of the gap-dependent P^ rivinoides, W^_ solanacea, and W^.
coccoloboides, there is no reason to suspect that they commonly
transport seeds of any of these plants directly to other gaps in a non-
random fashion.
Mean distances and time intervals between successive bird movements
varied more among individuals of a given species than among species
(Table 6). This variation may reflect different densities of fruit
sources within different birds' feeding ranges or between different
seasons. Without collecting data from numerous individuals of each
species throughout the year, it is impossible to identify sources of
variation in movement patterns more precisely. Because variation among
individuals within species was so high, data from each individual were
weighted egually for purposes of estimating seed shadows. Individuals
from which I was able to collect more extensive data are thus not
overrepresented in the analysis.
54
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