UNIVERSITY OF CALGARY
Quantity, Quality and Spatial Patterns of Seed Dispersal by
Cebus capucinus
by
KIM LISA VALENTA
A THESIS
SUBMITTED TO THE FACULTY OF GRADUATE STUDIES
IN PARTIAL FULFILMENT OF THE REQUIREMENTS FOR THE
DEGREE OF MASTER OF ARTS
DEPARTMENT OF ANTHROPOLOGY
CALGARY, ALBERTA
SEPTEMBER, 2007
© Kim Lisa Valenta 2007
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Abstract
From May to July 2005, and January to July, 2006, I collected 393.5 hours of
focal data on two habituated groups of white-faced capuchin monkeys (Cebus
capucinus), as well as planting and monitoring 3,157 individual seeds of 18 species in order to address three facets of capuchin’s effect on the fruiting plant species they consume: Quantity, quality, and the spatial pattern of dispersed seeds. Capuchins were found to consume and disperse a high number and diversity of seeds intact. Additionally, passage through the capuchin intestinal system, in 3 of 5 cases, significantly increases seed germination. Capuchins were also found to disperse seeds to locations that were suitable for their survival, germination and growth. Seed survival, germination and growth was found to be consistently affected by the distance that seeds are deposited away from fruiting trees of the same species, which provides support for a modified version of the Janzen-Connell model.
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Acknowledgements
Many individuals contributed to the completion of this project, without whom the experience would not have been nearly so rewarding. Firstly, I thank Linda Fedigan, without whom none of this would have been possible. Her incredible insight and direction have done a great deal to shape this project, as well as my understanding of what it means to be a researcher. It is a privilege to have worked with her guidance.
For helping me fight the uphill battle of data analysis with tireless cheer and remarkable patience I thank Drs. Tak Shin Fung and John Addicott, who never left a question unanswered, nor a violated assumption unturned.
For their great patience and willingness to have me and to answer my billions of questions, I thank the staff of Santa Rosa National Park.
For being the most remarkable field assistant a girl could hope for, as well as for her excellent dancing and unflagging optimism, I thank Mel Luinstra.
For all of their support, friendship, games of SET! and Sharpie hijinx, I thank
Elvin, Sarah, Grainne, Eugenia, Norbees, Nicola, Amanda, Courtney, Anna, Fernando,
Greg, Dan, Dean, Gillian L, Sal, Mari, Derby and Jeff.
For their guidance with this project, and throughout this entire process, I thank the teachers who helped to shape my experience: Drs. Pascale Sicotte, Mary Pavelka, Steig
Johnson, Brian Keating and Anne Katzenberg.
For her capacity to understand things I don’t and for always being there, I thank
Erins. For her humor and beans I thank Muffy.
For making all of this possible, I thank Gillian, Nikki, Mom and Dad.
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For his endless support, countless plane tickets, and invaluable advice and help on many aspects of this project, I thank John Paul, and look forward to returning the favour.
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Table of Contents
Approval Page…………………………………………………………………………….ii Abstract…………………………………………………………………………………...iii Acknowledgements……………………………………………………………………….iv Table of Contents…………………………………………………………………………vi List of Tables……………………………………………………………………………...x List of Figures and Illustrations………………………………………………………….xii
CHAPTER ONE: INTRODUCTION...... 1 1.1 Coevolutionary Models...... 2 1.2 The Seed Escape Hypothesis ...... 4 1.3 The Colonization Hypothesis...... 4 1.4 Environmental Homogeneity...... 5 1.5 Seed Handling...... 6 1.6 Gut Passage...... 6 1.7 Secondary Dispersal and Predation ...... 7 1.8 The Effect of Feces...... 8 1.9 Previous Studies of Seed Dispersal by White-Faced Capuchin Monkeys...... 9 1.10 The Current Study...... 9 1.11 Summary and Significance ...... 11
CHAPTER TWO: QUANTIFYING SEED DISPERSAL BY WHITE-FACED CAPUCHINS...... 13 2.1 Introduction...... 13 2.2 Research Questions and Predictions...... 15 2.2.1 Research Questions...... 15 2.2.2 Predictions ...... 15 2.3 Methods ...... 16 2.3.1 Study Site...... 16 2.3.2 Study Subjects ...... 17 2.3.3 Data Collection and Analysis ...... 17 2.3.4 Degree of Frugivory ...... 19 2.3.5 Diversity of Fruit Consumption and Passage ...... 20 2.3.6 Seeds and Species Passed ...... 20 2.3.7 Number of Defecations Containing Seeds...... 21 2.3.8 Frequency and Rate of Seed Dispersal ...... 21 2.3.9 Animal Density...... 21 2.4 Results...... 22 2.4.1 Degree of Frugivory ...... 22 2.4.2 Diversity of Fruit Consumption and Passage ...... 23 2.4.3 Number of Defecations Containing Seeds...... 23 2.4.4 Frequency and Rate of Seed Dispersal ...... 23 2.4.5 Animal Density...... 24 2.4.6 Comparison with Prior Studies...... 25 2.5 Discussion...... 25
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2.5.1 Degree of Frugivory ...... 25 2.5.2 Diversity of Fruit Consumption and Passage ...... 26 2.5.3 Seeds and Species Passed ...... 26 2.5.4 Number of Defecations Containing Seeds...... 27 2.5.5 Frequency and Rate of Seed Dispersal ...... 27 2.5.6 Animal Density...... 28 2.5.7 Seed Rain ...... 28 2.6 Conclusion ...... 29
CHAPTER THREE: EVALUATING THE QUALITY OF SEED DISPERSAL BY WHITE-FACED CAPUCHINS (CEBUS CAPUCINUS) ...... 38 3.1 Introduction...... 38 3.2 Research Questions and Predictions...... 41 3.2.1 Research Questions...... 41 3.2.2 Predictions ...... 41 3.3 Methods ...... 42 3.3.1 Study Site...... 42 3.3.2 Study Subjects ...... 43 3.3.3 Data Collection ...... 43 3.3.4 Seed Handling...... 45 3.3.5 Germination Experiments...... 45 3.4 Analysis ...... 47 3.4.1 The Effect of Feces and Gut Passage on Germination ...... 47 3.4.2 The Effect of Feces and Gut Passage on Time to Germination...... 47 3.5 Results...... 48 3.5.1 Seed Handling...... 48 3.5.2 The Effect of Gut Passage on Germination Rates ...... 48 3.5.3 The Effect of Gut Passage on Germination Latency ...... 48 3.5.4 The Effect of Feces on Germination Rates...... 49 3.5.5 The Effect of Feces on Germination Latency...... 49 3.5.6 The Effect of Monkey Treatment on Germination Rates Across All Species..50 3.6 Discussion...... 51 3.6.1 Seed Treatment ...... 51 3.6.2 The Effect of Gut Passage and Feces on Germination ...... 52 3.6.3 The Effect of Feces and Gut Passage on Time to Germination...... 54 3.6.4 Seed Treatment and Seed Germination across all Plant Species...... 55 3.7 Conclusion ...... 57
CHAPTER FOUR: SPATIAL PATTERNS OF SEED DISPERSAL BY WHITE- FACED CAPUCHINS (CEBUS CAPUCINUS) AND IMPLICATIONS FOR SEED SURVIVAL ...... 67 4.1 Introduction...... 67 4.1.1 The Janzen-Connell Model and the Seed Escape Hypothesis ...... 68 4.1.2 Colonization Hypothesis...... 69 4.1.3 Environmental Homogeneity...... 69 4.1.4 Measuring the Effect of Distance ...... 70
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4.2 Research Questions and Predictions...... 71 4.2.1 Research Questions...... 71 4.2.2 Predictions ...... 71 4.3 Methods ...... 72 4.3.1 Study Site...... 72 4.3.2 Study Subjects ...... 73 4.3.3 Data Collection ...... 73 4.3.4 Dispersal Distances...... 75 4.3.5 Defecated Seed Quadrats...... 76 4.3.6 Spit Seed Quadrats...... 78 4.3.7 Seedling Quadrats...... 79 4.3.8 The Dispersal Pattern of Feces ...... 80 4.4 Analysis ...... 81 4.4.1 Coefficient of Dispersion...... 82 4.5 Results...... 83 4.5.1 Dispersal Times and Distances...... 83 4.5.2 Effect of Distance and Microhabitat Variables on Seed Survival, Germination and Seedling Establishment...... 83 4.5.3 Effect of Distance and Microhabitat Variables on Seedling Survival...... 84 4.5.4 Effect of Distance and Microhabitat Variables on the Duration of Defecated Seed Survival...... 85 4.5.5 Effect of Distance and Microhabitat Variables on the Time to Defecated Seed Removal ...... 86 4.5.6 Effect of Distance and Microhabitat Variables on the Duration of Spit Seed Survival...... 87 4.5.7 Effect of Distance and Microhabitat Variables on the Time to Spit Seed Removal...... 88 4.5.8 Effect of Distance and Microhabitat Variables on Seedling Growth and Damage ...... 88 4.5.9 Dispersal Patterns of Capuchin Feces: The Coefficient of Dispersion...... 89 4.6 Discussion...... 89 4.6.1 Dispersal Patterns and Distances ...... 89 4.6.2 The Effect of Distance and Microhabitat Variables on Defecated Seed Survival and Germination...... 90 4.6.3 The Effect of Distance and Microhabitat Variables on Spit Seed Survival and Germination ...... 92 4.6.4 The Effect of Distance and Microhabitat Variables on Seedling Survival and Growth ...... 92 4.6.5 The Effect of Distance and Microhabitat Variables Across Species and Survival and Growth Variables...... 93 4.6.6 Evaluating the Janzen-Connell Model and the Seed Escape Hypothesis ...... 94 4.7 Conclusion ...... 96
CHAPTER FIVE: CONCLUSION...... 115 5.1 Summary of Results...... 115 5.2 Integration of Results...... 118
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5.3 Contributions and Future Directions...... 119 5.4 Conclusion ...... 121
REFERENCES ...... 122
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List of Tables
Table 2.1 Fruiting tree visitation…………....………………………………………...….31
Table 2.2 List of seed-bearing plant species consumed and passed intact………………32
Table 2.3 Number of species and intact seeds passed per defecation……………………33
Table 2.4 Comparison of the results of three seed dispersal studies of Cebus capucinus………………………………………………………………33
Table 3.1 Ethogram of seed treatment…………………………………………………...58
Table 3.2 Summary of germination experiments………………………………………...58
Table 3.3 Fruit treatment across all 27 species sampled…………………………………58
Table 3.4 Seed treatment by species……………………………………………………..59
Table 3.5 Summary of all germination experiments……………………………………..60
Table 4.1 The effect of distance and microhabitat variables on seed survival until the end of the study period……………………………….97
Table 4.2 The effect of distance and microhabitat variables on seed germination……………………………………………………………...97
Table 4.3 The effect of distance and microhabitat variables on seedling establishment………………………………………………………..98
Table 4.4 The effect of distance and microhabitat variables on seedling survival……………………………………………………………...98
Table 4.5 The effect of distance and microhabitat variables on the number of days seeds remain in quadrats………………………………...99
Table 4.6 The effect of distance and microhabitat variables on the number of days that elapse prior to the removal of all seeds from quadrats………………………………………………………..99
Table 4.7 The effect of distance and microhabitat variables on the number of days spit seeds remain in spit seed quadrats…………………100
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Table 4.8 The effect of distance and microhabitat variables on the number of days that elapse prior to total seed removal from spit seed quadrats…………………………………………………………100
Table 4.9 Effects of distance and microhabitat variables on seedling growth and damage…………………………...……………………101
Table 4.10 The effect of distance and microhabitat variables on seed and seedling survival, germination and growth………………………..102
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List of Figures and Illustrations
Figure 2.1 Bar graph depicting the percentage of time spent per activity, CP and LV combined, wet season………………………………….34
Figure 2.2 Bar graph depicting the percentage of time spent per activity, CP and LV combined, dry season…………………………………..34
Figure 2.3 Bar graph depicting activity budget differences between seasons, CP and LV combined…………………………………………35
Figure 2.4 Map of CP home range, showing 95% of range use and 50% of range use…………………………………………………………….36
Figure 2.5 Map of LV home range, showing 95% of range use and 50% of range use…………………………………………………………….37
Figure 3.1 Possible effects of gut passage and feces on germination rate and latency…………………………………………………………………..61
Figure 3.2 Equation for the Proportion of Difference Analysis…………………………61
Figure 3.3 Equation for the Test for Differences Between Means………………………62
Figure 3.4 Bar graph depicting the effect of gut passage on germination rates…………………………………………………….………..62
Figure 3.5 Bar graph depicting the effect of gut passage on germination latency…………………………………………………………...63
Figure 3.6 Bar graph depicting the effect of feces on germination rates……………………………………………………………..64
Figure 3.7 Bar graph depicting the effect of feces on germination latency…………………………………………………………..65
Figure 3.8 Photographs of the five most commonly consumed fruits of the 2005 and 2006 field season…………………………………………66
Figure 4.1 Map showing the home range of CP with 50x50 meter grid squares superimposed…………………………………………………………..103
Figure 4.2 Map showing the home range of LV with 50x50 meter grid squares superimposed…………………………………………………………..104
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Figure 4.3 Frequency distribution of the distance of seeds deposited from parent trees……………………………………………………..105
Figure 4.4 Cumulative frequency distributions of distance that seeds of the five most commonly consumed seeds are dispersed away from parent trees versus nearest fruiting conspecific trees…………………………..105
Figure 4.5 Frequency distribution of gut retention times………………………………108
Figure 4.6 Frequency distribution of distances between consecutive defecation events…………………………………………………..108
Figure 4.7 Frequency distribution of time between Consecutive defecation events………………………………………………….109
Figure 4.8 Bubble plot depicting the effect of canopy openness on seed survival to the end of the study period for Genipa americana………...109
Figure 4.9 Bubble plot depicting the effect of distance to nearest fruiting conspecific tree on seed survival to the end of the study period for Genipa americana…………………………………………….110
Figure 4.10 Bubble plot depicting the effect of distance to nearest fruiting conspecific tree on seed survival to the end of the study period for Casearia arguta……………………………………………….110
Figure 4.11 Bubble plot depicting the effect of distance to nearest fruiting conspecific tree on seed germination for Genipa americana………….111
Figure 4.12 Bubble plot depicting the effect of the diameter at breast height (DBH) of the nearest fruiting conspecific tree on seed germination for Genipa americana……………………………………………..111
Figure 4.13 Bubble plot depicting the effect of canopy openness on seed germination for Genipa americana………………………………………..112
Figure 4.14 Bubble plot depicting the effect of distance to nearest fruiting conspecific tree on seed germination for Casearia arguta…………….112
Figure 4.15 Bubble plot depicting the effect of distance to parent tree on seedling survival to the end of the study period for Genipa americana……113
Figure 4.16 Bubble plot depicting the effect of distance to nearest fruiting conspecific tree on seedling survival to the end of the study period for Genipa americana………………………………………...113
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Figure 4.17 Bubble plot depicting the effect of distance to nearest fruiting conspecific tree on seedling survival to the end of the study period for Casearia arguta…………………………………………...114
xiv 1 Chapter One: Introduction
There is an ongoing debate regarding the role of frugivores in the process of seed dispersal (Chapman and Chapman 2001). This debate has led to an abundance of recent studies on the role of numerous species of birds, mammals and insects in this process
(baboons, Lieberman et al. 1979; avifauna, Howe et al. 1985; white-faced capuchin monkeys, mantled howler monkeys and spider monkeys, Chapman 1989; elephants,
Chapman et al. 1992; black howler monkeys, Estrada et al. 1993; ants, Horvitz and
Schemske 1994; black-faced solitaire birds, Murray et al. 1994; forest chimpanzees,
Wrangham et al. 1994; red howler monkeys, Julliot 1997; lemurs, Overdorff and Strait
1998; black lemurs, Birkinshaw 1999; gibbons, McConkey 2000; woolly monkeys,
Stevenson 2004; maned wolves, Motta-Junior and Martins 2002; tamarin monkeys,
Knogge et al. 2003; avifauna and spider monkeys, Russo 2003). While the recent plethora of studies on seed dispersal has generated a better understanding of the subject, the results and conclusions of these studies vary greatly between, and even within, species.
Indeed, recent research on seed dispersal, while clarifying certain animal-plant relationships, has also done a great deal to highlight the complexity of the process, the number of possible factors involved in plant-animal relationships, and the resultant need for further study and clarification regarding the evolutionary basis of seed dispersal systems.
Fruit is an expensive item for a plant to produce, and seeds are weighty packages devoid of nutritional value for the animal that swallows them intact. And yet the system of seed dispersal has persisted to the extent of a widespread dominance of angiosperms over most of the earth, making seeded fruits a dominant plant reproductive strategy
2 (Herrera and Jordano 1981). Numerous hypotheses have been forwarded to explain the evolutionary basis of seed dispersal by animals, as well as the nature and extent of the relationship between plants and the animals that disperse their seeds.
1.1 Coevolutionary Models
Coevolution is defined as “an evolutionary change in a trait of the individuals in one population in response to a trait of the individuals of a second population, followed by an evolutionary response by the second population to the change in the first” (Janzen
1980). One of the models for the evolution of the primate order, known as the angiosperm radiation hypothesis, posits that primates and fruiting trees coevolved, with an explosive adaptive radiation of both. In essence, this hypothesis posits that in the early evolutionary history of primates there existed a mutualistic, dependent coevolution where angiosperms and ancestral primates coevolved, with each exerting roughly equal selective pressure on the other (Sussman and Raven 1978).
While coevolution and mutualism have been documented for some plant-animal dyads (e.g. wasps and figs in Madagascar, Dalecky et al. 2000), the case is much less clear for primates and angiosperms. In part this is due to the fact that fruiting trees existed prior to the evolution of the primate order. Additionally, numerous species of animals may disperse the seeds of the same fruiting species (Lambert and Garber 1998). This, coupled with the extremely high levels of post-dispersal seed mortality that is well documented in numerous studies (e.g. Chapman 1989, Howe et al. 1985) may “serve to dilute the influence that any primate species may have on the recruitment of the next generation of adult trees” (Lambert and Garber 1998). Moreover, given the relatively
3 slow evolutionary rates of plants relative to animals, the extensive gene flow in plant
populations and the weak selective pressures on the disperser (Chapman et al. 1992), the
likelihood of true coevolution between plants and animals is low. This becomes even more apparent with an examination of natural systems, where coevolutionary
relationships between plants and dispersal agents are very uncommon (Janzen 1980).
While numerous primate species show morphological and behavioural adaptations that enable them to successfully exploit fruit (Lambert and Garber 1998), and while primate fruit preferences for certain suites of fruit traits have been documented
(Stevenson 2004), the relationship between plants and the animals that disperse their seeds appears to be one of animals adapting to the resources available to them, rather than a strict case of coevolution, where each directs the development of the other. This, however, does not imply that animals have no effect on the plant communities that sustain them. Previous research on this subject indicates that the ecological and evolutionary impact of animals on the plant species they consume can vary based on a complex interplay of several factors, including distant-dependent seed and seedling
mortality, seed handling by frugivores, passage through the intestinal system of
frugivores, and secondary seed dispersal and predation. These factors are briefly explored in this chapter, within the theoretical framework of the three main ideas proposed to explain the very existence of seed dispersal: the Janzen-Connell model/seed escape hypothesis, the colonization hypothesis, and the environmental homogeneity model.
4 1.2 The Seed Escape Hypothesis
Seed dispersal by mammals and birds has been proposed as a reproductive
strategy of fruiting trees based on several lines of evidence. One of the earliest and most
pervasive explanations, known as the Janzen-Connell model, or seed escape hypothesis, states that there is a correlation between seed mortality and distance from parental trees
(Janzen 1970, Connell 1971). According to this model, non-dispersed seeds – those that
are deposited underneath the canopy of the parent tree – will attract and fall victim to a
series of species-specific seed predators and fungal pathogens, while those seeds that are
dispersed away from the parent plant will escape such a fate by virtue of their distribution
in lower densities away from host-specific predators.
Despite the theoretical elegance of this model, it has been heavily debated and has received only weak support from experimental studies (Nilson 2000, Howe et al. 1985).
Furthermore, studies of the actual distribution of adult fruiting trees have found that
species of trees that are dispersed by mammals have a clumped distribution relative to trees dispersed by birds, bats and wind (Hubbell 1979). This finding indicates that mammal-dispersed seeds are not being successfully dispersed across as wide a geographic range in lower densities as those trees with other mechanisms of dispersal
(Hubbell 1979). This model therefore still requires empirical testing, and the absence of support from field studies thus far suggest that other models warrant closer consideration.
1.3 The Colonization Hypothesis
This more recent hypothesis posits that the primary advantage to the dispersal of
seeds is the “chance occupation of favorable sites that are unpredictable in time and
5 space” (Howe and Smallwood 1982). The idea here is that the movement of seeds away
from parent plants can result in an increased chance of germination, establishment and
survival for seeds that are deposited in newly opened niches (e.g. tree fall gaps).
Additionally, seeds that are moved away from the parent plant decrease competition for
local resources (light, water, soil nutrients etc) between the offspring and the parent
(Howe and Smallwood 1982).
1.4 Environmental Homogeneity
The most recent model put forth to explain the function of seed dispersal by animals is that it is a process that will arise in areas of environmental homogeneity, where
microhabitats are consistent across a broad geographic range (Chapman and Chapman
1996). Essentially, where resources crucial to the germination, survival and growth of
seeds and seedlings are evenly distributed across the landscape there will be no risk of
seeds being deposited into microhabitats unsuitable for germination, survival and growth,
and in these instances trees will have a strategy that favors dispersal. Conversely, in areas
where resources important to seed and seedling survival and growth are patchily
distributed “the predictability of finding resources equivalent to the ones at the starting
location decreases with distance” (Chapman and Chapman 1996). Thus, in situations of
environmental heterogeneity, dispersal away from the parent will be a risky and
unsuccessful strategy, and in cases of environmental homogeneity, there will be no
relationship between resource availability and distance from the parent tree, and as such
the risks of dispersal will be minimal, and trees will have a strategy which favors
dispersal.
6 All three of the above explanations for the source of the benefit of seed dispersal focus on distance from the parent tree and the spatial distribution of predictors of survival
as the critical variables affecting seed and seedling survivorship and recruitment. And
while there is evidence suggesting that distance from the parent tree, and deposition in certain microhabitats can be important predictors of seed and seedling survival (e.g.
Howe et al. 1985), there are a series of other potentially important variables to consider in frugivore-plant interactions.
1.5 Seed Handling
The preliminary variable in the process of endozoochory is seed handling: Does an animal’s initial treatment of a seed destroy its chance for survival? Numerous studies of seed dispersal have documented the destruction of seeds by the animals that eat them, such that those seeds are no longer viable through chewing, pecking, biting etc. (see
Hulme 2002 for review). A comparison of the seed handling techniques of guenons in
Kenya and capuchins in Panama found that while guenons routinely chewed the seeds they ingested such that they were no longer viable, capuchins typically swallowed seeds whole, passing them intact and viable (Rowell and Mitchell 1991). Thus, if seeds of a given species are routinely destroyed by a species of animal, the possibility of seed dispersal ends. If, however, the seed escapes the mouth, beak, or hands of the animal unharmed, seed dispersal becomes possible and other potential variables come into play.
1.6 Gut Passage
One of these potential variables is the effect of passage through the intestinal system of frugivores. In some cases (e.g. howler monkeys, Smith 2004), studies have shown that gut passage neither helps nor hinders a seeds’ chance of germinating. In other
7 cases, passage through an animal’s digestive system appears to greatly increase the potential for germination. One study documenting elephant dispersal of Wilsonia balonites seeds found that, due to the very thick seed coat of Wilsonia seeds, those that had not been ingested by elephants didn’t germinate at all, while those that had passed through an elephant’s gut germinated in almost every case (Chapman et al. 1992). The effect of gut passage has been found to be a potentially significant predictor of germination success for numerous other species (e.g. black-faced solitaire birds, Murray et al. 1994; tamarin monkeys, Knogge et al. 2003; white-faced capuchin monkeys,
Chapman 1989). The strength of the above correlations between seed germination and gut passage indicate that this is a potentially crucial determinant of success in the seed dispersal process.
1.7 Secondary Dispersal and Predation
Yet another potential variable influencing the success of seed dispersal, is secondary dispersal and predation. Preliminary evidence from recent research on this topic indicates that secondary dispersal and predation are crucial aspects of the seed dispersal process (Chapman 1989, Estrada et al. 1999, Chapman et al. 2003). Essentially, the deposition of a seed is not the final step in the plant-animal interaction. This is because the forest floor is teeming with insects and rodents that variously prey on, or safely redeposit, dispersed seeds. One study on primate-dispersed seeds in Costa Rica found that approximately 80% of seeds were removed from animal feces a mere one week after initial deposition (Chapman 1989). Another study on howler monkey- dispersed seeds in Mexico found that a majority of the dung beetle species in the area were overwhelmingly attracted to howler dung, steering clear of the feces of other, more
8 folivorous, herbivores, and resulting in the massive redeposition of defecated seeds
(Estrada and Coates-Estrada 1991). Thus, initial field studies indicate that secondary
dispersal and predation represent another potentially crucial variable influencing seed
dispersal systems.
1.8 The Effect of Feces
Another potential variable that has never before been examined experimentally
for wild populations is the effect of animal feces on the germination potential of seeds.
The soils in tropical forests tend to be extremely nutrient-poor, as most of the nutrients
are locked up in plant and animal biomass (Bruijnzeel 1991). Given this paucity of
nutrients in tropical soils, it is possible that feces may increase the rate of seed coat
degradation, thus speeding the germination process, and that the nutritional content of an
animal’s feces may be an important source of food for a defecated seed in its earliest
days.
The plethora of data on seed dispersal that has been generated has served to
illuminate the complexity involved in frugivore-plant interactions, from fruit choice to
secondary dispersal, and the consequent need for further study. Primates are well suited to this, as on average they comprise between 25-40% of the frugivore biomass in tropical forests (Chapman 1995). Capuchins are particularly well suited because they rarely destroy the seeds that they ingest, and travel long distances in the time it takes for gut passage to occur (Fragaszy et al. 2004).
9 1.9 Previous Studies of Seed Dispersal by White-Faced Capuchin Monkeys
Studies of seed dispersal by white-faced capuchins have been preliminary
(Chapman 1989, Rowell and Mitchell 1991, Smith 2004), though a recent study did a great deal to establish a baseline of information regarding the effect of white-faced capuchins on primary seed input into the forest (Wehncke et al. 2003).
Chapman’s (1989) study of seed dispersal by the primates of Santa Rosa National
Park, Costa Rica established that gut passage through the digestive systems of the primates did not preclude germination, that a large number of dispersed seeds were
secondarily preyed upon or dispersed, and that capuchins disperse seeds in a clumped
manner. Rowell and Mitchell’s (1991) study of guenons in Kenya and capuchins in
Panama was limited to comparisons of the handling of seeds and the nature of the feces
of the two species, both of which indicate that the capuchins are better agents of seed
dispersal than guenons. Smith’s (2004) comparison of the germination rates of seeds that
had passed through the digestive system of howler monkeys and white-faced capuchins
found that seeds passed by the latter had a higher probability of germination than those
passed by the former. However, this study was limited in duration, as well as limited to a
single species of tree. Wehncke’s study (Wehncke et al. 2003) established the degree of
capuchin frugivory, rates of seed passage and distances that seeds are dispersed by white-
faced capuchin monkeys on Barro Colorado Island, Panama.
1.10 The Current Study
This study took place over the course of eight months in Santa Rosa National
Park, Costa Rica. The research was conducted over the course of two field seasons (May
10 to July 2005 and January to May 2006) which encompassed both the wet and dry
seasons of northwestern Costa Rica. Two well-habituated groups of white-faced capuchin
monkeys, the Cerco de Piedra and Los Valles groups, were the focus of this research. The
objective of this study was to answer some of the questions that remain regarding the role
of white-faced capuchin monkeys in the process of seed dispersal, as well as to refine
some of those questions.
Schupp (1993) has convincingly argued that “effectiveness, the contribution a
disperser makes to plant fitness, depends on the quantity of seeds dispersed and the
quality of dispersal provided each seed.” This study, as well as others of seed dispersal by
animals (e.g. Chapman 1989, Kaplin and Lambert 2000, Stevenson 2000, Wrangham et
al. 1994, Wehncke et al. 2003, Knogge et al. 2003) focuses on the quantity of seeds
dispersed by capuchins, as well as the quality of seed dispersal. Additionally, the spatial
pattern of dispersal produced by white-faced capuchins is measured and analyzed.
Chapter 2 focuses on quantifying seed dispersal by white-faced capuchins, the
measures of which include: species diversity of plants consumed, percentage of fruit in
the diet, number of plant species passed intact, average number of seeds and species per
defecation, number of defecations per animal per day, animal density, and the percentage
of defecations containing seeds. The results of this study are then compared to the results of the two previous attempts to quantify white-faced capuchin seed dispersal (Wehncke et
al. 2003 and Chapman 1989). Standards of data collection for comparative purposes
across and within species and sites are discussed.
11 Chapter 3 focuses on examining the quality of seed dispersal by white-faced
capuchins. Its goal is to answer the question: do capuchins have a positive or negative effect on the seeds of the fruiting species they consume? Measures of quality include the manner in which seeds are handled by capuchins, the effect of gut passage and feces on germination and time to germination, and the effect of all forms of monkey seed treatment (spitting, chewing, swallowing whole and defecating etc.) on germination.
The fourth chapter focuses on the spatial pattern of capuchin seed dispersal and its effect on seed germination and growth, and seedling survival and growth, an important aspect of the seed dispersal process, but one which has been less studied. The spatial dimension of seed dispersal is additionally the site of most theoretical attempts to understand the process of endozoochory. Measures explored here include: the distance seeds are deposited from parent trees, the distance between defecations containing seeds, the effect of distance from parent trees and nearest fruiting conspecific trees as well as canopy cover and the DBH of the nearest fruiting conspecific tree on seed survival and germination and seedling survival and growth, and the pattern (clumped versus dispersed) of the dispersal of capuchin feces. These measures are interpreted in light of the theoretical debate regarding the origins and purpose of seed dispersal by animals.
1.11 Summary and Significance
Recent studies have established the importance of primates as seed dispersers, and as a result, their important role in the maintenance and regeneration of tropical forests.
One such study in Uganda demonstrated a markedly lowered rate of seedling recruitment in areas where primate seed disperser populations are reduced, as compared with areas of
12 high seedling recruitment rate and intact frugivore communities (Chapman and
Oderdonk 1998). Similar results have been reached for black lemurs in Madagascar,
prompting the researchers to state that were the lemur populations in these forests to be
reduced, “a large proportion of the tree species would suffer from reduced seed dispersal
(which) could lead to their poor regeneration and, with time, a change in the plant species composition of the forest” (Birkinshaw 1999). Such findings further the understanding of the importance of frugivorous primates to the regeneration, maintenance and survival of
at least some of the fruiting trees which sustain them (Chapman and Chapman 1996).
Understanding the nature and extent to which primates influence the processes of forest
regeneration and maintenance is thus not only critical to understanding primates in the
context of the ecological communities of which they are a part; it is also critical to
understanding the potentially enormous implications that their behaviour and choices
exert on the survival of entire ecosystems. This study attempts to do just that: to explicate
the role that white-faced capuchins play in the complex and as yet little understood
process of seed dispersal, and to begin to determine what effect their role as seed
dispersers/predators will have on the regenerating forests of Santa Rosa National Park.
13 Chapter Two: Quantifying Seed Dispersal by White-Faced Capuchins
2.1 Introduction
Measuring the quantity of seeds dispersed by an animal is a critical initial step in understanding the dispersal ability of an animal. Schupp (1993) posits that “effectiveness, the contribution a disperser makes to plant fitness, depends on the quantity of seeds dispersed and the quality of dispersal provided each seed.” Studies of seed dispersal by animals tend to focus on both the quantity of dispersed seeds as well as the quality of dispersal (e.g. Chapman 1989, Kaplin and Lambert 2000, Stevenson 2000, Wrangham et al. 1994, Wehncke et al. 2003, Knogge et al. 2003). However, despite the recent plethora of research on seed dispersal by mammals, and specifically by primates, there is little overlap in the way in which quantity of seed dispersal is measured or reported in the literature. Here, I quantify the seeds dispersed by white-faced capuchin monkeys (Cebus capucinus), as well as compare these quantities to the values extant in the literature for white-faced capuchin monkeys, as well as suggest a means of standardizing measures of dispersal quantity for future comparisons.
Schupp (1993) suggests that the quantity of dispersal be measured as the number of visits made by a disperser (measured as the abundance of a disperser, disperser diet, and reliability of visitation) and the number of seeds dispersed per visit (measured as the number of seeds handled per visit and the probability of dispersing a handled seed).
While these are excellent measures where the tree species is the unit of analysis, in cases
(like most primate-based studies of seed dispersal) where the disperser is the unit of analysis, and especially where the disperser exploits a wide variety of angiosperms, it would be beneficial to create some way to look at the effectiveness of one disperser
14 across multiple plant species, instead of the relative effect of multiple dispersers across
a single plant species. The former is typically the way that seed dispersal is measured in
primate studies. However, there exists little in the way of a standard comparative basis
for measuring the quantitative effectiveness of one primate disperser species across
multiple plant species.
There are numerous ways in which to measure the dispersal effectiveness of a
single primate species vis-à-vis numerous plant species with regard to quantity of
dispersal. These include: degree of frugivory, diversity of species consumed, the number
of seeds consumed per unit time, the number of seeds dispersed intact per unit time, and
the number of seeds dispersed intact per unit space. However, the results of these
measurements are mere numbers. And without comparative contextualizing across other
species, it is difficult to say what it is that makes an effective disperser. At what point, for
example, can one determine that a particular frugivore is a “good disperser?” In this
chapter, I propose a standardization of quantitative measurements where the animal, and
not the angiosperm, is the unit of analysis to serve as a basis of comparison across
disperser species and between different populations of a given species, including my own measures of seed dispersal by white-faced capuchins.
I compare the values for these measures from the current study with two prior studies of white-faced capuchin seed dispersal, Chapman (1989) and Wehncke et al.
(2003). I do so in order to illuminate how differences in methodology can culminate in differences between results. I describe the method for obtaining each result individually with respect to its reliability and relevance to the question of seed dispersal quantity.
15 Additionally, I discuss differences among results arising from differences in lengths of the study, sample size and site-specific fruit species availability.
2.2 Research Questions and Predictions
2.2.1 Research Questions
1) What percentage of the total day, as well as the capuchin diet, is composed of
fruit and fruit feeding?
2) How many fruit species are consumed by capuchins, and how often are the seeds
of each species passed intact?
3) How many seeds and seed species are passed per defecation?
4) What proportion of capuchin feces contain intact seeds?
5) How often do capuchins defecate?
6) What is the density of capuchins in my study area?
2.2.2 Predictions
1) Based on previous studies of capuchin diets, I predict that fruit will comprise a
large portion of their diet, and that a large proportion of their day will be spent
foraging and feeding on fruits.
2) Based on previous studies of capuchin diets and seed handling behaviours, I
predict that capuchins will consume a high diversity of fruit species, and pass the
seeds of all, or most, intact.
16 3) Based on previous field observations (Fedigan, personal communication) I
predict that a high number of seeds will be passed per defecation, comprised of a
small number of tree species.
4) I predict that most, if not all, capuchin defecations will contain seeds of at least
one species.
5) Based on others’ field observations of capuchins (Fedigan, personal
communication), I predict that capuchins will defecate frequently, at least once
per hour.
2.3 Methods
2.3.1 Study Site
The study took place in Santa Rosa National Park, a 108 ha sector of the Area de
Conservacion Guanacaste (ACG). At 110,000 hectares the ACG encompasses the largest continuous tract of regenerating tropical dry forest in the world, and is composed of fragments of deciduous, semi-evergreen and riparian forest, as well as regenerating pasture land. There is a distinct dry season (January to May) and a distinct wet season
(May to December). The park is located in northwestern Costa Rica, approximately 40 km south of the Nicaraguan border in Guanacaste Province.
The park is home to thousands of plant species, as well as over 200 species of bird and over 100 species of mammal, including three species of non-human primate: the white-faced capuchin monkey (Cebus capucinus), the black-handed spider monkey
(Ateles geoffroyi) and the mantled howler monkey (Alouatta palliata).
17 2.3.2 Study Subjects
White-faced capuchins (Cebus capucinus) are arboreal, diurnal omnivores. Their diet is composed of numerous species of invertebrates, vertebrates, fruits, flower buds and flowers. They live in multimale/multifemale groups composed of related females and immigrant males. White-faced capuchins are found in both Central and South America, from Honduras in the North to Ecuador and Columbia in the South.
2.3.3 Data Collection and Analysis
Over the course of eight months of study (May to July 2005 and January to May
2006) a field assistant and I conducted all-day focal follows (N=50, 393.5 hours) on all adult individuals in two well-habituated groups- Cerco de Piedra (CP) group (N=19 monkeys, 8 adults) and Los Valles (LV) group (N=17 monkeys, 8 adults). Focal follows were conducted between the hours of 5:00 AM and 6 PM. Focal animals were observed continuously by two observers all day or for as long as possible (range= 2 hours and 12 minutes to 12 hours and 53 minutes, mean follow time= 7 hours and 43 minutes).
Follows that could not be maintained for longer than 2 hours or in cases where the focal animal was not visible for greater than 10 percent of the entire possible number of observation hours, were discarded.
Behavioural and defecation data were recorded using a hand-held data logger
(Psion Workabout MX). This device records time to the second each time an entry is made. Location data were recorded using a handheld Geographic Positioning System
(GPS).
18 Each time the focal animal fed on fruit, the tree species was recorded along with a number which corresponded to the number of trees of that species consumed during that follow (e.g. the second Genipa americana tree a focal animal visited during
one follow was recorded as Genipa americana 2, the third as Genipa americana 3, etc.).
A fruit-eating bout was considered to begin the moment that the focal animal picked or
bit the first piece of fruit, and ended when the focal animal left the tree, changed their
behavioural state (e.g. began to eat insects, groom, rest), or when they continued to
forage but did not pick or eat fruit for 30 seconds. A waypoint was recorded using the
GPS for each tree at which the focal animal consumed fruit, with the same name and
number as was recorded in the Psion.
Each time the focal animal defecated, the defecation event and number was
recorded in the Psion, a waypoint was taken, and the defecation was collected in a vial
and labeled. Fecal samples (N=549) were returned to the field laboratory, where each
species of seed was identified based on fruit samples taken during the focal animal
follows. All seeds were then counted and their species and number recorded. Any
apparent damage to the seeds was recorded.
In addition, general behavioural data (Rest, Social, Travel/Forage, Insect Feed,
Vertebrate Feed, Fruit Feed, Drink, and Other) were recorded during half-hour periods of
focal animal sampling in order to determine activity budgets (N=171 activity budget focal
animal samples, 85.5 hours). When the focal animal was out of sight (OOS) of both
observers, this was recorded, and in cases where this exceeded ten percent (3 minutes) of
the total focal animal sample time, the sample was discarded. This additional sampling
19 took place with the focal animal of the day. All activity budget focal animal samples
began and ended on the hour, or half-hour to help ensure the equal distribution of sampling times throughout the day.
2.3.4 Degree of Frugivory
The degree of capuchin frugivory was determined in two ways. Firstly, the duration of all recorded behaviours was extracted from the half-hour focal animal samples (N=95 sessions, 47.5 hours) and converted to time in seconds. A final percentage score was then arrived at for each individual monkey, and these scores were averaged for the wet season (April to July, 2005) and for the dry season (January to June, 2006). This method yields a percentage spent feeding on fruit for both groups in the dry and wet season, vis-à-vis all other activity categories (Rest, Social, Travel/Forage, Insect Feed,
Vertebrate Feed, Drink and Other).
Secondly, each event of feeding on fruit was identified in the all-day focal animal follow, and the duration converted to seconds. A percentage of time spent feeding on fruit was then arrived at by dividing the total number of seconds spent feeding on fruit by the total number of focal seconds for that all-day focal follow (minus any out of sight time).
A final percentage score was then arrived at for each individual monkey, and these scores were averaged for the wet season (April to July, 2005) and for the dry season (January to
June, 2006).
To further quantify fruit consumption by white-faced capuchins, the duration of feeding bouts per tree species was calculated per all-day focal follow by dividing the total number of seconds spent in all individual trees of each species consumed by the total
20 number of focal seconds spent feeding on fruit of any species for all all-day focal
follows combined (minus any out of sight time, N= 187,345 seconds). A final percentage
score was then arrived at across all individual monkeys.
2.3.5 Diversity of Fruit Consumption and Passage
The number of seed-bearing species consumed and passed intact was determined
by counting each seed-bearing species consumed during the course of focal animal
observation. The number reported here is an underestimate as it was not possible to
determine the individual species of the 9 individual trees of the Genus Ficus, as well as 7
fruiting tree species that were consumed by focal animals but were not identified. Here, all species of unidentified trees are referred to as 1 species, as are all individuals of the
Genus Ficus.
The number of seed species passed intact was extracted from the laboratory data, where all seeds in collected fecal samples were identified and counted. A percentage of seeded species observed to pass intact was then arrived at by dividing the total number of seed species where at least one seed had been observed to pass intact by the total number of seeded species consumed.
2.3.6 Seeds and Species Passed
The number of seeds passed per defecation as well as the number of species passed per defecation was extracted from the laboratory data where the contents of all fecal samples were recorded. A mean, median and range were arrived at for both the number of seeds per defecation as well as the number of species per defecation. An accurate count was possible for all species with the exception of species of the Genus
21 Ficus and Cecropia peltata. Seeds of these species are too small (<2mm in diameter) and usually too numerous to accurately count. Additionally, they are extremely delicate
and are damaged very quickly by human manipulation. Thus results pertaining to the
number of seeds passed per defecation are underestimates, as they do not account for the
very numerous seeds of the aforementioned species.
2.3.7 Number of Defecations Containing Seeds
The number of defecations containing intact seeds and the number containing 1, 2
and more than 2 species of seeds was determined by dividing the number of defecations
containing seeds and the number of defecations containing seeds of 1, 2 and more than 2
species by the total number of fecal samples (N=549).
2.3.8 Frequency and Rate of Seed Dispersal
The frequency of defecation was determined by calculating the time between two
focal animal defecations. In cases where the focal animal was not visible by at least one
observer for the entire time between two witnessed defecations, the record was not used.
The average time between defecations was then calculated across all individuals.
A rate of seed dispersal was also extrapolated by multiplying the average number
of seeds dispersed per defecation (see above) by the average number of defecations per
day.
2.3.9 Animal Density
During all-day focal animal follows, a waypoint was taken every thirty minutes
on the hour and half-hour. These waypoints (1344 for CP group, 974 for LV) were
combined for a twelve-month period spanning May 2005 to May 2006, and for each of
22 the two monkey groups a home range was determined using a 95% fixed kernel (in
ArcView 3.2, Animal Movement 2.04). Density was then determined by dividing the
total area of home range (CP=102.87 ha, LV=175.58 ha) by the total number of
capuchins inhabiting that range (CP= 18, LV=17), and deriving a mean of those two
numbers.
2.4 Results
2.4.1 Degree of Frugivory
From the half-hour sample data, CP and LV group spent 6% of all of their time in
the wet season feeding on fruit (Figure 2.1), and 22% of all of their time in the dry season
feeding on fruit (see Figure 2.2 for percent time spent per activity). This increase in fruit
consumption during the dry season likely represents a decreased availability in
invertebrate foods during the drier months. During the wet season, 21% of time was spent
feeding on invertebrates, while in the dry season only 7% of time was spent feeding on invertebrates (Figure 2.3).
When the all-day focal animal data are examined, the mean time spent feeding on fruit across both seasons is 15%, with a median time of 12% and a range of 3.96% to
58.35% (Table 2.1).
The average number of fruit species consumed per all-day focal animal follow is
5 (median=5, range=1 to 9), and the average number of individual fruit-bearing trees of
any species visited per all-day focal animal follow is 14 (median=13, range=2 to 26)
(Table 2.1). Therefore a new fruit-bearing tree species is visited on average every 92.6 minutes, and fruit of any species is consumed on average every 33.1 minutes. Over the
23 course of a 12 hour day, this yields a daily average of 7.8 species consumed per day and 21.8 individual fruiting trees exploited per day.
2.4.2 Diversity of Fruit Consumption and Passage
The fruit of 39 seed-bearing plant species were observed to be consumed by both groups of white-faced capuchins (Table 2.2). Seeds from 29 of these plant species, or
74%, were found intact in capuchin feces.
There are great differences between species in terms of their importance in the capuchin diet. The amount of time the capuchins were observed to spend feeding on different fruiting species ranges from <0.01 to 18.84% of time spent feeding on all tree species (Table 2.2).
The mean duration of fruit feeding bouts across all species is 12.85 minutes
(median=0.56 minutes, range=0.05 minutes to 152.27 minutes).
2.4.3 Number of Defecations Containing Seeds
Of the observed defecations (N=549), 408 (74%) contained intact seeds, whereas
141 (26%) did not. 52% of fecal samples (N=281) contained the intact seeds of 1 plant species, 26% (N=111) of fecal samples contained the intact seeds of 2 species, and 4%
(N= 16) of fecal samples contained the intact seeds of more than 2 plant species.
2.4.4 Frequency and Rate of Seed Dispersal
White-faced capuchins defecate frequently. The mean time between defecations is
28.32 minutes (median=22.5 minutes, range=0.2 to 292.13 minutes). Over the course of a twelve-hour day, this yields an average of 25.4 defecations per animal per day. In total,
24 for the two monkey groups observed during the course of this study (which are composed of 19 and 17 individuals respectively), the average daily number of defecations is 914.4.
Of the fecal samples containing countable seeds (N=349), the average number of seeds of any species passed intact (not including seeds of the Genus Ficus, and seeds of
Cecropia peltata) is 15.7 (median= 8, range= 1 to 107). Of all fecal samples containing seeds (N=408), the average number of plant species per defecation is 1.3 (median= 1, range= 1 to 4) (Table 2.3).
Given the average number of countable seeds per defecation (15.7) and the average number of defecations containing seeds per day (18.8), an individual animal can be expected to pass intact an average of 295.16 intact seeds per day. Extrapolated to the individuals of both groups studied here (N=36 individual animals), the average daily dispersal of countable seeds by both CP and LV group is 10, 625.76. When animal density is considered (here, the mean of both groups), CP and LV combined will disperse
85,212.5 intact seeds per hectare per day.
2.4.5 Animal Density
Cumulative white-faced capuchin home ranges at this site are 102.87 ha for CP, and 175.58 ha for LV (Figures 2.4 and 2.5). White-faced capuchin density is 5.72 animals per ha in CP’s home range, and 10.33 animals per ha in LV’s home range.
25 2.4.6 Comparison with Prior Studies
Here I compare the results from this study to two sets of published results on
white-faced capuchins: Colin Chapman’s study in Santa Rosa National Park, Costa Rica,
and Elizabeth Wehncke’s study on Barro Colorado Island and the Summit Zoo, Panama.
The results from the current study vis-à-vis the two other extant studies are, in some cases
disparate and in some cases very similar (Table 2.4). These discrepancies, discussed in
detail below, result from differences in methodology, as well as differences in the
duration and location of studies, and highlight the need for a standardized set of
measurements in frugivore-based studies of seed dispersal.
2.5 Discussion
2.5.1 Degree of Frugivory
Percentage of fruit in the diet of capuchins can be measured as either the
percentage of total time spent feeding on fruit per total observation time, or as a
percentage of time spent feeding on fruit per total time spent feeding. Differences in the
way in which this is measured will produce vast differences in results. For example, in
this study, white-faced capuchins spent 15% of all observation time feeding on fruits, but
49% of all feeding time feeding on fruits. Because questions related to the quantity of seed dispersal centre on questions of degree of frugivory, and because time spent feeding on fruit as a percentage of total observation time can be skewed by differences in species- specific differences in time spent feeding during the course of a day, I propose that cross- species and cross-population comparisons of frugivory be focused on the percentage of all feeding time spent feeding on fruit, and not the percentage of time spent feeding on
fruit vis-à-vis all other activities.
26 2.5.2 Diversity of Fruit Consumption and Passage
Surprisingly, there is great discrepancy between the three studies with regard to the diversity of plant species consumed (see Table 2.4). This difference does not coincide with length of time of study period, but rather with study sites. Both the current study and
Chapman’s (1989) study show similar diversity of fruit consumption (39 and 41 species respectively) and both studies took place in Santa Rosa National Park, Costa Rica. In the third study, which took place on Barro Colorado Island, Panama, more than double the number of plant species were observed to be consumed by white-faced capuchins in only half the time of my study (four versus eight months) and less than one-sixth the time of the Chapman study (26 months). This difference in diversity of fruit consumption suggests a difference in fruit species availability between sites. It is a potentially interesting measure of fruit and dietary diversity between forest sites, but also indicates that caution should be taken when comparing fruit consumption between different sites.
2.5.3 Seeds and Species Passed
The number of plant species passed intact (as a percentage of the total number of plant species consumed) is a measure of the efficacy of a frugivore as a disperser.
However, here as elsewhere, there are discrepancies in results. The difference seems to be due to the numbers of fecal samples collected. Despite the fact that both the current study and Chapman’s study took place at the same field site and that similar numbers of plant species were observed to be consumed, the percentage of plant species observed to pass intact is vastly different between these studies (74% and 34%). Given the similar conditions of the studies, it is likely that these differences are a result of the number of fecal samples collected (549 versus 28). Because of seasonal variation in fruit
27 consumption and seed defecation, collecting a low number of fecal samples over a short period can result in under- or overestimated percentages.
2.5.4 Number of Defecations Containing Seeds
The percentage of defecations containing intact seeds is a reliable way to estimate
the quantity of seed dispersal. This measure can be combined with animal density measurements, number of defecations per animal per day, and the number of seeds and seed species per defecation to estimate seed fall in a given area.
There are differences among results for the three studies (see Table 2.4), but these do not correspond to site differences or differences in the duration of studies. They do, however, correspond to differences in number of fecal samples obtained. In the case of the least fecal samples (28) we see the highest percentage of defecations containing intact seeds, and in the study with the highest number of fecal samples (549), we see the lowest percentage of defecations containing seeds. This discrepancy is likely the result of the under- or overestimations that result from low sample numbers.
2.5.5 Frequency and Rate of Seed Dispersal
The number of defecations per animal per day is more than twice the upper limit of Wehncke et al.’s (2003) study (8-10 versus 25.42 defecations per animal per day). This is likely the result of differences in sampling method. During the course of this study, individual animals were followed for several hours at a time, and all defecations recorded. In Wehncke’s study, defecation rates per day were estimated based on shorter periods of focal animal sampling. Consecutive defecation events over long periods of
28 time were not recorded, which is likely led to an underestimation of the rate of
defecations per day.
The number of seeds and seed species per defecation is another measure of the
quantity of seed dispersal, and it can be combined with the number of defecations per day and the number of animals per area to estimate seed fall in a given area. It is also a relatively easy thing to measure, as seed counting and identification is usually done in the course of seed dispersal studies for other reasons (e.g. germination experiments).
Here, while there is no comparative data available for the average number of seeds per defecation, Wehncke’s mean of 2 seed species per defecation is relatively consistent with this study’s result of 1.3 species per defecation.
2.5.6 Animal Density
The mean density of the two capuchin groups studied here is relatively high, with
8.02 animals per ha. This is an important aspect in determining seed fall in a given area,
and can be used to aid in establishing a comparative basis for seed rain between
conspecific frugivores as well as within species and between sites.
2.5.7 Seed Rain
Capuchins disperse a remarkably high number of intact seeds of many species
each day, as a consequence of their high rates of defecations per animal per day, their
large group sizes, the frequency of seed occurrence in the feces and the high number of
seeds per defecation. Despite the extremely high rate of seed dispersal, however, the
numbers here are underestimates. Seeds of the species Cecropia peltata, as well as those
of the Genus Ficus, were not counted due to the difficulty of separating and counting
29 individual seeds. Seeds of these species are <2mm in diameter, and are deposited in
capuchin feces in extremely high numbers. The quantity of seed input by capuchins is
thus not used here as a point of comparison because of the difficulty of accurately
gauging the number of very small and fragile seeds dispersed.
2.6 Conclusion
Given that primate-based studies of seed dispersal tend to focus on the dispersal abilities of one species of animal (e.g. Chapman 1989, Kaplin and Lambert 2000,
Stevenson 2000, Wrangham et al. 1994, Wehncke et al. 2003, Knogge et al. 2003), rather than the dispersal methods and mechanisms of one species of tree, seed dispersal studies where the animal is the unit of analysis tend to focus on the question of how one species of animal intersects with numerous species of plants. This differs from the theoretical and methodological bent of other types of seed dispersal studies, which tend to focus on seed dispersal from the point of view of the plant, and involve measuring the relative effect of different animal species on individual plant species (see Herrera and Jordano 1981 for review). Despite this divide, Schupp’s (1993) suggestion for measurements of dispersal effectiveness have been employed repeatedly as a reference for measures of seed dispersal quantity for individual disperser species, or, in other words, seed dispersal from the point of view of the animal. It would be beneficial to develop a standard set of measurements which would facilitate comparison between individual disperser species.
White-faced capuchin monkeys disperse a high number and a high diversity of plant species. However, given the dearth of standardized measures of seed dispersal quantity, it is difficult to put these numbers into context.
30 Reliable and easily comparable measures of the quantity of dispersed seeds are:
The percentage of fruit in the diet, the number of plant species consumed, the percentage of plant species passed intact, the number of seeds and species per defecation, the number of defecations per animal per day, animal density, and the percentage of defecations containing seeds. Standardizing these measures will allow for the comparison of the effectiveness of primates as seed dispersers both between species, and between different populations of the same species.
31 Tables
Table 2.1. Fruiting tree visitation # Species Visited # Individual trees Percent time spent fruit per follow visited per follow feeding per follow Mean 5 14 15% Median 5 13 12% Range 1 – 9 2 – 26 3.96% - 58.35%
32 Table 2.2. List of seed-bearing plant species consumed and passed intact.
Plant Species Consumed Percentage of each species (* indicates seeds pass intact) in the diet. Acacia collinsii* 9.33 Alibertia edulis* 0.08 Anona reticulada* 1.59 Ardisia revolute* 0.61 Apeiba tibourbou* 0.81 Brysonima crassifolia* 0.06 Bursera simaruba* 0.58 Casearia arguta* 1.43 Cecropia peltata* 2.28 Cedrela odorata 0.17 Curatella americana* 0.45 Ficus spp.* 12.06 Genipa americana* 6.40 Guazuma ulmilfolia* 0.07 Jacquinia nervosa* <0.01 Karwinskia caldronii* 8.92 Luehea alternifolia 14.66 Luehea candida 1.40 Lasciviasis negra* 0.34 Lasciviasis ruscifolia 0.49 Malvaviscus arboreus* 0.70 Manilkara chicle 0.85 Miconia argentea* <0.01 Mouriri myrtilloides 0.38 Muntingia calabura* 0.05 Randia monantha* 0.22 Randia thurberi* 0.35 Sciadodendron excelsum* 5.74 Simarouba glauca 6.92 Spondias mombin 0.18 Stemmadenia obovata* 0.10 Spondias purpurea <0.01 Sloanea terniflora* 18.84 Trichilia martiana* 1.35 Trema micrantha <0.01 Trophis racemosa* 0.18 Trichilia spp.* 0.06 Zuelania guidonia* 1.06 Unknown* 1.30
33 Table 2.3. Number of species and intact seeds per defecation. Seeds per defecation Species per defecation Mean 15.7 1.3 Median 8 1 Range 1-107 1-4
Table 2.4. Comparison of the results of three seed dispersal studies of Cebus capucinus. Wehncke et al. 2003 Chapman 1989 Current Study % Fruit in Diet 53%♦ 81.2%* 49%* Number of Plant 95 (over 4 months) 41 (over 26 39 (over 8 months) Species Consumed months) Percentage of Plant 71% (67/95) 34% (14/41) 74% (29/39) Species Passed Intact Average Number of NA NA 15.7 (N=349) Seeds per Defecation Average Number of 2 (N=174) NA 1.3 (N=349) Species per Defecation Number of Defecations 8-10 NA 25.42 per Animal per Day Animal Density NA NA CP-5.72 per ha LV-10.33 per ha Mean-8.02 per ha Percentage of 93% (161/174) 100% (28/28) 74% (408/549) Defecations containing seeds ♦Calculated as the percentage of total observation time spent feeding on fruits. * Measured as the percent of all feeding time spent feeding on fruits. In current study this is derived by taking the mean of the mean total for each season.
34 Figures
Figure 2.1. Bar graph depicting the percentage of time spent per activity, CP and LV combined, wet season
Activity Budgets, CP and LV - Wet Season
45 40 35 30 25 20 15 Per Activity 10 5 0
Percentage of Total Time Total Spent of Percentage t t e al r S rat ate Res the r Frui Soci O OO l/Forage e erteb v Verteb In Trav Activity
Figure 2.2. Bar graph depicting the percentage of time spent per activity, CP and LV combined, dry season
Activity Budgets, CP and LV - Dry Season
45 40 35 30 25 20 15 Per Activity 10 5 0
l st e er Percentage of Total Time Spent Spent Time of Total Percentage rat rink Re th OOS Fruit b Socia D O /Forage rte ve Vertebrate In Travel Activity
35
Figure 2.3. Bar graph depicting activity budget differences between seasons.
Activity Budgets: Percent Differences Between Seasons
50% 45% 40% 35% 30% Wet Season 25% 20% Dry Season
Percentage 15% 10% 5% 0%
t te l r e it a ia u rage r c OS r Res o b O brat F F te So Othe te er r vel/ v Ve In Tra Activ ity
36
Figure 2.4. Map of CP home range, showing 95% of range use and 50% of range use.
37
Figure 2.5. Map of LV home range, showing 95% of range use and 50% of range use.
38 Chapter Three: Evaluating the Quality of Seed Dispersal by White-Faced Capuchins (Cebus capucinus)
3.1 Introduction
Seed dispersal by animals has recently been the focus of numerous studies that attempt to determine the nature and extent of plant-animal mutualisms, and the ecological and evolutionary impacts that frugivores and angiosperms have on one another (Lambert and Garber 1998). These studies have focused on several aspects of the seed dispersal process, and along with the growing body of literature on the subject there has developed an increased understanding of the complexity of the process and a resultant profusion of potential measures and theoretical frameworks within which to understand it (McKey
1975). Of these measures, there are two that have been convincingly argued by Schupp
(1993) to be key means to understanding the effectiveness of an animal as a seed disperser: the quantity of seeds dispersed, and the quality of seed dispersal. Here, I focus on the latter.
The quality of seed dispersal can be measured in a number of ways. The most basic and preliminary variable is seed handling. In other words, does an animal’s initial treatment of a seed destroy its chance for survival? Numerous studies of seed dispersal have documented initial seed fate through seed handling. Initial seed fate can fall anywhere along a broad spectrum, from the destruction of seeds by the animals that eat them through chewing, biting, pecking etc., such that those seeds are no longer viable,
(e.g. Propithecus diadema edwardsi, Eulemur fulvus rufus and Eulemur rubriventer,
Overdorff and Strait 1998; Cercopithecus mitis stuhlmanni and C. ascanius schmidti,
Rowell and Mitchell 1991; Macaca fascicularis faciscularis, Lucas and Corlett 1998) to
39 careful de-fleshing followed by spitting of seeds (e.g. Cercopithecus campbelli and
Cercopithecus petaurista, Kankam 2000) to the swallowing and intact passage of seeds
(e.g. Cercopithecus mitis doggetti and C. l’hoesti, Kaplin and Moermond 1998;
Hylobates mulleri, McConkey 2000; Cebus capucinus, Rowell and Mitchell 1991.) If seeds of a given species are routinely destroyed by an animal, the possibility of seed dispersal ends, and the question of the effectiveness of that animal is answered. If, however, the seeds escape the mouth, beak or hands of an animal unharmed, seed dispersal becomes possible and other potential variables come into play.
One of these variables concerns treatment after a seed has been swallowed- namely, what effect, if any, does passage through the intestinal system have on the viability of a dispersed seed? Endozoochorous dispersal involves exposure to digestive fluids during gastrointestinal passage, and any assessment of endozoochory therefore requires an examination of seed survival through this phase (Cosyns et al. 2005). In some cases, studies have shown that gut passage neither helps nor hinders a seed’s chance of germinating (e.g. Alouatta palliata, Smith 2004; Saguinus mystax and S. fuscicollis,
Knogge et al. 2003). In other cases, in at least some plant species, passage through an animal’s digestive system appears to greatly increase the potential for germination (e.g.
Cercopithecus ascanius, Lambert 2001; Pan troglodytes, Wrangham et al. 1994; Papio anubis, Lieberman et al. 1979; Cebus capucinus, Wehncke and Dalling, 2005; black- faced solitaire birds, Murray et al. 1994). One study documenting elephant dispersal of the seeds of the Wilsonia balonites plant found that, due to the very thick seed coating of
Wilsonia seeds, those ingested by elephants germinated in almost every experimental case, while those that had not been ingested by elephants did not germinate at all
40 (Chapman et al. 1992). Given the potential importance of gut passage as a predictor of
germination, it is likely to be a crucial aspect of the seed dispersal process, and one that is
explored below (Figure 3.1).
Another potential predictor of the quality of seed dispersal that has received less
attention in the literature is the effect of feces on germination potential, i.e. does the
presence of a fecal matrix, after seed ingestion and defecation, increase the likelihood of
germination? One study of dispersal by ungulates and rabbits found a decrease in
germination of passed seeds when planted in dung versus soil (Cosyns et al. 2005).
Alternatively, it is possible that the chemical composition of animal feces induces
germination and that the nutritional content of some animal feces may be an important
source of food for a defecated seedling in its earliest days (Figure 3.1). Indeed, previous
studies have shown systematic changes to soil gradients based on nutrient input from
primate feces (Alouatta seniculus, Feeley 2005). This seems especially likely in tropical forests, where the soils tend to be extremely nutrient-poor (Bruijnzeel 1991), and in areas like Santa Rosa National Park, the location of this study, where soils are characterized by variation in soil depth likely leading to variations in soil quality (J.A. Klemens, personal communication).
Additional to the effect of gut passage and the presence of feces on germination rates is the potential effect of these two factors on the time to germination. Previous studies have indicated that for some species, even where germination rate is not affected by gut passage, the time to germination is affected (e.g. latency in some seed species after gut passage by Saguinus mystax and S. fuscicollis, Knogge et al. 2003). The speed to
41 germination can be a crucial variable in dispersal effectiveness given the potential for massive re-deposition of defecated seeds through secondary seed dispersal and predation
(Estrada and Coates-Estrada 1991). In an earlier study at Santa Rosa National Park,
Chapman (1989) found that 80% of all seeds left in primate feces were removed within one week after initial deposition. Thus, a reduction in the time to germination would potentially increase the likelihood of a seed surviving to the next stage.
3.2 Research Questions and Predictions
3.2.1 Research Questions
1) Does capuchin seed handling typically result in the dispersal of seeds, or in seed
death, or a mixture of both?
2) What effect does gut passage by white-faced capuchins have on seed germination
rates?
3) Does passage through the intestinal system increase or decrease germination
latency?
4) What effect does the presence of capuchin feces have on the germination rate of
passed seeds?
5) Does the presence of feces increase or decrease germination latency?
3.2.2 Predictions
1) Based on previous observations of capuchin seed handling (Rowell and Mitchell
1991, Fragaszy et al. 2004), I predict that they will swallow and pass a majority of
seeds intact.
42 2) Based on previous studies of the effect of white-faced capuchin gut passage on
seed germination (Chapman 1989, Smith 2004), I predict an increase in seed
germination after intestinal passage.
3) Based on a previous study of germination latency and capuchin gut passage
(Wehncke and Dalling 2005) I predict that passage through the capuchin intestinal
system will decrease the time to germination for passed seeds.
4) Based on previous studied showing increased nutrient levels in soil due to input
from primate species (Feeley 2005), I predict that the presence of white-faced
capuchin feces will cause an increased likelihood of seed germination.
5) Based on the potential for increased seed coat scarification and dissolution, I
predict that the presence of white-faced capuchin feces will decrease the time to
germination for passed seeds.
3.3 Methods
3.3.1 Study Site
The study took place in the Santa Rosa sector of the Area de Conservacion
Guanacaste (ACG), a 110,000 hectare reserve of regenerating tropical dry forest. The
ACG lies in the north-western corner of Costa Rica approximately 40 km south of the
Nicaraguan border, and is composed of fragments of deciduous, semi-evergreen and riparian forest, as well as regenerating pasture land. The dominant habitat in the Santa
Rosa sector is tropical dry forest, with most trees losing their leaves during the distinct dry season (Janzen 1983).
43 The park is home to thousands of plant species, over 200 species of bird and
over 100 species of mammal. The park is also home to three species of non-human
primate: the white-faced capuchin monkey (Cebus capucinus), the black-handed spider
monkey (Ateles geoffroyi) and the mantled howler monkey (Alouatta palliata).
3.3.2 Study Subjects
Cebus monkeys are widely distributed throughout Central and South America
from Honduras to Ecuador (Rowe 1996). White-faced capuchins, like other members of
the genus Cebus, are small, omnivorous monkeys. They live in multi-male, multi-female
groups of approximately 15-20 individuals and are moderately sexually dimorphic in
many aspects of their physiology. They are well known for their eclectic diets, consisting
of fruit, insects, and small vertebrates such as lizards, birds, squirrels and neonate
coatimundis. Unlike other members of the genus Cebus, however, they are found in both
Central and South America, from Honduras in the North to Ecuador and Columbia in the
South. They are a good species in which to study foraging behaviour because of their highly varied diet and complex food extracting and processing behaviours (Fragaszy et
al. 2004).
3.3.3 Data Collection
During an eight month long study period (May to July 2005 and January to May
2006), covering parts of both the wet and the dry seasons, an assistant and I collected
behavioural data and fecal samples from adults in two well-habituated groups of white-
faced capuchin monkeys (Cerco de Piedra [CP] group [N=18 monkeys, 8 adults] and Los
Valles [LV] group [N=17 monkeys, 8 adults]. Behavioural observations took the form of
all-day focal follows, which were conducted between the hours of 5:00 AM and 6:00 PM
44 (N=50, 393.5 hours). All monkeys were individually identifiable based on their age, sex, facial markings and other individual markings such as scars. Each day two observers would continuously observe one adult monkey all day or for as long as conditions deemed possible (range= 2 hours and 12 minutes up to 12 hours and 53 minutes, mean follow time= 7 hours and 43 minutes). Data were discarded when focal sessions could not be maintained for longer than 2 hours or in cases where the focal animal was not fully visible by at least one observer for greater than 10 percent of the entire amount of possible observation time.
Behavioural and defecation data were recorded using a hand-held data logger
(Psion Workabout MX). This device records time to the second each time an entry is made. Location data were recorded using a handheld Geographic Positioning System
(GPS).
Each time the focal animal fed on fruit, the tree species was recorded and in ideal viewing conditions, the treatment of the seed or seeds in each piece of fruit consumed was recorded as one of a series of mutually exclusive categories (Table 3.1).
Each time the focal animal defecated, the defecation event and number was recorded in the Psion, a waypoint was taken, and the defecation was collected in a vial and labeled. Fecal samples (N=549) were returned to the field laboratory, where each species of seed was identified based on fruit samples that were collected during the focal animal follows. All seeds were then counted and their species and number recorded.
Seeds were examined and any damage apparent to the eye was recorded. The seeds were then planted in one of a series of germination trials (see below). Additionally, where
45 possible, seeds that were handled by the focal animal and discarded (e.g. spat out, rubbed and dropped) were collected and returned to the field laboratory for planting.
3.3.4 Seed Handling
During focal animal follows, when the focal animal fed on fruit and viewing conditions were ideal, the treatment of the seed/seeds in each individual fruit was recorded as one of five mutually exclusive categories (Table 3.1). Because several species of fruit contained multiple seeds, the individual fruit, and not each individual seed, is the unit of analysis here.
The number of records of each category of seed treatment was extracted from the data recorded in the Psion. A percentage of records for each category was determined across all species, as well as the percentage of each category of treatment for each individual species.
3.3.5 Germination Experiments
Each focal animal defecation (N=549) was collected in a small vial, labeled, and returned to the field laboratory. The seeds inside were identified and counted (except in the case of Cecropia peltata and seeds of the Genus Ficus, whose extremely small size and delicacy made individual counts impossible) and any instance of damage recorded.
Seeds of the top five most commonly encountered species, due to their availability, were then subjected to two different experimental treatments in order to determine the effect of gut passage and of feces on germination. These plant species are: Genipa americana
(GA), Sciadodendron excelsum (SE), Trichilia martiana (TM), Acacia collinsii (AC) and
Casearia arguta (CA).
46 In order to test the effect of gut passage on germination rates, a portion
(N=870/1984) of gut passed seeds of the five species were cleaned of feces and planted alongside conspecific seeds that were removed directly from ripe fruit, cleaned of all pulp and planted (N=1028-see Table 3.2 for summary.)
In order to test the effect of white-faced capuchin feces on germination, another portion (N=619/1984) of gut passed seeds of the five species were left in the feces in which they had been deposited and collected. These were planted alongside another portion (N=495) of gut passed seeds that were removed from the same defecation, cleaned of feces and planted in soil that was collected from the exact location of that defecation. Typically in germination experiments where soil is used, controls are planted in sterile, high quality soil (e.g. Kankam 2000) but in this case, due to the natural variation in soil quality at the study site (J.A. Klemens, personal communication) a decision was made to build the possible effect of that variation into the study.
Additionally, seeds in both treatments were taken in equal numbers from the same fecal samples, to minimize the possibility of the experiments being skewed based on variation in gut passage time and its potential effect on seed germination.
Seeds in all treatments were planted on florist’s foam, a commercially available, nutrient-free, sponge-like substance that controls the amount of water available to the plant/seed, thereby controlling for over- and under- watering. These were placed in clean
Petri dishes, watered as needed, housed in a screened outdoor enclosure with natural light, and checked daily for germination.
47 Some seed species were collected from feces for which there was not a sufficient number for a comparative sample (N= 3,157 seeds of 18 species). These were planted in florist’s foam in Petri dishes, watered as needed and checked daily for germination. I compare the germination rates of these to seeds that have been handled by capuchins (e.g. spat out, rubbed and dropped, ingested and passed), with seeds removed directly from fruit.
3.4 Analysis
3.4.1 The Effect of Feces and Gut Passage on Germination
All germination experiments were analyzed using a Proportion of Difference
Analysis (Freund and Simon 1997), which compares the difference between two proportions (Figure 3.2). Where z exceeds 2.33 the difference between proportions is greater than expected by chance at an alpha = 0.05..
3.4.2 The Effect of Feces and Gut Passage on Time to Germination
The time to germination was calculated by multiplying the number of germinations by the number of days since planting, adding the resultant values, and dividing by the total number of germinated seeds in that experimental treatment to arrive at an average number of days to germination.
The mean time to germination was then analyzed for significance using a Test for
Differences Between Means (Freund and Simon 1997, Figure 3.3). Where z exceeds 1.96 the null hypothesis is rejected, the difference between means is considered to be greater than expected by chance at an alpha of 0.05 and therefore significant.
48 3.5 Results
3.5.1 Seed Handling
For the most part, white-faced capuchins swallowed and passed intact either all of
the seeds contained in the 3,596 fruits observed (34%), or part of the seeds contained in
these fruits (34%). Thus they swallow the majority of seeds intact. (Table 3.3). In a further 17% of all records, seeds were spat out, but this treatment was limited to 9 of the
27 species sampled here (Table 3.4). Nine percent of fruits were picked and then
dropped. In only 6% of cases were seeds destroyed through chewing, but this was limited
to 8 of the 27 species.
3.5.2 The Effect of Gut Passage on Germination Rates
For 3 of the 5 species (Acacia collinsii, Casearia arguta and Genipa americana) differences in proportion of germinated seeds were significantly higher for gut passed seeds than for seeds removed directly from fruit (A. collinsii, N1=118/282, N2=187/600,
z=3.24, p<0.001; C. arguta, N1=217/285, N2=66/125, z=4.02, p<0.001; G. americana,
N1=40/100, N2=21/100, z=2.92, p<0.001). For one species there was no difference (T.
martiana, N1=85/100, N2=85/103, z=0, p=1), and for the fifth species, there was a
decrease of 13%, but the difference was not significant (S. excelsum, N1=47/100,
N2=48/100, z=1.83, p=0.03) (Figure 3.4).
3.5.3 The Effect of Gut Passage on Germination Latency
For 4 of the 5 species, the mean time to germination was significantly faster for
gut passed seeds than for controls (G. americana: 14.5 versus 23 days, z=3.72, N1=40,
N2=21, p=<0.001; T. martiana: 7.4 versus 8.5 days, z=2.76, N1=85, N2=85, p=0.006; A.
49 collinsii: 12.8 versus 21.4 days, z=8.97, N1=118, N2=187, p=<0.001; C. arguta: 6.8 versus 10.4 days, z=8.04, N1=217, N2=66, p=<0.001). For the fifth species, control seeds
germinated slightly faster than gut passed seeds, but the difference in mean time to
germination was not significant (S. excelsum: 22.6 days versus 23.7 days, z=0.26, N1=47,
N2=58, p=0.795) (Figure 3.5).
3.5.4 The Effect of Feces on Germination Rates
For 2 of the 5 species (T. martiana and S. excelsum), the difference in proportion
of germinated seeds was significantly higher for seeds cleaned of feces and planted in soil
than for seeds planted in feces (T. martiana, N1=33/85, N2=0/100, z=7.06, p=<0.001; S.
excelsum, N1=45/100, N2=0/100, z=7.76, p=<0.001). For two species, there was a slight
decrease in germination for those seeds planted in feces, but not a statistically significant
one (A. collinsii, N1=45/225, N2=22/101, z=0.375, p=0.352; G. americana, N1=70/1037,
N2=75/99 z=0.823, p=0.206). For one species there was almost no difference between the
two treatments (C. arguta, N1=71/110, N2=72/110, z=0, p=1). (Figure 3.6).
3.5.5 The Effect of Feces on Germination Latency
In two species (S. excelsum and T. martiana) seeds planted in feces did not
germinate at all. For 1 of the 3 species where seeds planted in feces and soil germinated
in both experimental treatments, mean time to germination was significantly faster for
seeds planted in soil (G. americana: 15.5 versus 21.4 days, z=5.25, N1=75, N2=70,
p=<0.001). For one species, seeds planted in feces germinated faster, but the difference
was not significant (A. collinsii: 14.3 versus 15.6 days, z=0.631, N1=22, N2=45,
p=0.528). For the third species, the average time to germination was significantly faster
50 for seeds planted in feces than for seeds planted in soil (C. arguta: 12.9 versus 14.8 days, z=3.29, N1=72, N2=71, p=<0.001) (Figure 3.7).
3.5.6 The Effect of Monkey Treatment on Germination Rates Across All Species
Seeds of 17 of the 18 species that were processed by capuchins and planted by me were ingested and passed intact, one species was rubbed and dropped, three species were spat out and one species was chewed (see Table 3.5 for summary). 49% of gut passed seeds germinated, compared to 32% of seeds removed directly from fruit. No seeds that were rubbed and dropped or chewed germinated (this treatment only occurred in the species Sloanea terniflora). Twenty percent of spat seeds germinated.
Of all monkey treatments across all species, ingestion and gut passage is the only treatment that is associated with a higher rate of germination than seeds removed directly from fruit (49% versus 32%). This increased germination rate with gut passage is statistically significant (N=3157, z=9.44, p=<0.001).
Spat seeds across all species show a statistically significant decrease in germination rate of 12% when compared to seeds removed directly from fruit (N=1501, z=3.24, p=<0.001), as well as a statistically significant decrease in germination rate of
29% compared to gut passed seeds (N=1733, z=7.75, p=<0.001).
When combined, all monkey treated seeds show a statistically significant increase in germination rate of 12% when compared to seeds removed directly from fruit
(N=3157, z=7.19, p=<0.001).
51 3.6 Discussion
3.6.1 Seed Treatment
White-faced capuchins benefit several of the plant species they consume via seed
dispersal. For almost all plant species consumed, and in 68% of fruit treatment records,
capuchins ingest and pass intact either all or some of the seeds contained in consumed
fruits. There were very few observed instances of systematic seed destruction, and those
few observed cases are confined to five species: Guazuma ulmilfolia (100% of records,
N=6), Luehea alternifolia (46%, N=136), Luehea candida (83%, N=19), Lasciviasis negra (100%, N=26), Lasciviasis ruscifolia (70%, N=19).
The fruit of both species of the Genus Luehea accounts for 75% (155 of 266) of all cases of seed chewing and destruction. In both species of Luehea, the fruit is a woody pod that dehisces while on the tree during the months of February and March, allowing the winged seeds, or keys to drop out when the fruits are jostled by the strong papagayo
and nortes trade winds of the dry season (Haber and Frankie 1983). It is during the
months of February and March that capuchins spend much of their time consuming the
seeds of the fruits of Luehea trees. In order to extract the seeds, capuchins bang the
dehisced pods against branches and tree trunks, releasing the winged seed pods. While
they are able to retain some for consumption, a large number are inadvertently dispersed.
So, while they act as seed predators on these two species, it is interesting to note that they
also facilitate the dispersal of these species by mimicking the effect of the winds that
shake the seed pods free.
52 3.6.2 The Effect of Gut Passage and Feces on Germination
Three of the 5 species analyzed here show a significant increase in germination
rates when passed through the intestinal system of a capuchin. In contrast, the presence of
feces has either no effect on germination, or, in 2 of the 5 species analyzed here, is
significantly detrimental to germination. This variable answer to the question of whether
capuchins have a positive or negative effect on the seeds of the plants they consume can
be better understood when the results are examined more closely.
The two species (S. excelsum and T. martiana) that are significantly negatively
affected by the presence of feces are both species that fruit in the wet season, a part of the year when precipitation is extremely high (Coen 1983) and occurs on an almost daily basis. Of the 800 seeds that were placed out in the forest during the wet season as another part of this study, none had any fecal matter remaining after 3 days- it had all been washed away. Therefore, while feces has a negative effect on germination for these two species, the effect of feces- at least for fruit consumed and defecated in the wet season- may not be a biologically meaningful measure due to the absence of feces.
Additionally, the two species that do not germinate when left in feces are the only two species in this sample that do not show a significant increase in germination when passed through the capuchin intestinal system. They are also the only two species in this sample that exhibit signs of a bird dispersal syndrome, having small, unprotected, unhusked, brightly coloured fruits (see Janson 1983, Link and Stevenson 2004). S. excelsum produces small (mean width=7.1mm, N=102) bright purple fruit that contain multiple seeds (mean=8, N=24) that are paper-thin and extremely small (<2mm in all
53 dimensions). T. martiana produces yellow seed pods that dehisce to reveal small seeds
(mean width=4.2mm, N=206, mean number of seeds per pod=4.8, N=27) covered in a
brilliant red aril (Figure 3.8).
The remaining three species (and those for which gut passage increases germination) exhibit signs of a mammal-dispersal syndrome (Ibid.). Genipa americana is
a large (70mm in diameter), pale greenish-yellow fruit (Enquist and Sullivan 2001) with a
very tough, difficult to penetrate outer skin. Fruits contain multiple, large seeds (mean width=13.2mm, N=204, mean number of seeds per fruit=149, N=11). Casearia arguta is also a large (6-6.5cm long), pale greenish-yellow fruit with a very tough, difficult to penetrate outer skin. Fruits contain multiple, large seeds (mean width=11.1mm, N=79, mean number of seeds per fruit=23.1, N=32). Acacia collinsii, while producing relatively
small seeds as well as relatively few seeds per fruit (mean width=2.76mm, N=200, mean
number of seeds per fruit=7.78) is heavily protected (Figure 3.8).
Acacia collinsii trees are covered by sharp thorns that provide highly aggressive
Pseudomyrmex ants shelter in exchange for protection from predators. This ant-acacia mutualism is one that has long been studied by ecologists (Janzen 2003), and is rarely interrupted by frugivores. During the course of this study, only one other species, the white-throated magpie jay (Calocitta formosa) was observed to consume the fruit of A. collinsii. They would do so by flying closely to the dehisced, woody seed pod and quickly picking out the small black seeds that are covered in and stuck together with yellow aril, without landing on the tree itself. Their attempts were rarely successful, and they were never observed to open seed pods, or remove seed pods from trees. This
54 indicates that their consumption was limited both by the difficulty of this method of foraging as well as by the constraint of foraging on only those seed pods which had dehisced. Capuchins, on the other hand, are able to remove and open non-dehisced seed pods, and overcome and ignore ant defenses, consuming large amounts of A. collinsii fruit in the process. The nearly unique ability of the white-faced capuchin to successfully forage on this species indicates the possibility of a mutually beneficial relationship between these two species (Young et al., In Press).
3.6.3 The Effect of Feces and Gut Passage on Time to Germination
The effect of feces and gut passage on germination latency follows the same pattern as the previously described effect of each on germination rate: increased time to germination when planted in feces, and decreased time to germination for gut passed versus control seeds. In the 3 species for which feces does not preclude germination, 1 species (Genipa americana) germinates significantly faster when planted in soil than when planted in feces. Here, as with germination, the presence of feces has a negative or minor effect on time to germination for all species.
Four out of 5 species germinate significantly faster when passed through the capuchin intestinal system than when removed from fruit and cleaned. In the fifth case, there is a slight increase in time to germination with gut passage (Sciadodendron
excelsum). Interestingly, this is one of the two species that also does not show an increase
in germination rates with gut passage, and did not germinate at all when planted in feces.
The remaining 4 species germinate faster after gut passage. Here, as with germination rates, gut passage has a markedly positive effect on germination time in three species
55 (Acacia collinsii, Genipa americana and Casearia arguta) and a relatively minor effect
on the fourth, Trichilia martiana (7.4 versus 8.5 days).
Differences in time to germination can have a strong effect on the dispersal success of a seed. Preliminary evidence from recent research indicates that secondary predation is a crucial aspect of the seed dispersal process (Chapman 1989, Estrada et al.
1999, Chapman et al. 2003). The deposition of a seed is not the final step in the plant-
animal interaction, as the forest floor is teeming with insects and rodents that prey on
dispersed seeds. One study on primate-dispersed seeds in Costa Rica found that
approximately 80% of seeds were removed from animal feces a mere one week after initial deposition (Chapman 1989). Any reduction in the time a dispersed seed spends on the ground prior to germinating reduces its chance of being preyed upon, and is hence a
potentially crucial aspect of the dispersal process.
3.6.4 Seed Treatment and Seed Germination across all Plant Species
The most common form of seed treatment is ingestion, and across the 18 species
that were planted in a controlled environment the highest rate of germination occurs
amongst seeds that have been consumed and passed. While there are a few cases where
capuchin seed handling precludes germination, these are comparatively rare, and
confined, in two cases (rubbing and chewing) to one species: Sloanea terniflora.
S. terniflora is a rare, large, evergreen tree, occurring with local abundance
around the stream beds and wetter areas of the forest (Hartshorn 1983). It occurs very
rarely in the home ranges of the groups studied here, with a density of 0.6 per ha in the
CP range, and 0.0 per ha in the LV range (Chapman and Fedigan 1990). However, during
56 the field season of 2006 the LV group frequently traveled approximately 1 km west of
the western edge of their usual home range to a streambed containing a cluster of 12
large, fruiting Sloanea terniflora trees.
The fruit of S. terniflora is a small ovoid, covered with thick, purple urtricating
hairs that resemble fiberglass (Enquist and Sullivan 2001), and are extremely irritating to
the skin. Capuchins rub the hairs off of the woody seed pods (see O’Malley and Fedigan
2005 for a description of techniques) and then bite into the seed pod, often fracturing at least some of the aril-covered seeds inside. Capuchins also spit out, as well as swallow and pass the seeds of this fruit. It is only in some cases that seeds are rubbed and dropped unopened, or chewed.
It is interesting to note that white-faced capuchins are, to my knowledge, one of only two species to consume the fruits of this tree (the other being Ateles geoffroyi,
Chapman et al. 1995), which seems to belie classification within any of the existing dispersal syndromes. Therefore, while rubbing and dropping these seed pods seems to preclude germination (0 of the 29 rubbed and dropped pods germinated when planted), it is a form of seed treatment that seems unique to this species of tree, and is not the only form of treatment this fruit receives.
Overall, germination success is highest in gut-passed seeds, and the most common form of seed treatment by capuchins is consumption and gut passage. Other forms of seed handling (e.g., spitting, chewing, picking and dropping) result in decreased germination success, but are comparatively rare as well as confined to a relatively small number of species.
57 3.7 Conclusion
In a few cases capuchin seed handling systematically results in seed death, but this is interspersed with inadvertent dispersal of these species in a manner which mimics the natural dispersal mechanism of the species. While it was not possible during the course of this study to examine the effect of capuchins on some of the wind-dispersed species which they consume, it would be interesting in future to have some measure of the number of seeds which are inadvertently dispersed in cases of seed predation.
White-faced capuchins benefit many of the food trees they consume via seed dispersal. In most cases, capuchins swallow seeds whole and pass them intact, and, of the seed treatment types and species considered here, this form of seed handling results in the highest rates of germination vis-à-vis other treatments. In four of the five cases examined here, seed ingestion and defecation also causes seeds to germinate faster. Decreased germination latency, along with increased germination potential, are advantages that white-faced capuchins offer some of their food species. Thus, with respect to quality, capuchins contribute positively to the reproduction of certain plants, and thereby affect the patterns of maintenance and regeneration of the forests in which they live.
58 Tables
Table 3.1. Ethogram of seed treatment.
Treatment Definition
Swallows Whole Swallows an entire fruit, or seed-bearing section of fruit.
Spits Out Spits out each seed.
Picks and Drops Picks a fruit and drops it without feeding on any seed- bearing part.
Chews Chews and swallows or spits out every chewed seed.
Partial Swallow/ Partial Swallows at least one seed in a fruit, and spits out, drops Spit/Partial Pick/Drop/Chew or chews at least one seed in the same fruit.
Table 3.2. Summary of germination experiments Species N Seeds- Gut N Seeds- Gut N Seeds- N Seeds- Minimum Passage Passage Feces Feces Number of Control Control Days Surveyed GA 100 100 100 99 35
SE 100 100 100 100 33
TM 103 103 84 85 22
AC 282 600 225 101 155
CA 285 125 110 110 35
All 870 1028 619 495 280
Table 3.3 Fruit treatment across all 27 species sampled Swallows Partial Spits Out Picks and Chews % (N) % (N) % (N) Drops % (N) % (N) 34% (1,213) 34% (1,245) 17% (602) 9% (327) 6% (209)
N= 3, 596 fruits of 27 species
59 Table 3.4 Seed treatment by species Species Swallows Partial Spits Out Picks and Chews N % (N) % (N) % (N) Drops % (N) % (N) Bursera simarouba 16% (5) 5% (2) 41% (13) 38% (12) 0% (0) 32 Genipa americana 15% (15) 76% (76) 0% (0) 0% (0) 0% (0) 101 Acacia collinsii 1% (8) 96% (595) 1% (7) 2% (11) 0% (0) 621 Alibertia edulis 0% (0) 100% (1) 0% (0) 0% (0) 0% (0) 1 Anona reticulada 43% (9) 57% (12) 0% (0) 0% (0) 0% (0) 21 Ardisia revolute 83% (24) 0% (0) 7% (2) 10% (3) 0% (0) 29 Apeiba tibourbou 0% (0) 62% (8) 0% (0) 31% (4) 8% (1) 13 Casearia arguta 82% (125) 13% (19) 0% (0) 5% (8) 0% (0) 152 Cecropia peltata 54% (46) 19% (16) 12% (10) 15% (13) 0% (0) 85 Cedrela odorata 0% (0) 100% (3) 0% (0) 0% (0) 0% (0) 3 Ficus spp. 43 (248) 48% (280) 0% (2) 8% (48) 0% (0) 578 Guazuma ulmilfolia 0% (0) 0% (0) 0% (0) 0% (0) 100% 6 (6) Karwinskia 2% (7) 2% (6) 88% (299) 8% (27) 0% (0) 339 caldronii Luehea alternifolia 0% (0) 51% (153) 0% (0) 3% (9) 46% 298 (136) Luehea candida 0% (0) 9% (2) 0% (0) 9% (2) 83% 23 (19) Lasciviasis negra 0% (0) 0% (0) 0% (0) 0% (0) 100% 26 (26) Lasciviasis 0% (0) 30% (8) 0% (0) 0% (0) 70% 27 ruscifolia (19) Malvaviscus 67% (31) 33% (15) 0% (0) 0% (0) 0% (0) 46 arboreus Manilkara chicle 18% (2) 18% (2) 0% (0) 64% (7) 0% (0) 11 Muntingia calabura 96% (130) 4% (5) 0% (0) 0% (0) 0% (0) 135 Randia monantha 100% (2) 0% (0) 0% (0) 0% (0) 0% (0) 2 Sciadodendron 92% (377) 0% (0) 3% (11) (6%) 23 0% (0) 411 excelsum Simarouba glauca 0% (0) 0% (0) 47% (117) 53% (134) 0% (0) 251 Sloanea terniflora 4% (5) 0% (0) 96% (136) 0% (0) 0% (0) 141 Trichilia martiana 86% (155) 0% (0) 3% (5) 11% (19) 0% (1) 180 Unknown 95% (19) 0% (0) 0% (0) 0% (0) 5% (1) 20 Zuelania guidonia 9% (5) 78% (42) 0% (0) 13% (7) 0% (0) 54 N= 3,596 fruits of 27 species
60 Table 3.5. Summary of all germination experiments
Seed Species Planted %Germinated Treatment (N)
Acacia collinsii, Alibertia edulis, Anona reticulada, Casearia arguta, Curatella americana, Genipa Gut Passed americana, Karwinskia caldronii, Luehea 49% alternifolia, Lasciviasis negra, Malvaviscus arboreus, Muntingia calabura, Randia monantha, (756/1549) Sciadodendron excelsum, Sloanea terniflora, Trichilia martiana, Zuelania guidonia, Unknown
Rubbed and Sloanea terniflora 0% Dropped (0/29)
Spit 20% Simarouba glauca, Sloanea terniflora, Karwinskia caldronii (36/184)
Chewed 0%
Sloanea terniflora (0/26)
All Monkey All of the above 44% Treatments (804/1840)
Removed from Acacia collinsii, Casearia arguta, Trichilia 32% Fruit martiana, Sciadodendron excelsum, Simarouba (Unprocessed) glauca, Sloanea terniflora, Karwinskia caldronii (419/1317)
N=3157
61 Figures
Figure 3.1. Possible effects of gut passage and feces on germination rate and latency.
Dispersal Stage Process Possible Effects
Seed Ingestion
Digestive fluids reduce or Gut Passage scarify seed coat Increased germination
rate
Chemical composition of Decreased feces further reduces germination seed coat latency Chemical composition of Seeds Deposited in Feces feces induces germination
Feces provides nutrients
for germinated seed
Figure 3.2. Equation for the Proportion of Difference Analysis
x1 - x2 z = . n1 n2………………… with p-hat = x1 + x2 √ p-hat (1 – p-hat) (1 + 1 ) n1 + n2 n1 n2
62 Figure 3.3. Equation for the Test for Differences Between Means
mean1 - mean2 z = . n1 n2………………… √ ơ11 + ơ12 n1 n2
Figure 3.4. Bar graph depicting the effect of gut passage on germination rates.
1.0 Gut Passed Control 103 * 103 0.8 285
0.6 100 125 * * 100 282 100 0.4 600
99 0.2
Proportion of Germinated Seeds 0.0 ii a a a llins ican rgut tian lsum . co mer C. a mar exce A G. a T. S.
Species * indicates a significant difference.
63 Figure 3.5. Bar graph depicting the effect of gut passage on germination latency.
25 100 * 100 * 100 600 20 Gut Passed Control 15 100 282 * 125 10 * 103 103 285
5
0 i Mean Number of Days to Germination cana llinsi guta lsum tiana meri . co C. ar xce mar G. a A S. e T.
Species
* indicates a significant difference.
64 Figure 3.6. Bar graph depicting the effect of feces on germination rates
0.8 99 100 Seeds in Feces Seeds in Soil 110 110 0.6
* 100 * 0.4 85
84 100 101 225 0.2
Proportion of Germinated Seeds Proportion of Germinated 0.0 i llinsi cana guta tiana lsum . co meri C. ar mar xce A G. a T. S. e
Species
* indicates a significant difference.
65 Figure 3.7. Bar graph depicting the effect of feces on germination latency.
25 Seeds in Feces 225* Seeds in Soil 20 * 101 225 110 15 101 110
100 10
5
0
Mean Number of Days to Germination i cana llinsi guta meri . co C. ar G. a A
Species
* indicates a significant difference.
66 Figure 3.8. Photographs of the five most commonly consumed fruits of the 2005 and 2006 field season: a) Sciadodendron excelsum, b) Trichilia martiana, c) Genipa americana, d) Casearia arguta, e) A member of CP group opening an Acacia collinsii seed pod. a) b)
c) d)
e)
(Photo Credits: SE, TM and GA- Smithsonian Tropical Research Institute, Center for Tropical Forest Science Tree Atlas of Panama, ctfs.si.edu. CA- Area de Conservacion Guanacaste Species Home Page, acguanacaste.ac.cr. AC- E. Luinstra.)
67 Chapter Four: Spatial Patterns of Seed Dispersal by White-Faced Capuchins (Cebus capucinus) and Implications for Seed Survival
4.1 Introduction
There are numerous ways of measuring the effect of animals on the seeds of the fruit they disperse. Quantity and quality are two important measures of dispersal effectiveness (Schupp 1993). A third equally important although less often examined aspect of seed dispersal, is the impact of distance and seed distribution patterns (seed shadows) on germination and growth, and on seedling survival. The spatial dimension of seed dispersal is particularly important because it is the focus of most theoretical attempts to understand the process of endozoochory, or seed dispersal by animals.
Fruit is expensive for a plant or tree to produce, and when the possible reproductive benefits of fruit production for the plant are considered, the primary question is: where exactly does the benefit for the plant lie? Why did some plants evolve to produce fruit? In short, what is the purpose, from the point of view of the plant, of animal dispersal? This matter of animal dispersal of seeds is crucial to understanding the
theoretical basis of the long-standing relationship between animals and angiosperms. And
the answer to these questions is: movement of seeds, in some manner and at variable
distances, away from the parent plant benefits the plant. Essentially, while other factors in
the seed dispersal process (e.g. seed handling, seed coat scarification in the gut etc.) are
important predictors of seed survival in the present moment, these are likely secondary
effects of an original long-standing dispersal strategy on the part of the plant.
There are many studies of seed dispersal and on the other aspects of endozoochory, such as secondary dispersal and predation, recruitment limitation, and the
68 effects of gut passage and handling. But, with respect to the question of the basis of
dispersal per se there are three main hypotheses: the Janzen-Connell model, the
colonization hypothesis, and the environmental homogeneity model.
4.1.1 The Janzen-Connell Model and the Seed Escape Hypothesis
The Janzen-Connell model or seed escape hypothesis (Howe and Smallwood
1982), addresses the correlation between seed mortality and distance from parental trees
(Janzen 1970; Connell 1971). According to the Janzen-Connell model, seeds that are
deposited underneath the canopy of the parent tree will attract and are more likely to fall
victim to a host of species-specific seed predators, fungal pathogens and later herbivores
at a higher rate than those that are deposited further from the adult tree. Janzen (1970)
further proposed that predators may be density-responsive by concentrating their
destruction near fruiting adults, where initial seed fall will be highest. As well, seedlings
that establish closer to parent trees suffer higher rates of competition with conspecifics
(Connell 1971). Forest diversity is thus maintained, and a sort of checkerboard pattern of
different species, intermingled and dispersed away from one another, should prevail, as
non-conspecifics successfully establish themselves adjacent to other species in niches
containing seed and seedling predators that are host-specific to their neighbours and busy
competing with each other.
This elegant model was well received and survived largely undisputed for many years, even without much evidence from field studies to support it (Clark and Clark
1984). However, later studies that focused on the spatial patterns of existing tropical forests have yielded evidence to dispute it, e.g. Hubbell’s (1979) study which plotted the
69 actual spatial distribution of all adult trees in a plot of mature tropical forest and found mammal-dispersed tree species to be more highly clumped in distribution than trees with other dispersal mechanisms. Other studies since have found evidence that both supports and disputes this hypothesis (see Howe and Smallwood 1982 for review), indicating that this model still requires empirical testing, and that this once largely undisputed theoretical stronghold is perhaps not the right answer.
4.1.2 Colonization Hypothesis
The second hypothesis posits that the primary advantage to the dispersal of seeds is the “chance occupation of favorable sites that are unpredictable in time and space”
(Howe and Smallwood 1982). Essentially, dispersal can increase the likelihood of germination, establishment and survival, when it results in seed deposition in an open niche (e.g. tree fall gap) while minimizing competition for resources (light, water, soil nutrients, etc.) between offspring and parent (Howe and Smallwood 1982).
4.1.3 Environmental Homogeneity
Another, more recent, theoretical model that seeks to explain the purpose of endozoochory as a function of distant-dependent seed mortality is that seed dispersal by animals will arise in areas of environmental homogeneity where microhabitats are similar across a larger area (Chapman and Chapman 1996). This model is the mirror image of the colonization hypothesis, in that it states that where the resources important for the survival, germination and growth of a tree species are patchily distributed, “the predictability of finding resources equivalent to the ones at the starting location decreases with distance” (Chapman and Chapman 1996). Thus, in situations of environmental heterogeneity, or patchy resource distribution, trees should not favour strategies of
70 dispersal, as this would be likely to result in dispersal away from areas favourable to germination and growth. Conversely, if these resources are randomly or evenly distributed throughout the environment there should be no relationship between predictability and distance from the parental tree, and in these cases, trees should have a strategy favouring dispersal (Chapman and Chapman 1996).
4.1.4 Measuring the Effect of Distance
All three hypotheses rely on the idea of distance as the critical variable not only in seed survival, but in the resultant structure of forests and the very existence of fruiting trees. Indeed, “the ultimate null hypothesis is that adult distributions closely reflect seed distributions” (Howe and Smallwood 1982). Thus, the distance and patterns of seed dispersal are not only one possible result of plant-animal relationships, but perhaps the very reason they exist. Given that all extant models used to explain the existence of seed dispersal by animals focus on the reproductive benefit to the plant as being situated in the distance that a seed is carried and the location of its deposition, the patterns of seed dispersal produced by animals are crucial to both a practical evaluation of disperser effectiveness, and a theoretical evaluation of dispersal systems.
In this study, I address whether white-faced capuchins disperse ingested seeds in a clumped or dispersed manner, as well as the variables most closely associated with seed germination and seedling survival at these sites. The distance of seed dispersal by white- faced capuchins is examined within the context of the above models, as well as the distance that seeds are carried, the distance of defecated seeds from one another, and the patterns that this dispersal takes. Additionally, the suitability of microhabitats for seed
71 germination and seedling establishment and growth in deposition locations are examined with respect to distance from parent trees and fruiting conspecifics. Primarily,
this study is an attempt to directly test the Janzen-Connell model, as it is a comparison of
survival and growth rates of mammal-dispersed plants in light of the distance to their
parent trees.
4.2 Research Questions and Predictions
4.2.1 Research Questions
1) At what distance do capuchins disperse seeds away from parent trees?
2) At what distance are seeds dispersed from each other?
3) Are seeds dispersed in a clumped or dispersed manner?
4) What is the effect of distance from parent trees and fruiting conspecific trees on
secondary dispersal and predation of seeds and seedling establishment and
growth?
5) What is the effect of microhabitat variables in locations of seed deposition on
secondary dispersal and predation of seeds and seedling establishment and
growth?
4.2.2 Predictions
1) Based on the distances that white-faced capuchins travel each day, I predict that
seeds will be dispersed away from parent trees.
72 2) Based on the distances that white-faced capuchins travel each day and the
frequency of their defecations, I predict that seeds will be dispersed far away from
each other, though closer to each other than to parent trees.
3) Based on the distances that white-faced capuchins travel each day and the
frequency with which they defecate, I predict that seeds will be widely dispersed,
and not clumped.
4) Based on the Janzen-Connell model/seed escape hypothesis, I predict that seeds
deposited further from parent trees and fruiting conspecifics will remain
unaffected by secondary dispersers and predators longer, resulting in higher rates
of germination, and that seedlings growing further from parent trees and fruiting
conspecifics will achieve higher rates of growth and survival than those growing
closer to parent trees and fruiting conspecifics.
5) I predict that microhabitat variables in deposition locations will be suitable for
seed germination and seedling growth, but that these variables will be less critical
in predicting survival and growth than distance to parent trees and nearest fruiting
conspecific trees.
4.3 Methods
4.3.1 Study Site
The study took place at Santa Rosa National Park, a sector of the Area de
Conservacion Guanacaste (ACG). The ACG is located in northwestern Costa Rica on the
Pacific Ocean, approximately 40 km south of the Nicaraguan border. At 110,000 hectares the ACG is the largest continuous reserve of regenerating tropical forest in the world.
73 Much of the forest of the Santa Rosa sector is deciduous, tropical dry forest, though there are fragments of semi-evergreen and riparian forest at various stages of growth and regeneration, as well as regenerating pasture land (Janzen 1983).
Santa Rosa National Park is home to thousands of plant species, hundreds of bird species, and over 100 species of mammals. These mammal species include three non- human primate species: the white-faced capuchin monkey (Cebus capucinus), the black- handed spider monkey (Ateles geoffroyi) and the mantled howler monkey (Alouatta palliata).
4.3.2 Study Subjects
White-faced capuchin monkeys (Cebus capucinus) are arboreal, diurnal omnivores. Their highly varied diet is composed of numerous species of invertebrates, vertebrates, fruits, flower buds and flowers. Cebus monkeys are widely distributed throughout Central and South America from Honduras to Ecuador (Rowe 1996). White- faced capuchins, like other members of the genus Cebus, live in multi-male, multi-female groups of approximately 15-20 individuals and are moderately sexually dimorphic in many aspects of their physiology.
4.3.3 Data Collection
During an eight month long study period (May to July 2005 and January to May
2006) an assistant and I collected behavioural data and fecal samples from adults in two well-habituated groups of capuchins: Cerco de Piedra (CP) group (N=18 monkeys, 8 adults) and Los Valles (LV) group (N=17 monkeys, 8 adults). Behavioural observations were done as focal follows between the hours of 5:00 AM and 6:00 PM. A total of 50
74 follows were conducted involving a total of 393.5 hours of observation. All monkeys were individually identifiable based on their age, sex, facial markings and other individual markings such as scars. Each day the two observers would continuously observe one adult monkey all day or for as long as conditions were deemed appropriate
(see below). The mean duration of a follow was 7:43 with a range from 2:12 to 12:53.
Focal follows that lasted less than 2 hours were not analyzed, nor were focal follows where the focal animal was not fully visible by at least one observer for greater than 10 percent of the entire amount of possible observation time.
Behavioural and defecation data were recorded using a hand-held data logger
(Psion Workabout MX). Location data was obtained using a Garmin GPS unit..
Each time the focal animal fed on fruit, the event was recorded in the Psion along with the tree species and the number of trees of the same species that the focal animal fed on during the follow, e.g. the third Genipa americana tree fed on during a follow would be recorded as Genipa americana 3, the fourth as Genipa americana 4. A fruit-eating bout was considered to begin the moment that the focal animal picked or bit the first piece of fruit, and ended when the focal animal left the tree, changed their behavioural state (e.g. began to eat insects, groom, rest), or when they continued to forage but did not pick or eat fruit for 30 seconds. A waypoint was recorded using the GPS unit for each tree at which the focal animal consumed fruit, with the same name and number as was recorded in the Psion.
Each time the focal animal defecated, the defecation event and number was recorded in the Psion, a waypoint was taken, and the defecation was collected in a vial
75 and labeled. Fecal samples (N=549) were returned to the field laboratory, where each species of seed was identified based on fruit samples that were collected during the focal animal follows. All seeds were then counted and their species and number recorded.
Some seeds were planted in florist’s foam in the lab and, upon germination, planted in soil collected directly from the forest. Those that established as seedlings such that two or more leaves were present were retained in order to be planted in quadrats used in testing distance and microhabitat variables and their effect on seedling growth and survival (see below). Remaining seeds were returned to the feces in which they had been deposited in order to be placed in quadrats for use in testing distance and microhabitat variables and their effect on secondary dispersal and predation, seed germination and seedling establishment (see below).
4.3.4 Dispersal Distances
The distance a seed traveled from the parent tree was determined by counting back from a defecation event containing a seed to that species of tree within the range of capuchin gut passage time. The range of possible gut passage times for capuchins is quite high (from 35 minutes to up to 5 hours). This gut passage time range was determined during the course of the focal animal follows. Whenever a species of a fruit was consumed that had been eaten only once during the day by a focal animal that was continuously observed for up to 12 and a half hours, the time between eating the fruit and defecating the seed was determined by counting back the minutes from the defecation event to the feeding event. This range is consistent with the range of gut passage times
observed by Wehncke (2003) for wild white-faced capuchins consuming rarely eaten
fruits (mean=94 minutes, + 43 minutes) and on captive white-faced capuchins fed four
76 different cultivated fruit species and observed until seeds appeared (mean time for
<75% of seeds to appear=105 minutes, + 38 minutes).
It often happened that multiple individual trees of a species would be consumed
over the course of a single day, and the focal animal would produce multiple defecations
containing seeds of that species. In these cases, where the exact parent tree wasn’t
known, Wehncke et al.’s (2003) mean of 105 minutes to seed appearance was used. Thus,
whichever tree of the species found in the focal animal’s feces was consumed closest to
105 minutes prior to the defecation event (excluding any outside of the observed possible gut retention time range of 35 minutes to 5 hours) was defined as the parent tree. The distance between the parent tree and the defecation event was then determined by comparing the distance between the waypoint records for the parent tree and defecation using Ozi Explorer.
Distances between defecations were calculated in all cases where two focal animal defections were observed that were not separated by any period during which the focal animal was out of the sight of at least one of the two observers. In these cases, distances between the two defecation events were determined by comparing the distance between the waypoint records using Ozi Explorer.
4.3.5 Defecated Seed Quadrats
Feces containing seeds collected during the focal animal follows were returned to the field laboratory for counting and identification. Seeds of the five most commonly ingested and passed species (Acacia collinsii, Casearia arguta, Sciadodendron excelsum,
Trichilia martiana and Genipa americana) were placed back in the feces in which they
77 had been deposited and returned to between 5 and 10 different actual defecation
locations. Quadrat locations were chosen based on the distances of defecation locations
from the parent tree, where one was the closest recorded defecation to the parent tree, another was the furthest, and the remaining locations were at roughly equally spaced
intermediate distances between the two. At each defecation location, four piles of ten
seeds would be placed on the forest floor a minimum of a meter away from each other
and microhabitat variable data taken at that time.
Microhabitat variable data recorded for each pile was: the percentage of canopy
openness (hereafter referred to as canopy cover), the distance of the pile from the nearest
fruiting conspecific tree, the diameter at breast height (DBH) of the nearest fruiting
conspecific tree, and the distance to the parent tree. Canopy cover was determined using a
spherical concave densiometer. The distance of the nearest fruiting conspecific was
determined by walking in ever-increasing rings around the defecation site and recording a
waypoint using a handheld GPS unit for each adjacent fruiting conspecific tree, up until
the distance of the parent tree.
All piles were checked for disappearance, germination, seed establishment and
seedling growth three days after their initial deposition at the quadrat sites. They were
then checked every seven days thereafter until the end of the study period in the wet
season (July 27th, 2005), and for those planted in the dry season, the end of that field
season (July 15th, 2006). All cases of disappearance, germination, seedling establishment
and seedling growth were recorded.
78 4.3.6 Spit Seed Quadrats
In the case of three commonly consumed fruit species (Acacia collinsii,
Simarouba glauca and Karwinskia caldronii), seeds were frequently cleaned of the fruit
pulp and spit out underneath the canopy of the parent tree by white-faced capuchins. In
these cases, several individual trees of each species were chosen as quadrat sites, where
seeds that were cleaned of fruit and spit out by white-faced capuchins were returned to
locations underneath the canopy of parent trees in five piles of five seeds each. Because
capuchins will spit seeds out underneath the canopy at varying distances from the trunk
and the canopy edge, piles were laid out in one transect emanating out from the trunk.
The piles were evenly spaced along transects such that there was a pile next to the trunk of the parent tree, one pile at the edge of the parent canopy, and the remaining piles were evenly spaced between them. This exact spacing depended on the size of the canopy, e.g. if the radius of the canopy was 5 meters and 6 piles were being laid out along a single transect, the piles would be spaced at 1 meter intervals starting from the trunk, and ending at the canopy edge. A second transect of equal distance emanating from the same parent trunk was laid out with an equal number of piles containing an equal number of intact fruits that had not been cleaned of the fruit pulp. These, too, were spaced equidistantly from one another, as described above.
All piles were checked for disappearance, germination, seed establishment and seedling growth three days after their initial deposition at the quadrat sites. They were then checked every seven days thereafter until the end of the study period in the wet season (July 27th, 2005), and for those planted in the dry season, the end of that field
79 season (July 15th, 2006). All disappearance, germination, seedling establishment and
seedling growth was recorded.
4.3.7 Seedling Quadrats
Feces containing seeds collected during focal animal follows were returned to the
field laboratory for counting and identification. A portion of the seeds of the five most
commonly ingested and passed species (Acacia collinsii, Casearia arguta,
Sciadodendron excelsum, Trichilia martiana and Genipa americana) were planted in
florist’s foam until germination and, upon germination, planted in soil collected from the
forest. Those that established as seedlings such that two or more leaves were present were retained for use in seedling quadrats. These seedlings were planted on the forest floor a minimum of one meter away from each other at the same defecation locations as conspecific seed piles. Each seedling was planted at least a meter from its closest neighbour and tagged with a numbered aluminum tree tag. Data on microhabitat variables were taken at the time of planting and the same measures taken as in the seed data (see above).
At the time of planting the following information about each individual seedling was recorded: height of the plant stem (hereafter referred to as height), the number of leaves, the length of the longest leaf, and the state of the leaves. Leaf state was recorded as either undamaged (all leaves), some damage (one or more leaves) or completely destroyed/gone. Size measurements were taken using vernier calipers.
The seedling quadrats, as with the seed quadrats, were checked three days after planting, and every seven days thereafter until the end of the study period in the wet
80 season (July 27th, 2005), and for those planted in the dry season, the end of that field season (July 15th, 2006). Seedlings were also checked on the last day of every month between field seasons.
4.3.8 The Dispersal Pattern of Feces
In order to determine whether capuchin feces are clumped or dispersed a coefficient of dispersion is used (Sokal and Rohlf 1995). Typically this is done using quadrats or fecal collection sites placed out in the field (e.g. Sokal and Rohlf 1995,
Chapman 1989), but because of the large home ranges of white-faced capuchins (LV group’s home range for 2005-2006 encompassed 175.58 ha), this was deemed to be impractical. Instead, a map was made which includes the home range of each of the two study groups (in ArcView 3.2). A 95% kernel was used (in ArcView 3.2, Animal
Movement 2.04) to delineate the groups’ home ranges based on waypoints taken every thirty minutes on the hour and half-hour during focal animal follows spanning the twelve months between May 2005 and May 2006 (1344 waypoints for CP group, 974 waypoints for LV). This map was then superimposed with a 50 meter x 50 meter grid, and all waypoints of defecations from both field seasons were then uploaded into the map. Each grid was assigned an alphanumeric identification and the number of defecations in each
50 meter x 50 meter grid square falling within each home range were then counted (CP group N=404 quadrats containing 335 defecations; LV group N=699 quadrats containing
197 defecations). Grid squares were not counted in cases where less than 50% of the grid square was part of the home range (Figures 4.1 and 4.2). In this way, post-hoc quadrats were constructed for use in a coefficient of dispersion analysis.
81 4.4 Analysis
Separate backward stepwise logistic regressions were conducted to determine the
effects of distance from the parent tree, percentage of canopy openness, distance to nearest fruiting conspecific tree, and diameter at breast height (DBH) of nearest fruiting conspecific tree on four different dependent variables: 1) whether there were seeds/germinated seeds/seedlings present at the end of the study period for the three species for which seeds survived to the end of the study period (Genipa americana,
Casearia arguta and Sciadodendron excelsum); 2) whether seeds germinated, given that there were seeds remaining in the piles at least 10 days after they were put out; 3) whether seedlings established in those piles where one or more seeds had germinated; 4) whether seedlings survived in the seedling quadrats to the end of the study period for the four species where seedlings remained alive to the end of the study period (Genipa americana, Acacia collinsii, Casearia arguta and Trichilia martiana). The pile, and not
the individual seed, is the unit of analysis.
Separate backward stepwise regressions were conducted to determine the effects
of distance from the parent tree, percentage of canopy openness, distance to nearest
fruiting conspecific tree, and diameter at breast height (DBH) of nearest fruiting
conspecific tree on three different dependent variables: 1) the length of time that seeds
remained in seed quadrats, where length of time was entered both as the maximum
number of days since placement in quadrats that (a) live seed(s) remained in any form,
and as the number of days since placement in quadrats that was the first instance of all
seeds being removed; 2) the length of time that seeds remained in spit seed quadrats; 3)
seedling growth for seedlings planted in quadrats, where seedling growth was measured
82 as the change in seedling height, length of longest leaf, number of leaves and seedling
damage. Change in the first three variables was recorded as the percentage increase
between the values at first planting and at last measurement, which was determined by
dividing the initial measurement by the final measurement, e.g. if a seedling was 4cm tall
when planted and 8cm tall at the end of the study period, height increase was recorded as
50%. Damage was measured as the percentage of records where each plant was recorded
as damaged versus undamaged, e.g. if the plant was undamaged for 6 of 10 weekly
observations, plant damage was recorded as 60%.
Unless stated otherwise, all analyses were conducted in SPSS for Windows 14.0.
4.4.1 Coefficient of Dispersion
A Coefficient of Dispersion (CD) analysis was used to determine whether
capuchin defecations were clumped or dispersed, using the number of defecations per
50x50m grid square (Figures 4.1 and 4.2) as the units of analysis. A number of
defecations per grid square was computed and the coefficient of dispersion calculated as
the ratio of the variance to the mean of the number of defecations per quadrat: CD = s2 Y
This test is a means to determine whether the defecations are distributed in a
Poisson distribution, i.e. randomly (Sokal and Rohlf 1995). The CD value will be near 1 in Poisson distributions (randomly distributed about a mean, and dispersed), while a value >1 indicates a clumped distribution. A Coefficient of Dispersion was determined for both CP and LV groups.
83 4.5 Results
4.5.1 Dispersal Times and Distances
White-faced capuchins disperse seeds an average of 235.6 meters away from the parent tree (median=200 meters, range=4 to 757 meters, N=333) (Figure 4.3) (see Figure
4.4 for cumulative frequency distributions of dispersal distances from parent trees versus nearest fruiting conspecific trees for Acacia collinsii, Sciadodendron excelsum, Trichilia martiana, Genipa americana and Casearia arguta.)
White-faced capuchins defecate seeds an average of 136 minutes after ingestion
(median=118 minutes, range=37 to 355 minutes, N=373) (Figure 4.5).
The average distance between two consecutive defecation events is 81 meters
(median=59 meters, range=0 to 677 meters, N=434) (Figure 4.6).
The average time between two consecutive defecations is 28.32 minutes
(median=22.5 minutes, range=12 seconds to 292 minutes, N=434) (Figure 4.7).
4.5.2 Effect of Distance and Microhabitat Variables on Seed Survival, Germination and Seedling Establishment
Of the three species for which seeds remained until the end of the study period
(Genipa americana, Casearia arguta and Sciadodendron excelsum), two were significantly affected by the distance and microhabitat variables measured here (Table
4.1). The likelihood of Genipa americana seeds/seedlings surviving until the end of the study period decreased in relation to greater canopy openness (b= -0.166, df=1, p=0.042)
(Figure 4.8), and increased in relation to the distance from the nearest fruiting conspecific
(b=0.022, df=1, p=0.002) (Figure 4.9). Similarly, the likelihood of seed survival for seeds
84 of the species Casearia arguta increased in relation to the distance from the nearest
fruiting conspecific (b=0.083, df=1, p=0.001) (Figure 4.10). None of the independent variables was a good predictor for Sciadodendron excelsum. It is important to note that seed removal from feces does not necessarily indicate seed death due to the possibility of seed deposition by a secondary disperser.
Of the four species whose seeds germinated in quadrats (Genipa americana,
Casearia arguta, Acacia collinsii and Sciadodendron excelsum) two species were significantly affected by the distance and microhabitat variables measured here (Table
4.2). Genipa americana seed germination increased in relation to the distance from the nearest fruiting conspecific tree (b=0.025, df=1, p=0.024) (Figure 4.11), and decreased in relation to the DBH of the nearest fruiting conspecific tree (b=-0.230, df=1, p=0.079)
(Figure 4.12) and canopy openness (b=-0.259, df=1, p=0.084) (Figure 4.13). Casearia arguta seed germination increased in relation to the distance from the nearest fruiting conspecific tree (b=0.140, df=1, p=0.003) (Figure 4.14).
Of the two species whose germinated seeds also established as seedlings (Genipa americana and Casearia arguta), neither were significantly affected by the distance and microhabitat variables measured here (Table 4.3).
4.5.3 Effect of Distance and Microhabitat Variables on Seedling Survival
Of the four species for which seedlings survived until the end of the study period, two were significantly affected by the distance and microhabitat variables measured here
(Table 4.4). The likelihood of Genipa americana seedlings surviving until the end of the study period increased in relation to both the distance from the parent tree (b=0.007,
85 df=1, p=0.014) (Figure 4.15) and distance to the nearest fruiting conspecific tree
(b=0.011, df=1, p=0.035) (Figure 4.16). The likelihood of Casearia arguta seedlings
surviving until the end of the study period increased in relation to the distance to the
nearest fruiting conspecific tree (b=0.040, df=1, p=0.039) (Figure 4.17).
4.5.4 Effect of Distance and Microhabitat Variables on the Duration of Defecated Seed Survival
Of the five species for which seed quadrats were established, secondary dispersal
and predation are affected by at least one of distance and microhabitat variables analyzed
here in three of the species (Table 4.5). The amount of time that Genipa americana seeds
remained in seed quadrats also increased in relation to the distance to the nearest fruiting
conspecific tree (Y=23.56 + -0.136 X, t=2.827, p=0.008). The other variables had no
significant effect (distance to parent, p=0.520; canopy cover, p=0.182; DBH of nearest fruiting conspecific, p=0.561).
The amount of time that Casearia arguta seeds remained in seed quadrats
increased as a function of distance to the nearest fruiting conspecific tree (Y=19.457 +
0.715 X, t=4.842, p=0.000). The other variables had no significant effect on seed duration
in the field (distance to parent, p=0.788; canopy cover, p=0.436; DBH of nearest fruiting
conspecific, p=0.412).
The amount of time that Acacia collinsii seeds remained in seed quadrats
increased in relation to the distance to the nearest fruiting conspecific tree (Y=14.242 +
1.065 X, t=5.072, p=0.000) as well as canopy cover (Y=14.242 + 0.457 X, t=2.311, p=0.027). The other variables had no significant effect (distance to parent, p=0.151; DBH
of nearest fruiting conspecific, p=0.903).
86 4.5.5 Effect of Distance and Microhabitat Variables on the Time to Defecated Seed Removal
The number of days that elapsed prior to the removal of all seeds from quadrats
was affected by a minimum of one of the distance and microhabitat variables in the case of each of the five species for which seed quadrats were established (Table 4.6).
The amount of time that elapsed prior to the removal of Genipa americana seeds increased as a result of the distance to the nearest fruiting conspecific tree (Y=19.763 +
0.094 X, t=1.912, p=0.071), and decreased in relation to the DBH of the nearest fruiting conspecific tree (Y=19.763 + -0.553 X, t=-2.024, p=0.057). The remaining two variables did not have a significant effect on the length of time before seeds were removed from the quadrats (distance to parent, p=0.112; canopy cover, p=0.560).
The amount of time that elapsed prior to the total removal of Casearia arguta
seeds increased as a function of the distance to the nearest fruiting conspecific tree
(Y=15.482 + 0.516 X, t=2.773, p=0.014). The remaining three variables did not have a
significant effect (distance to parent, p=0.108; canopy cover, p=0.967; DBH of nearest
fruiting conspecific, p=0.215).
The amount of time that passed prior to the removal of Acacia collinsii seeds
increased as a result of distance to the nearest fruiting conspecific tree (Y=21.040 + 1.003
X, t=4.733, p=0.000), as well as canopy cover (Y=21.040 + 0.457 X, t=2.290, p=0.028).
The remaining variables did not significantly effect the duration of seeds remaining in the
quadrats (distance to parent, p=0.213; DBH of nearest fruiting conspecific tree, p=0.777).
87 The amount of time that elapsed prior to the total removal of Trichilia martiana seeds decreased as a function of canopy cover (Y=12.276 + -0.872 X, t=-1.950, p=0.069).
None of the other variables had a significant effect on seeds remaining in the quadrats
(distance to parent, p=0.955; distance to nearest fruiting conspecific, p=0.709; DBH of nearest fruiting conspecific, p=0.604).
The amount of time that passed prior to the total removal of Sciadodendron excelsum seeds decreased in relation to the distance to nearest fruiting conspecific (Y=-
36.015 + -0.490 X, t=-10.972, p=0.000) and canopy cover (Y=-36.015 + -1.198 X, t=-
4.747, p=0.001), and increased as a function of the distance to the parent tree (Y=-36.015
+ 0.045 X, t=5.873, p=0.000), and the DBH of the nearest fruiting conspecific tree (Y=-
36.015 + 2.505 X, t=10.411, p=0.000).
4.5.6 Effect of Distance and Microhabitat Variables on the Duration of Spit Seed Survival
Of the three species (Acacia collinsii, Simarouba glauca and Karwinskia caldronii) for which spit seed quadrats were established, the duration of spit seed survival is affected by at least one of independent variables analyzed here in one species (Table
4.7).
The duration of spit seed survival for seeds of the species Acacia collinsii increased as a function of distance to the nearest fruiting conspecific tree (Y=14.242 +
1.065 X, t=5.072, p=0.000) and canopy openness (Y=14.242 + 0.457 X, t=2.311, p=0.027). The remaining two variables did not have a significant effect (distance to parent tree, p=0.151; DBH of nearest fruiting conspecific, p=0.903).
88 4.5.7 Effect of Distance and Microhabitat Variables on the Time to Spit Seed Removal
Here, as with the duration of seed survival in spit seed quadrats, the number of
days that elapsed prior to the removal of all seeds from quadrats was affected by the independent variables measured here only in the case of seeds of the species Acacia
collinsii (Table 4.8). The number of days that passed prior to total removal of spit seeds from quadrats in this species increased as a function of the distance to the nearest fruiting
conspecific tree (Y=21.040 + 1.003 X, t=4.733, p=0.000) as well as canopy cover
(Y=21.040 + 0.457 X, t=2.290, p=0.028). The remaining two variables had no significant
effect (distance to parent tree, p=0.213; DBH of nearest fruiting conspecific, p=0.777).
4.5.8 Effect of Distance and Microhabitat Variables on Seedling Growth and Damage
At least one aspect of seedling growth or damage, measured here as an increase in
seedling height, longest leaf length, number of leaves and percentage of time spent
damaged, was significantly affected by one or more microhabitat variables for each of the
five species analyzed (Table 4.9).
The dependent variable most commonly affected across all species by
microhabitat variables is longest leaf length, though each of the four dependent variables
measured here are affected in at least one species by at least three of the independent
variables measured here.
The independent variable most responsible for variation in seedling growth and
damage across all species is the distance to nearest fruiting conspecific tree. Distance to
89 nearest fruiting conspecific tree significantly affects each of the four dependent variables, across three of the five species.
4.5.9 Dispersal Patterns of Capuchin Feces: The Coefficient of Dispersion
At the level of 50x50m quadrats, capuchin feces are distributed in a clumped manner in both CP and LV groups. In CP group the coefficient of dispersion (CD) is
2.212 (mean=0.829 defecations per quadrat, median=0, sample variance=1.8343,
N=335). The CD value of LV group’s defecations is 2.387 (mean=0.282 defecations per quadrat, median=0, sample variance=0.673, N=197). The CD values, being greater than
1, indicate that capuchin feces are distributed across their home range in a clumped manner in both CP and LV groups.
4.6 Discussion
4.6.1 Dispersal Patterns and Distances
The dispersal pattern of feces is clumped when the entire home range is considered (CD=>1 for both groups), which coincides with Chapman’s (1989) calculation of primate defecation patterns in Santa Rosa National Park. This clumping together of defecations on a home-range wide scale may partially reflect the repeated use of a small number of sleep trees. During the course of this study, only 4 individual sleeping trees or small clusters of adjacent sleeping trees were observed to be utilized by
CP group, with one individual tree accounting for 74% (51 of 69) of recorded sleep tree usage. LV group was observed to use 9 different sleeping trees or clusters of adjacent sleeping trees, using one small cluster of trees in 23% (8 of 35) of observations.
Capuchins tend, in many cases, to focus activities occurring for the first few hours of
90 dawn and the last part of each day around the site where they have slept or will sleep.
This could partially account for the clumped pattern of feces dispersal.
While on a home range-wide scale, feces are distributed in a clumped manner,
they are still well dispersed on a smaller level, given that the average dispersal distance of
a seed away from its parent is 235.6 meters, and an average of 81 meters away from a previous or subsequent defecation. This apparent anomaly likely has to do with both the increased focus around sleep tree areas in the morning and evening, as well as the scale of measurement.
4.6.2 The Effect of Distance and Microhabitat Variables on Defecated Seed Survival and Germination
The independent variable that had the most consistent effect on seed survival to the end of the study as well as on seed germination was the distance to the nearest fruiting conspecific tree. Both seed survival and the likelihood of germination increased as a function of the distance of the nearest fruiting conspecific tree for two of the three species for which seeds survived to the end of the study (Genipa americana and Casearia arguta). However, while seeds of the species Sciadodendron excelsum also survived to the end of the study period and germinated, none of the independent variables measured here had any effect.
Distance to the nearest fruiting conspecific tree also consistently affected the duration of seed survival, as well as the number of days that elapsed prior to total seed removal for each of the five species analyzed here. In the case of seeds of the species
Genipa americana, Casearia arguta and Acacia collinsii, the duration of seed survival increased as a function of distance to the nearest fruiting conspecific tree. In the case of
91 seeds of the species Trichilia martiana and Sciadodendron excelsum, the number of
days that elapsed prior to total seed removal decreased as a function of distance to the nearest fruiting conspecific. While the other variables had an effect on the duration of
seed survival in the case of at least one species (canopy cover, two cases; DBH of nearest
fruiting conspecific, two cases; distance to parent; one case) these variables were not
consistently significant, and were not always consistent in the direction of their effect
(Tables 4.5 and 4.6).
The trend for at least three of the five species analyzed here is that an increase in
distance between a defecated seed and the nearest fruiting conspecific tree results in an
increase in survival and germination. Interestingly, the two species for which distance to
nearest fruiting conspecific tree does not correlate with increased survival and
germination are also the only two species in this sample that do not show increased
germination potential with capuchin gut passage (see Chapter 3), and that exhibit signs of
a bird dispersal syndrome, having small, unprotected, unhusked, brightly coloured fruits
(see Janson 1983, Link and Stevenson 2004). The remaining three species - and those for
which gut passage increases germination - exhibit signs of a mammal-dispersal syndrome
(Ibid.). This indicates that the importance of dispersal away from the parent crown may
be specific to individual trees and be related to that species’ strategy of seed dispersal.
Working in Santa Rosa National Park, Costa Rica, Hubbell (1979) found that
adult trees exhibiting different dispersal syndromes (wind, bird and bat, mammal) were
dispersed in different patterns from one another, in separate clusters along a leptokurtic
continuum. Presumably, any forces working toward or against this pattern (e.g. the need
92 for a seed of a given species to escape the crown of the parent tree in order to avoid
predation) would be reflected in the factors affecting seed survival and germination, e.g.
trees showing a clumped distribution as adults would be primarily dispersed in a more
clumped manner, or show a lower incidence of secondary predation in relation to distance
to the parent crown. This is perhaps what we are seeing here.
4.6.3 The Effect of Distance and Microhabitat Variables on Spit Seed Survival and Germination
Spit seed survival was responsive to the variables measured here only in the case
of Acacia collinsii, where, as with defecated seeds, in both measures, the duration of seed
survival increased as a function of the distance to the nearest fruiting conspecific tree.
However, since no seeds placed beneath the crown of the parent tree survived to the end
of the study period, or established as seedlings, it can be concluded that, at least for the
three species examined here, capuchins do not benefit their food trees via seed cleaning
and spitting.
4.6.4 The Effect of Distance and Microhabitat Variables on Seedling Survival and Growth
Three of the five species for which seedling survival and growth was analyzed
show increased survival and growth rates for at least one measure as an effect of distance
to the nearest fruiting conspecific tree (Casearia arguta: number of leaves, leaf length;
Trichilia martiana: height, number of leaves, leaf length; Genipa americana: leaf length,
damage; Table 4.9). In only one case (Trichilia martiana: seedling damage) is the effect
reversed. With seedlings, as with seed survival and germination, the distance to the
nearest fruiting conspecific tree accounts for most of the variation in survival and growth, and, along with DBH of nearest fruiting conspecific, is largely consistent in the direction
93 of its effect. The other independent variables measured here are not consistent in the direction of their effect. Additionally, here, as with seed survival and germination, seedlings of the species Sciadodendron excelsum are not responsive to the distance of the nearest fruiting conspecific.
4.6.5 The Effect of Distance and Microhabitat Variables Across Species and Survival and Growth Variables
Overall, across species and survival and growth variables, the distance to the nearest fruiting conspecific tree is the most consistent and frequent predictor of seed and seedling survival, germination, and growth (Table 4.10). Of the 24 dependent variables that are affected across all species by the distance to the nearest fruiting conspecific tree, only 3 show decreased benefit as a function of distance. All species in this analysis have several dependent variables that are affected by the distance to the nearest fruiting conspecific, excepting Sciadodendron excelsum, where only the number of days until total seed removal was affected by distance, and this, negatively. Sciadodendron excelsum, here as elsewhere, defies the general pattern.
Canopy cover, while affecting 11 dependent variables of four different species,
shows an inconsistent directionality of effect. 5 of the 11 affected variables show
increased benefit with increased canopy openness, while 6 show a decrease. It is
interesting to note that 4 of 5 of the cases of increased benefit with canopy openness
occur for the species Acacia collinsii, which is the only “pioneer” tree species in this
sample. Acacia collinsii is uniquely suited to occupying open niches, as it is extremely
light tolerant, and can thrive and grow in situations of little shade, growing as a
94 secondary succession tree (Janzen 1983). This species-specific tolerance likely
accounts for the overwhelmingly positive effect of canopy openness for this species.
The DBH of nearest fruiting conspecific tree shows a consistent directionality of
effect, with 5 of 6 of significant effects across three species showing decreased benefit in
relation to the DBH of the nearest fruiting conspecific across 3 species. The single case of
an increased benefit occurs for seeds of the species Sciadodendron excelsum. Here, as
elsewhere, this species is the exception.
Distance to the parent tree has, overall, less of an effect than distance to the
nearest fruiting conspecific tree and canopy cover. Additionally, this variable does not
consistently affect the dependent variables measured here. 6 of the 10 affected variables are positively affected as a result of distance to the parent tree, while the remaining 4 are negatively affected. 3 of the 4 cases for which distance to parent has a negative effect
occur within the species Trichilia martiana, and all four are seedling growth variables.
Otherwise, distance to parent tree has little consistent effect on seed growth or seed and
seedling survival and growth.
4.6.6 Evaluating the Janzen-Connell Model and the Seed Escape Hypothesis
The pattern in the data does not support the Janzen-Connell model of distant-
dependent seed mortality, which holds that the dispersal of seeds away from the parent
crown will result in an increased likelihood of germination and survival due to the
avoidance of seed and seedling predators attracted to the parent crown. However, the
pattern does support a variation of the Janzen-Connell model, namely, that seeds that are
dispersed a greater distance from any individual tree of the same species increase the
95 likelihood of survival and germination, and that seedlings that establish there have a
higher likelihood of surviving. This is a logical outgrowth of the Janzen-Connell model:
If the distance from the parent tree is the crucial variable in seed survival and seedling
growth due to the resultant proximity of host-specific predators, and is indeed the basis of
the dispersal strategy, then proximity to any other individual tree of that species should
be equally crucial to seed and seedling survival as they will also harbor at least some of
the same host-specific predators as the parent.
Additional support for a revised version of the Janzen-Connel model comes from
the effect of the DBH of nearest fruiting conspecific trees on seed survival and germination and seedling growth. DBH is a measure of fruit production (Chapman et al.
1994), and DBH of the nearest fruiting conspecific tree consistently negatively affects
seed survival and germination, as well as seedling growth. A larger fruit crop would
likely be coincident with a higher local density of species-specific seed and seedling
predators, and thus, within this model, result in higher rates of secondary predation. That
is the trend in this data, and occurs alongside the aforementioned effect of distance to the
nearest fruiting conspecific tree, lending further credence to a revised version of the seed
escape hypothesis.
If deposition away from fruiting conspecifics increases the success of an escaping
seed of mammal-dispersed species, then it follows that studies of seed dispersal should
take account not only of the straight-line distance that a seed travels from a parent, but
also the deposition location in terms of the nearest fruiting adult of that species, as well as
the fruit production of that individual tree.
96 4.7 Conclusion
White-faced capuchins, while dispersing seeds large distances from parent trees and each other, disperse seeds in a clumped manner over the expanse of their home range. Seeds are dispersed to locations where they survive, germinate, establish as seedlings and grow. The most consistent predictor of seed and seedling survival, germination and growth is the distance they are deposited from the nearest fruiting tree of their own species. They are also consistently affected by the size of that tree. This supports a variation of the Janzen-Connell seed escape hypothesis, indicating that seeds are secondarily dispersed and seedlings damaged and killed at higher rates when in proximity to a fruiting adult of their own species, whether or not that adult is the parent tree.
Future studies of seed dispersal should take account of the location of dispersed seeds vis-à-vis fruiting conspecifics. Mapping the locations of trees of a given species would also allow for a direct test of the environmental homogeneity model, as it would be possible to measure the likelihood of a seed being dispersed towards or away from a nearest fruiting conspecific, here, the most important predictor of seed and seedling survival, germination and growth across species.
97 Tables
Table 4.1. The effect of distance and microhabitat variables on seed survival until the end of the study period. Species % Cases Variable Wald chi- Df Coeffic Odds S.E. P N Correctly square ient Ratio Classified (B) (Exp(B)) GA 75% Distance NFC 9.698 1 0.022 1.022 0.007 0.002 40 Canopy Cover 4.153 1 -0.166 0.847 0.082 0.042 DBH of NFC 0.282 Distance Parent 0.812 CA 82.5% Distance NFC 10.904 1 0.083 1.087 0.025 0.001 40 Canopy Cover 0.738 DBH of NFC 0.572 Distance Parent 0.940 SE 100% Distance NFC 1 0.993 40 Canopy Cover 0.978 DBH of NFC 0.979 Distance Parent 0.980
Table 4.2. The effect of distance and microhabitat variables on seed germination. Species % Cases Variable Wald chi- df Coeffic Odds S.E. P N Correctly square ient Ratio Classified (B) (Exp(B)) GA 83.9% Distance NFC 0.024 1 0.025 1.026 0.011 0.024 31 Canopy Cover 2.991 -0.259 0.772 0.150 0.084 DBH of NFC 3.081 -0.230 0.794 0.131 0.079 Distance Parent 0.558 CA 79.5% Distance NFC 8.991 1 0.140 1.150 0.047 0.003 39 Canopy Cover 0.276 DBH of NFC 0.256 Distance Parent 0.704 SE 91.7% Distance NFC 1 0.982 12 Canopy Cover 0.982 DBH of NFC 0.982 Distance Parent 0.982 AC 60% Distance NFC 1 0.985 5 Canopy Cover 0.122 DBH of NFC 0.197 Distance Parent 0.084
98 Table 4.3. The effect of distance and microhabitat variables on seedling establishment. Species % Cases Correctly Variable d.f. P N Classified GA 100% Distance NFC 1 0.901 22 Canopy Cover 0.898 DBH of NFC 0.903 Distance Parent 0.896 CA 74.1% Distance NFC 1 0.627 27 Canopy Cover 0.744 DBH of NFC 0.880 Distance Parent 0.703
Table 4.4. The effect of distance and microhabitat variables on seedling survival. Species % Cases Variable Wald d.f. Coeffi Odds S.E. P N Correctly chi- cient Ratio Classified square (B) (Exp(B)) GA 82.9% Distance NFC 4.431 1 0.011 1.011 0.005 0.035 70 Canopy Cover 0.959 DBH of NFC 0.929 Distance Parent 6.020 0.007 1.007 0.003 0.014 CA 70% Distance NFC 4.264 1 0.040 1.041 0.019 0.039 40 Canopy Cover 0.432 DBH of NFC 0.725 Distance Parent 0.809 TM 88% Distance NFC 1 0.256 25 Canopy Cover 0.194 DBH of NFC 0.179 Distance Parent 0.172 AC 70% Distance NFC 1 0.451 40 Canopy Cover 0.396 DBH of NFC 0.314 Distance Parent 0.318
99 Table 4.5. The effect of distance and microhabitat variables on the number of days seeds remain in quadrats. Spp. Y R F d.f. Variable Coeffic t P N Intercept ient (B) (B) GA 23.56 0.456 7.990 29 Distance NFC 0.136 2.827 0.008 30 Canopy Cover 0.182 DBH of NFC 0.561 Distance Parent 0.520 CA 19.457 0.623 23.450 37 Distance NFC 0.715 4.842 0.000 38 Canopy Cover 0.436 DBH of NFC 0.412 Distance Parent 0.788 AC 14.242 0.660 14.281 37 Distance NFC 1.065 5.072 0.000 39 Canopy Cover 0.457 2.311 0.027 DBH of NFC 0.151 Distance Parent 0.903
Table 4.6. The effect of distance and microhabitat variables on the number of days that elapse prior to the removal of all seeds from quadrats. Spp. Y R F d.f. Variable Coeffic T P N Intercept ient (B) (B) GA 19.763 0.639 6.570 19 Distance NFC 0.094 1.912 0.071 21 Canopy Cover 0.560 DBH of NFC -0.553 -2.024 0.057 Distance Parent 0.112 CA 15.482 0.570 7.692 16 Distance NFC 0.516 2.773 0.014 17 Canopy Cover 0.967 DBH of NFC 0.215 Distance Parent 0.108 AC 21.040 0.637 12.656 37 Distance NFC 1.003 4.733 0.000 39 Canopy Cover 0.457 2.290 0.028 DBH of NFC 0.777 Distance Parent 0.213 TM 12.276 0.438 3.802 16 Canopy Cover -0.872 -1.950 0.069 17 DBH of NFC 0.604 Distance Parent 0.955 Distance NFC 0.709 SE -36.015 0.982 68.721 10 Distance NFC -0.490 -10.972 0.000 14 Canopy Cover -1.198 -4.747 0.001 DBH of NFC 2.505 10.411 0.000 Distance Parent 0.045 10.411 0.000
100 Table 4.7. The effect of distance and microhabitat variables on the number of days seeds remain in spit seed quadrats. Spp. Y R F d.f. Variable Coeffic t P N Intercept ient (B) (B) AC 14.242 0.660 14.281 37 Distance NFC 1.065 5.072 0.000 39 Canopy Cover 0.457 2.311 0.027 DBH of NFC 0.903 Distance Parent 0.151 SG 17 Distance NFC 0.537 17 Canopy Cover 0.198 DBH of NFC 0.775 Distance Parent 0.537 KC 19 Distance NFC 0.470 19 Canopy Cover 0.469 DBH of NFC 0.191 Distance Parent 0.470
Table 4.8. The effect of distance and microhabitat variables on the number of days that elapse prior to total seed removal from spit seed quadrats. Spp. Y R F d.f. Variable Coeffic t P N Intercept ient (B) (B) AC 21.040 0.637 12.656 37 Distance NFC 1.003 4.733 0.000 39 Canopy Cover 0.457 2.290 0.028 DBH of NFC 0.777 Distance Parent 0.213 SG 17 Distance NFC 0.571 17 Canopy Cover 0.158 DBH of NFC 0.982 Distance Parent 0.571 KC 19 Distance NFC 0.503 19 Canopy Cover 0.478 DBH of NFC 0.183 Distance Parent 0.503
101
Table 4.9. Effects of distance and microhabitat variables on seedling growth and damage. Spp. Dependent Independent Y Intercept Coefficient R F T df P N Variable Variable (B) (B) CA # Leaves Distance NFC 9.461 1.734 0.445 9.360 3.059 38 0.004 39 CA Leaf Length Distance NFC 63.617 2.124 0.276 3.129 1.769 38 0.085 39 SE Height Canopy Cover 59.806 -1.976 0.423 7.202 -2.684 33 0.011 34 SE Leaf Length Canopy Cover 63.127 -3.524 0.432 3.675 -2.563 32 0.015 34 Distance Parent 0.133 2.594 0.014 AC Height DBH of NFC 17.626 -6.791 0.401 3.548 -1.759 37 0.039 39 Distance Parent 0.120 2.653 AC Damage Distance Parent 76.012 -0.049 0.345 5.125 -2.264 38 0.029 39 TM Height Distance NFC 692.101 1.869 0.609 4.129 3.090 21 0.006 24 Distance Parent -1.124 -3.351 0.003 DBH of NFC -51.735 -3.163 0.005 TM Leaf Length Distance NFC 2311.320 6.598 0.409 1.408 2.035 21 0.055 24 Distance Parent -3.688 -2.050 0.053 DBH of NFC -174.29 -1.988 0.060 TM # Leaves Distance NFC 196.822 0.621 0.610 6.503 2.120 22 0.046 24 Distance Parent -0.678 -3.510 0.002 TM Damage Distance NFC 55.097 -0.180 0.410 4.647 -2.156 23 0.042 24 GA Height Distance Parent 44.856 0.057 0.215 3.305 1.818 68 0.073 69 GA Leaf Length Distance NFC -18.770 0.459 0.471 9.566 3.599 67 0.001 69 Canopy Cover 3.524 2.271 0.026 GA # Leaves Distance Parent 120.476 0.247 0.351 9.530 3.087 68 0.003 69 GA Damage Distance NFC 48.447 0.079 0.332 4.140 1.948 67 0.020 69 Canopy Cover -1.094 -2.229 0.029
102 Table 4.10. The effect of distance and microhabitat variables on seed and seedling survival, germination, and growth. Independent Direction of Dependent Variable Spp. P Variable Effect Distance to + Seed survival to end of study GA 0.002 NFC + Seed survival to end of study CA 0.001 + Seed germination GA 0.024 + Seed germination CA 0.003 + Seedling survival to end of study GA 0.035 + Seedling survival to end of study CA 0.039 + Duration of seed survival GA 0.008 + Duration of seed survival CA 0.000 + Duration of seed survival AC 0.000 + # of days until total seed removal GA 0.071 + # of days until total seed removal CA 0.014 + # of days until total seed removal AC 0.028 - # of days until total seed removal TM 0.069 - # of days until total seed removal SE 0.000 + Duration of spit seed survival AC 0.000 + # of days until total spit seed removal AC 0.000 + Number of leaves CA 0.004 + Longest leaf length CA 0.085 + Seedling height TM 0.006 + Longest leaf length TM 0.055 + Number of leaves TM 0.046 - Seedling damage TM 0.042 + Longest leaf length GA 0.001 + Seedling damage GA 0.020 Canopy - Seed survival to end of study CA 0.001 Cover - Seed germination GA 0.084 + Duration of seed survival AC 0.027 + # of days until total seed removal AC 0.028 - # of days until total seed removal SE 0.001 + Duration of spit seed survival AC 0.027 + # of days until total spit seed removal AC 0.028 - Seedling height SE 0.011 - Longest leaf length SE 0.015 - Longest leaf length GA 0.026 + Seedling damage GA 0.029 DBH of NFC - Seed germination GA 0.047 - # of days until total seed removal GA 0.057 + # of days until total seed removal SE 0.000 - Seedling height AC 0.039 - Seedling height TM 0.005 - Longest leaf length TM 0.060 Distance to + Seedling survival to end of study GA 0.014 Parent + Number of days until total seed removal SE 0.000 + Longest leaf length SE 0.085 + Seedling height AC 0.014 - Seedling damage AC 0.029 - Seedling height TM 0.003 - Longest leaf length TM 0.053 - Number of leaves TM 0.002 + Seedling height GA 0.073 + Number of leaves GA 0.003
103 Figures
Figure 4.1. Map showing the home range of CP (dark blue area) with 50x50m grid squares superimposed. Each dot indicates a single defecation.
104 Figure 4.2. Map showing the home range of LV (dark blue area) with 50x50m grid squares superimposed. Each dot indicates a single defecation.
105 Figure 4.3. Frequency distribution of the distance seeds deposited from parent trees.
30
25
20
15
10
Number of Occurrences 5
0
0 0 0 0 0 2 60 o -340 -460 41- 1-140 1-220 1 1 1-540 1-740 1 t 81-100 0 12 161-18 2 241-26 281-30032 361-380401-42044 481-50052 561-58 601-620641-66 681-70072 Dispersal Distance from Parent in Meters
Figure 4.4. Cumulative Frequency Distributions of distance that seeds of five most commonly consumed seeds are dispersed away from parent trees vs. nearest fruiting conspecific trees, a) Acacia collinsii, b) Casearia arguta, c) Genipa americana, d) Trichilia martiana, e) Sciadodendron excelsum. a) Acacia collinsii
1.0
0.8
0.6
0.4 Cumulative Frequency Cumulative 0.2
0.0 0 100 200 300 400 500 600 Distance in Meters
Distance to Parent Distance to Nearest Fruiting Conspecific
106 b) Casearia arguta
1.0
0.8
0.6
0.4 Cumulative Frequency Cumulative
0.2
0.0 0 100 200 300 400 500 600 Distance in Meters
Distance to Parent Distance to Nearest Fruiting Conspecific
c) Genipa americana
1.0
0.8
0.6
0.4 Cumulative Frequency Cumulative
0.2
0.0 0 100 200 300 400 500 600 700 Distance in Meters
Distance to Parent Distance to Nearest Fruiting Conspecific
107 d) Trichilia martiana
1.0
0.8
0.6
0.4 Cumulative Frequency Cumulative
0.2
0.0 0 100 200 300 400 Distance in Meters
Distance to Parent Distance to Nearest Fruiting Conspecific
e) Sciadodendron excelsum
1.0
0.8
0.6
0.4 Cumulative Frequency
0.2
0.0 0 100 200 300 400 500 Distance in Meters
Distance to Parent Distance to Nearest Fruiting Conspecific
108 Figure 4.5. Frequency distribution of gut retention times.
80
70
60
50
40
30
20 Number of Defecations
10
0 20 40 60 80 100 120 140 160 180 200 220 240 260 280 300 320 Time In Minutes
Figure 4.6. Frequency distribution of distances between consecutive defecation events.
45 40 35 30 25
20 15 10 Number of Occurrences 5 0
0 0 0 0 -70 0-10 130 380 620 30-40 60 0-220 0-320 0-470 0-560 90-100 120- 150-160180-1921 240-250270-2831 340-350370- 400-410430-4446 490-500520-5355 580-590610- 640-650 Distance Between Defecations in Meters
109 Figure 4.7. Frequency distribution of time between consecutive defecation events.
120
100
80
60
40
Number of Occurences 20
0
0 0 0 0 30 -70 0-10 300 20- 40-50 60 80-90 0-130 0-170 0-240 6 3 100-110 12 140-15 1 180-19 210-22 2 250-26 270-280 290- Time Categories in Minutes
Figure 4.8. Bubble plot depicting the effect of canopy openness on seed survival to the end of the study period for Genipa americana.
Effect of Canopy Cover on Seed Survival to End of Study Period - Genipa americana
0.8
0.6
0.4
0.2 ProportionPiles Seed Survive
0.0 0 5 10 15 20 25 30 Percentage Canopy Openness
110 Figure 4.9. Bubble plot depicting the effect of distance to nearest fruiting conspecific tree on seed survival to the end of the study period for Genipa americana.
Effect of Distance to Nearest Fruiting Conspecific Tree on Seed Survival to End of Study Period - Genipa americana
1.0
0.8
0.6
0.4
Proportion Seed Piles Survive 0.2
0.0
0 50 100 150 200 250 Distance to Nearest Fruiting Conspecific Tree in Meters Figure 4.10. Bubble plot depicting the effect of distance to the nearest fruiting conspecific tree on seed survival to the end of the study period for Casearia arguta.
Effect of Distance to Nearest Fruiting Conspecific Tree on Seed Survival to End of Study Period - Casearia arguta
1.0
0.8
0.6
0.4
Proportion Seed Piles Survive Piles Seed Proportion 0.2
0.0
0 102030405060 Distance to Nearest Fruiting Conspecific Tree in Meters
111 Figure 4.11. Bubble plot depicting the effect of the distance to the nearest fruiting conspecific tree on seed germination for Genipa americana.
Effect of Distance to Nearest Fruiting Conspecific Tree on Seed Germination - Genipa americana
1.0
0.9
0.8
0.7
0.6
Proportion Seed Piles Germinate 0.5
0.4 0 50 100 150 200 250 Distance to Nearest Fruiting Conspecific Tree in Meters
Figure 4.12. Bubble plot depicting the effect of the diameter at breast height (DBH) of the nearest fruiting conspecific tree on seed germination for Genipa americana.
Effect of DBH of Nearest Fruiting Conspecific Tree on Seed Germination - Genipa americana
1.0
0.8
0.6
0.4
0.2 Proportion Seed Piles Germinate
0.0 4 6 8 10121416182022 DBH of Nearest Fruiting Conspecific Tree in Centimeters
112 Figure 4.13. Bubble plot depicting the effect of canopy openness on seed germination for Genipa americana.
Effect of Canopy Cover on Seed Germination - Genipa americana
1.0
0.8
0.6
0.4
0.2 Proportion Seed Piles Germinate
0.0 4 6 8 10121416182022 Percentage Canopy Openness
Figure 4.14. Bubble plot depicting the effect of distance to the nearest fruiting conspecific tree on seed germination for Casearia arguta.
Effect of Distance to Nearest Fruiting Conspecific Tree on Seed Germination - Casearia arguta
1.0
0.8
0.6
0.4
0.2 Proportion Seed Piles Germinate
0.0 0 10203040506070 Distance to Nearest Fruiting Conspecific Tree in Meters
113 Figure 4.15. Bubble plot depicting the effect of the distance to the parent tree on seedling survival to the end of the study period for Genipa americana.
Effect of Distance to Parent Tree on Seedling Survival - Genipa americana
0.6
0.5
0.4
0.3
0.2
0.1 Proportion Seedlings Survive
0.0
0 100 200 300 400 500 600 700 Distance to Parent Tree in Meters
Figure 4.16. Bubble plot depicting the effect of distance to the nearest fruiting conspecific tree on seedling survival to the end of the study period for Genipa americana.
Effect of Distance to Nearest Fruiting Conspecific Tree on Seedling Survival - Genipa americana
0.6
0.5
0.4
0.3
0.2 Proportion Seedlings Survive 0.1
0.0
0 50 100 150 200 250 Distance to Nearest Fruiting Conspecific Tree in Meters
114 Figure 4.17. Bubble plot depicting the effect of distance to the nearest fruiting conspecific tree on seedling survival to the end of the study period for Casearia arguta.
Effect of Distance to Nearest Fruiting Conspecific Tree on Seedling Survival to End of Study Period - Casearia arguta
0.8
0.7
0.6
0.5
0.4
0.3 Proportion Seedlings Survive 0.2
0.1 0 102030405060 Distance to Nearest Fruiting Conspecific Tree in Meters
115 Chapter Five: Conclusion
There are numerous hypotheses to explain the origin and function of seed
dispersal by animals (Chapman and Chapman 1996), as well as a number of ways in
which to measure the effectiveness of seed dispersal by animals (Schupp 1993). This
study is an attempt to address the latter in light of the former; to determine the
effectiveness of white-faced capuchin monkeys as seed dispersers and the implications of
their disperser behaviour for the ecological and evolutionary basis of seed dispersal
systems. Chapters Two and Three deal primarily with the effectiveness of white-faced
capuchins as seed dispersers, while Chapter Four addresses the ecological and
evolutionary implications of white-faced capuchin seed dispersal in light of the spatial patterns in which seeds are dispersed.
5.1 Summary of Results
In Chapter Two I address the question of the quantity of seeds dispersed by white- faced capuchin monkeys, and find that they disperse a high number and high variety of plant species intact. I compare the quantitative results of this study to those of other studies of white-faced capuchins (Chapman 1989, Wehncke et al. 2003), and discuss possible reasons for similarities and discrepancies in the results.
Additionally, I posit the adoption of a standardized set of measures for the quantity of seeds dispersed by animals in order to address the current inability to compare quantitative measures of seed dispersal across, and even within, species, for seed dispersal studies which have an individual animal species as the unit of analysis. These measures include: The percentage of fruit in the diet, the number of plant species
116 consumed, the percentage of plant species passed intact, the number of seeds and species per defecation, the number of defecations per animal per day, animal density, and the percentage of defecations containing seeds. I conclude that while white-faced capuchins disperse a large number and a high diversity of seeds intact, without standardized measures of seed dispersal quantity it is difficult to meaningfully contextualize the quantity of seed dispersal.
In Chapter Three I address qualitative measures of white-faced capuchin seed dispersal, evaluating the capuchin’s effect on seed survival, germination potential and germination latency through every step of the seed dispersal process: initial seed handling
(spitting, swallowing whole, picking and dropping, etc.), passage through the intestinal system, and deposition in feces. This is achieved through measures of the proportion of seeds handled in each of five mutually exclusive categories (swallows whole, spits out, picks and drops, chews, partially swallows/partially spits/picks and drops), as well as germination experiments which compare germination rates and germination latency in gut passed versus non-gut passed seeds, as well as seeds planted in feces versus seeds cleaned of feces and planted in soil for the five most commonly consumed and passed plant species. Additional germination experiments measuring germination were conducted on 18 additional capuchin-handled seed species.
According to the qualitative measurements described in Chapter Three, white- faced capuchins provide a benefit to some of the seed species they consume. Seed handling records show that across all species, capuchins are most likely to swallow seeds whole and pass them intact in their feces. Germination experiments indicate that across
117 all species, seeds that are ingested and passed have higher germination rates than
seeds that are cleaned of fruit and spit out, or left with fruit intact. Additionally, of the
five most commonly ingested and passed seed species, three show a significant increase
in germination rates when passed through the capuchin intestinal system, while the
remaining two species show similar rates of germination. For four of five species, gut
passage significantly decreased the time to germination.
The presence of feces, on the other hand, has a neutral effect on the germination rates of three species, and a significantly negative effect on the remaining two species.
For the three species where seeds planted in feces germinated, the time to germination significantly decreased for one, significantly increased for one, and had no significant effect on the third. Upon closer inspection of the data, it becomes apparent that the two species that are not significantly effected by intestinal passage are the two for which there is no germination in the presence of feces. These are also species that fruit in the wet season, a time when almost daily rains wash fecal matter away from deposited seeds within a short period of time after deposition. These are also species that exhibit signs of a bird dispersal syndrome. I therefore conclude that, overall, capuchins provide a benefit to most of the plant species that they disperse via seed handling, gut passage and deposition.
In Chapter Four I examine the spatial pattern of seed dispersal by capuchins and its effect on seed survival and germination, as well as seedling survival and growth in light of extant theoretical hypotheses for the evolutionary and ecological bases of seed dispersal systems. I do so through an analysis of seed and seedling survival, germination
118 and growth data for five species that were placed in various locations throughout the forest at known distances from parent trees and nearest fruiting conspecific trees. The results of the analyses indicate that, across all five species, the most important predictor of seed survival and germination, as well as seedling survival and growth, is distance from the nearest fruiting conspecific tree. My results show that the chances of seed and seedling survival, germination and growth increase as a function of increased distance to the nearest fruiting conspecific tree.
I also present data on the distance that seeds are dispersed from parent trees in
Chapter Four, as well as a coefficient of dispersion analysis, which indicates that although seeds are dispersed away from parent trees, the overall pattern of seed dispersal throughout capuchin home ranges is clumped.
The results arrived at in Chapter Four support a variation of the Janzen-Connell
seed escape hypothesis, indicating that seeds are secondarily dispersed and seedlings
damaged and killed at higher rates when in proximity to a fruiting adult of their own
species, whether or not that adult is the parent tree.
5.2 Integration of Results
White-faced capuchin monkeys, according to qualitative, quantitative and spatial
measures, are effective seed dispersers, and thereby provide benefit to the plant species
that they consume. Capuchins disperse a high number and variety of seeds intact, and disperse them in locations which are suitable for their survival, germination, and growth.
They do so with the added benefit to the plant of increased germination rates, and in some cases reduced germination latency, for ingested, gut-passed seeds. According to
119 extant definitions of effective seed dispersers (Schupp 1993) white-faced capuchins
are extremely effective.
5.3 Contributions and Future Directions
My conclusions regarding the dispersal effectiveness of white-faced capuchin
monkeys are consistent with previous studies of seed dispersal by this species (Chapman
1989, Rowell and Mitchell 1991, Wehncke et al. 2003, Smith 2004); namely, that along
several lines of inquiry white-faced capuchin monkeys are effective seed dispersers.
Quantitatively, high numbers of a wide variety of seeds are dispersed, which is consistent with other studies (Chapman 1989, Wehncke et al. 2003), though here I argue that future studies of seed dispersal that, like this one, are concerned with dispersal from
the point of view of the frugivore, should adopt standardized measures of quantity such
that it is possible to compare disperser effectiveness between species, and within species
at different times, seasons, and locations. A failure to do so will result in data that can be
used descriptively, but not comparatively.
Qualitatively, capuchin seed handling, ingestion, gut passage and deposition
provide a benefit to the plant species consumed in the form of increased likelihood of
germination and in some cases a decreased time to germination. This is consistent with
previous studies of capuchin seed handling (Rowell and Mitchell 1991), and gut passage
experiments (Chapman 1989, Wehncke 2003, Smith 2004). Interestingly, there is at least
one case where capuchins seem to be harming the seeds they ingest through ingestion and
defecation, for a species exhibiting a bird dispersal syndrome. Further research into the
effect of gut passage on other primarily bird-dispersed species consumed by capuchins
120 might shed some light on the extent of the harm or benefit offered to plants consumed by animals outside of their intended disperser guild, and possible evolutionary implications of plant traits.
Spatially, capuchins disperse seeds far away from parent trees and each other in most cases, though the home-range wide pattern of seed dispersal is clumped, a finding consistent with Chapman’s (1989) analysis of primate defecation patterns at the same site. Here, the most consistent predictor of seed and seedling survival, germination and growth is the distance that seeds are deposited from the nearest fruiting tree of their own species, a finding consistent with Howe’s (1985) work on bird dispersal of Virola surinamensis seeds. This finding is also consistent with a variation of one of the founding models of seed dispersal studies: the Janzen-Connell model, or seed escape hypothesis, which posits that seed dispersal is a strategy in which seeds dispersed away from the parent suffer lower rates of predation, because they will be deposited away from the high densities of species-specific parasites, predators and pathogens occurring in proximity to the fruiting adult. I posit that if the distance from the parent tree is the crucial variable in seed survival and seedling growth due to the resultant proximity of host-specific predators, and is indeed the basis of the dispersal strategy, then proximity to any other individual tree of that species should be equally crucial to seed and seedling survival as they will also harbor at least some of the same host-specific predators as the parent.
Additional support for a revised version of the seed escape hypothesis comes from the effect of the DBH of nearest fruiting conspecific trees on seed survival and germination and seedling growth. DBH is a measure of fruit production (Chapman et al.
121 1994), and DBH of the nearest fruiting conspecific tree consistently negatively affects seed survival and germination, as well as seedling growth in this study. Since a larger fruit crop would likely be coincident with a higher local density of species-specific seed and seedling predators, it follows that it would also result in higher rates of secondary predation. Thus, future studies of the spatial patterns and distribution of seed dispersal should try and take into account the location not only of parent trees, but of fruiting trees of the same species.
5.4 Conclusion
White-faced capuchin monkeys are effective seed dispersers. They disperse a high number and a high variety of seeds intact in locations that are suitable for survival, germination and growth. Passage through the capuchin intestinal system additionally increases germination rates and decreases germination latency in at least some of the species consumed. Given the number of seeds dispersed by white-faced capuchins, their role in the regeneration and maintenance of the forests in which they live deserves closer inspection. Understanding the nature and extent to which their “inadvertent gardening” influences these processes is critical to understanding them in their whole ecological context, as well as the potentially enormous implications that their feeding and ranging behaviour exerts on the survival, and the patterns of survival, of the ecosystems which sustain them.
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