bb408gp7470.ttx

title         |  FUNCTIONAL TRAIT MEDIATION OF PLANT-ANIMAL INTERACTIONS:
              |  EFFECTS OF DEFAUNATION ON PLANT FUNCTIONAL DIVERSITY IN A
              |                     NEOTROPICAL FOREST
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text          |                       A DISSERTATION
              |           SUBMITTED TO THE DEPARTMENT OF BIOLOGY
              |           AND THE COMMITTEE ON GRADUATE STUDIES
              |                   OF STANFORD UNIVERSITY
              | IN PARTIAL FULFILLMENT OF THE REQUIREMENTS FOR THE DEGREE OF
              |                    DOCTOR OF PHILOSOPHY
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text          |                        Erin Leigh Kurten
              |                          August 2010
              |                   © 2010 by Erin Leigh Kurten. All Rights Reserved.
              |          Re-distributed by Stanford University under license with the author.
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text          |                          This work is licensed under a Creative Commons Attribution-
              |                          Noncommercial 3.0 United States License.
              |                          http://creativecommons.org/licenses/by-nc/3.0/us/
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text          | This dissertation is online at: http://purl.stanford.edu/bb408gp7470
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text          | I certify that I have read this dissertation and that, in my opinion, it is fully adequate
              | in scope and quality as a dissertation for the degree of Doctor of Philosophy.
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text          |                                                             Rodolfo Dirzo, Primary Adviser
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text          | I certify that I have read this dissertation and that, in my opinion, it is fully adequate
              | in scope and quality as a dissertation for the degree of Doctor of Philosophy.
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text          |                                                                                 Peter Vitousek
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text          | I certify that I have read this dissertation and that, in my opinion, it is fully adequate
              | in scope and quality as a dissertation for the degree of Doctor of Philosophy.
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text          |                                                                                 David Ackerly
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text          | Approved for the Stanford University Committee on Graduate Studies.
              |                                  Patricia J. Gumport, Vice Provost Graduate Education
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text          | This signature page was generated electronically upon submission of this dissertation in
              | electronic format. An original signed hard copy of the signature page is on file in
              | University Archives.
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title         | Preface
              | Dissertation Abstract
text          |         This dissertation examines how terrestrial vertebrates, as seed dispersers, seed
              | predators and herbivores, influence plant functional trait composition in tropical forests and
              | thereby diversity. I conducted this work in the Barro Colorado National Monument (BCNM)
              | in Central Panama, where a long term mammal exclosure experiment has been ongoing, and in
              | neighboring Parque Nacional Soberanía (PNS), which together with the BCNM forms a
              | defaunation gradient driven by hunting.
              |         I first comprehensively review what is known about how the loss of vertebrates in
              | tropical forests alters plant-animal interactions, plant demography, and plant diversity.
              | Defaunation consistently lowers primary dispersal and creates a seed shadow that is more
              | dense around the parent tree and less dense at sites farther away. However, it also often
              | lowers seed predation by rodents, and as a consequence, species with rodents as seed predators
              | and dispersers often benefit from defaunation. While demographic and diversity responses
              | tend to be more mixed, a few consistent trends emerge. Community dominance tends to
              | increase in response to defaunation. Often, plants with particular functional traits or abiotic or
              | unhunted dispersal agents are favored by defaunation.
              |         I next examined how community-level functional trait composition shifts in seedling
              | communities (Chapter 2) and sapling communities (Chapter 3) which have experienced
              | exclosure from terrestrial mammals. Seedling communities in exclosures had higher median
              | seed mass than paired plots open to the mammal community, but treatments did not differ in
              | their leaf traits (leaf mass per area and laminar toughness) or wood density. In contrast to the
              | seedling community, the sapling community did show significant shifts toward higher specific
              | leaf area and lower leaf toughness in response to herbivore exclosure, primarily due to an
              | increased dominance of species with those traits, and secondarily due to differences in the
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text          | species present in each treatment type.   These data, combined with data from PNS, also
              | suggest that hunting results in community mean wood density in seedling communities, due to
              | a disproportionate number of high wood density species relying on hunted animals for their
              | seed dispersal.
              |         Finally, I investigated the seed size response to changes in mammal abundance by
              | measuring vertebrate seed predation rates in a protected and hunted forest (Chapter 4). I
              | found that in central Panama, seed mass does not correlate well with either body size of the
              | seed predator, or vertebrate seed predation rates. I suggest that rather than formulate seed
              | predation rates as a linear function of seed predator abundance, these interactions may be
              | better modeled as threshold-dependent processes.
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text          | This work suggests that terrestrial vertebrates play an underappreciated role in maintaining
              | plant diversity and that pan-tropical levels of unsustainable hunting may indirectly lead to
              | losses of plant biodiversity.
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title         | Acknowledgments
text          | My deep gratitude goes to my two advisors, Rodolfo Dirzo and David Ackerly, for giving me
              | the flexibility and support to pursue this work. Rodolfo’s generosity as a teacher and advisor,
              | and his tireless contributions to teaching, research and conservation, both at Stanford and
              | internationally, are a great inspiration to me. I am thankful to David for graciously and
              | supportively allowing me to build a network of intellectual support that allowed me to
              | successfully complete this journey. He has also been an excellent intellectual role model for
              | me, challenging me to grapple with complexity and nuance and to confront problems from
              | new perspectives.
              |         Joe Wright has been a generous and supportive mentor and collaborator throughout
              | my time at the Smithsonian Tropical Research Institute, and some of this work would not have
              | been possible without his contributions. Peter Vitousek contributed many insightful
              | suggestions throughout the course of this work as a committee member, and his service
              | activities, from facilitating collaboration among scientists in Hawaii, to the First Nations’
              | Futures Program, have also inspired me. I also thank Fio Micheli for her enthusiasm as a
              | committee member and for helping me frame my work in a broader context. Walter Carson
              | very generously permitted me to work on the long-term mammal exclosure experiment he
              | established in the Barro Colorado National Monument in Panama and shared with me his
              | long-term datasets.
              |         The communities at Stanford, Berkeley and STRI were essential in shaping my
              | graduate school experience. At Stanford, Will Cornwell, Nathan Kraft, Virginia Maztek,
              | Steve Allison, Stephen Porder, Katie Amatangelo, Jen Funk, Camila Donatti, and Mauro
              | Galetti provided helpful feedback and support throughout the various stages of my work.
              | Doug Turner was an essential help in analyzing leaf nutrients, both for chapter three, and work
              | not included in this thesis. Alex Royo, Allen Herre, Scott Magnan, Liza Comita, Mike Tobin,
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text          | Patrick Jansen, Noelle Beckman, Roland Kays, Jackie Willis, Stephan Schnitzer generously
              | shared their advice and knowledge of the field site with me, improving the feasibility and
              | execution of this work.
              |         Many thanks go to the botanists at BCI. Without their assistance, this work would not
              | have been possible. Andrés Hernández, Oldemar Valdes, David Brassfield, and Osvaldo
              | Calderón were always happy to help me identify whatever leaf, fruit, seed, or flower I
              | brought to their office. Andrés and Oldemar in particular taught me most of what I know
              | about the BCI flora.
              |         Many paid and volunteer field and lab assistants helped to make this work possible.
              | Lissie Jiménez helped immensely with the collection and processing of the thousands of
              | leaves collected for Chapter three. Ana Patricia Calderón and Rousmery Bethancourt
              | contributed many early mornings conducting mammal transect surveys. Clare Sherman was
              | such a dedicated help in the lab and fieldwork for chapter 4, that I sometimes had to remind
              | her to take a break and have some fun. Susan Rebellon helped with the pilot studies for
              | chapter four, and also with leaf sample processing at Stanford. Gaspar Bruner, Karen
              | Kapheim, Adam Roddy, and David Bethancourt, helped me recover (most of) my leaf
              | samples after they were destroyed in a freezer accident.
              |         I would also like to thank staff at Stanford and STRI who helped make the logistical
              | aspects of this work easier. The competence of Pam Hung, Oris Acevedo, Belkys Jiménez,
              | Orelis Arosemana, and Marcela Paz made them a pleasure to work with. The Falconer library
              | and copy staff, as well as Allen Smith, did their best to get me the literature I needed, despite
              | STRI’s rigorous firewall. Valerie Kiszka and Jennifer Mason helped with countless
              | administrative tasks and advice during my time as a student at Stanford.
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title         | Contents
text          | Preface                                                                         iv
              | Acknowledgements                                                                vi
              | List of tables                                                                  ix
              | List of figures                                                                 x
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text          | Introduction………………………………………………………………………...                                      1
              | 1 Contemporaneous defaunation and cascading effects on tropical forests…...…    3
              |       Introduction………………………………………………………………….                                    3
              |       Scope of Review…………………………………………………………….                                   4
              |       Methodology………………………………………………………………...                                    5
              |       Plant-animal interactions…………………………………………………....                          7
              |             Seed dispersal………………………………………………………....                             7
              |             Seed Predation…………………………………………………………                                14
              |             Herbivory & Trampling…………………………………………….…                            17
              |       Plant Demography……………………………………………………….….                                  17
              |             Recruitment……………………………………………………………                                  17
              |             Seedling survival………………………………………………………                              19
              |             Standing abundance……………………………………………….…..                            20
              |             Linking Dispersal and Seedling Recruitment…………………………                22
              |       Community Diversity….……………………………………………………                                 24
              |             Seedling density……………………………………………………….                              24
              |             Diversity………………………………………………………………                                   24
              |             Plant Functional Groups………………………………………………                           25
              |       What is defaunation? ……………………………………………………….                               27
              |       Heterogeneity Among Studies………………………………………………                             28
              |       Conclusions……………………………………………………………….…                                     29
              |       Appendix 1.1……………………………………………………………..…                                    30
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text          | 2   Reduced seed dispersal as a consequence of hunting lowers community-level
              |     wood density in a Neotropical forest ………………………………………                        35
              |       Abstract……………………………………………………………………                                        35
              |       Introduction……………………………………………………………..….                                   36
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text          |         Methods……………………………………………………………………                                                  38
              |         Results……………………………………………………………………..                                                41
              |         Discussion…………………………………………………………………                                                45
              |         Acknowledgments…………………………………………………………..                                            49
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text          | 3     Terrestrial mammalian herbivores influence the distribution of defense and
              |       nutrient traits in a Neotropical forest…………………………………………..                            51
              |         Abstract………………………..……………………………………………                                               51
              |         Introduction………………………………………………………………….                                             52
              |         Methods……………………..………………………………………………                                                54
              |         Results……………………..………………………………………………..                                              56
              |         Discussion……………..……………………………………………………                                              61
              |         Acknowledgments…………………………………………………………..                                            65
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text          | 4     Hunting does not alter seed predation rates as a function of seed size in a
              |       Neotropical forest………………………………………………………………                                           67
              |         Abstract…………………………………………………………………..…                                               67
              |         Introduction………………………………………………………………...                                            68
              |         Methods…………………………………………………………………..…                                                72
              |         Results……………………………………………………………………….                                                76
              |         Discussion………………………………………………………………..…                                              81
              |         Conclusion…………………………………………………………………...                                             86
              |         Acknowledgments…………………………………………………………..                                            86
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text          | Bibliography……………………………………………………………………….                                                   87
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title         | List of Tables
text          | 3.1    The number of species and stems for which traits were measured…………..           57
              | 3.2    R2 values for pair-wise correlations between species mean trait values ……...   57
              | 3.3    Effect of species and exclosure on variation in leaf toughness………..            61
              | 4.1    Mean fresh seed masses of study species……………………………...                          75
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title         | List of Figures
text          | 1.1  Primary seed dispersal in defaunated sites relative to non-defaunated
              |      sites……………………………………………………………………                                           9
              | 1.2 Differences in seed caching in defaunated sites relative to non-
              |      defaunated sites………………………………………………………                                     10
              | 1.3 Changes in seedling distribution as a consequence of defaunation……         13
              | 1.4 Differences in vertebrate seed predation rates as a consequence of
              |      defaunation…………………………………………………………….                                       16
              | 1.5 Differences in invertebrate seed predation rates as a consequence of
              |      defaunation…………………………………………………………….                                       17
              | 1.6 Plant recruitment responses to defaunation for seedlings and saplings..    19
              | 1.7 Seedling survival in defaunated sites relative to non-defaunated sites..   20
              | 1.8 Differences in seedling densities in defaunated sites relative to non-
              |      defaunated sites………………………………………………………..                                   22
              | 1.9 Community-level herb densities in defaunation forest comparisons
              |      and mammal exclosure experiments…………………………………..                           24
              | 1.10 Differences in species richness, dominance, and diversity for
              |      defaunation forest comparisons and mammal exclosure experiments...        26
              | 2.1 Vertebrate activity in open and exclosure plots………………………..                 41
              | 2.2 Proportion of seedlings by dispersal mode class in open and exclosure      42
              |      treatments……………………………………………………………..
              | 2.3 Proportion of seedlings by life form class in open and exclosure           42
              |      treatments……………………………………………………………..
              | 2.4 Median seed mass is significantly higher in exclosures………………               43
              | 2.5 Effects of exclosure and hunting on community median wood density.         44
              | 2.6 Associations between dispersal agents and species wood specific
              |      gravity…………………………………………………………………                                          45
              | 3.1 Changes in plot-level trait means, unweighted by species abundance...      58
              | 3.2 Abundance-weighted, plot-level trait means in open and exclosure
              |      plots……………………………………………………………………                                           59
              | 3.3 Intraspecific differences in species’ mean leaf toughness…………….            60
              | 4.1 Model of how seed predation should vary with seed mass as a
              |      function of defaunation intensity……………………………………..                         71
              | 4.2 Map of Lake Gatun study area………………………………………..                              73
              | 4.3 Animal abundances in BCI and PNS in 2008…………………………                         77
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text          | 4.4   Seed predation rates as a function of seed size………………………..            78
              | 4.5   Number of palm seed cached in BCI and PNS………………………...                 79
              | 4.6   Identity of species removing seeds……………………………………                      80
              | 4.7   Published studies examining seed predation of large-seeded palms…..   85
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title         | Introduction
text          | Tropical forests are among the most biodiverse ecosystems on the planet. Many
              | mechanisms have been proposed to explain the maintenance of that diversity,
              | including negative distance- or density- dependent mortality, niche partitioning, and
              | neutral processes.   However, little attention has been paid to the role vertebrate
              | consumers play in maintaining tropical diversity. Evidence from defaunated tropical
              | forests suggests that these animals play a critical role in diversity maintenance
              | (Chapter 1). This dissertation examines how terrestrial vertebrates, as seed dispersers,
              | seed predators and herbivores, influence plant community composition in tropical
              | forests and thereby levels of diversity. Specifically, I used plant functional traits as a
              | lens through which to observe changes in seedling and sapling communities, identify
              | which guilds of consumers were responsible for the changes, and elucidate trait-
              | mediated mechanisms for the observed change. This work suggests that terrestrial
              | vertebrates play an underappreciated role in maintaining plant diversity and that pan-
              | tropical levels of unsustainable hunting may indirectly lead to losses of plant
              | biodiversity.
              |        I first examined how community-level functional trait composition shifts in
              | seedling communities which have been protected from terrestrial mammals (Chapter
              | 2). I conducted this work in the Barro Colorado National Monument in Central
              | Panama, where a long term mammal exclosure experiment was established in 1993-
              | 94, and where terrestrial mammals are relatively abundant. I found that seedling
              | communities in exclosures did not differ in their dispersal mode or in the relative
              | abundance of free standing and climbing growth forms, as may be expected in an
              | experiment that did not manipulate primary dispersal agents. Seedling communities in
              | exclosures had higher median seed mass than paired plots open to the mammal
              | community, but treatments did not differ in their leaf traits (leaf mass per area and
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text          | laminar toughness) or wood density. These results were validated with similar data
              | from a defaunation gradient in the same region of Central Panama. One key contrast
              | to the exclosure, however, was that seedling communities in defaunated sites had a
              | higher representation of species with abiotic dispersal modes, lianas, and species with
              | lower wood densities, which is consistent with the fact that primary dispersers are
              | impacted by hunting.
              |        I next examined the sapling community in the exclosure experiment to evaluate
              | the effects of herbivores specifically, and to identify the relative contributions of
              | altered species present, abundance, and trait expression to the differences in functional
              | trait composition observed (Chapter 3). In contrast to the seedling community, the
              | sapling community did show significant shifts toward higher leaf nitrogen and lower
              | leaf toughness in response to herbivore exclosure, primarily due to an increased
              | dominance of species with those traits, and secondarily due to differences in the
              | species present in each treatment type.      Interestingly, I also found evidence that
              | intraspecific differences in leaf traits were also contributing minorly to changes in
              | community mean leaf toughness, though whether this is the result of differential
              | mortality among genotypes or microhabitats, or a plastic response to decreased
              | mammalian herbivory is unknown.
              |        Finally, I investigated the seed size response to changes in mammal abundance
              | by measuring vertebrate seed predation rates in a protected and hunted forest (Chapter
              | 4). I aimed to both test a model of how seed predation rates should vary with seed size
              | and defaunation intensity, and potentially clarify discrepancies in community level
              | seed-size responses to hunting at different sites. I found that in central Panama, seed
              | mass does not correlate well with either body size of the seed predator, or vertebrate
              | seed predation rates. In fact, I found little difference in seed predation rates between
              | the protected and hunted forests, despite large differences in key seed predators such
              | as peccaries and agoutis. I suggest that rather than formulate seed predation rates as a
              | linear function of seed predator abundance, these interactions may be better modeled
              | as threshold-dependent processes.
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title         | Chapter 1
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title         | Contemporaneous defaunation and
              | cascading effects on tropical forests
              | Erin. L. Kurten, Mauro Galetti
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title         | INTRODUCTION
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text          |          Large bodied vertebrates have been subject to human hunting for millennia. At
              | the end of the Pleistocene, a diversity of large mammals became extinct worldwide,
              | with human overhunting likely being one of the major drivers (Barnosky et al. 2004).
              | The extinction of mammoth, giant sloths, giant kangaroos, giant deer, and many more
              | megafauna in such a short time likely changed the structure and composition of their
              | associated plant communities (Zimov et al. 1995, Guimares et al. 2008, Johnson
              | 2009).
              |          The extinction of large vertebrates is not a phenomenon restricted to the past,
              | but rather continues in the present day. While scientists still debate what caused the
              | Pleistocene megafaunal extinction (Alroy 2001; de Vivo & Carmignotto 2004; Koch
              | & Barnosky 2006; Webb 2008), there is little doubt that human activities are
              | resposible for threatening the persistence of approximately 22 percent of all mammal
              | and 12 percent of all bird species in the world today (Pimm et al. 2006). Particularly
              | in tropical forests, animal populations are currently in decline due to both
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text          | unsustainable hunting and habitat fragmentation throughout Asia (Corlett 2007),
              | Africa (Fa & Brown 2009) and Latin America (Peres & Palacios 2007).
              |           Whether changes in vegetation structure and composition have occurred as a
              | result of the extinction of the megafauna or climate change in the past, the effects of
              | comtemporaneous defaunation on vegetation is measurable. In many parts of the
              | tropics, plants have lost their major seeds dispersers, seed predators, and herbivores,
              | likely altering plant demography, spatial distribution, genetic diversity and selection
              | on seed and plant defense traits within species, with cascading effects on community
              | composition and diversity.
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title         | SCOPE OF REVIEW
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text          |     Because the animals most vulnerable to defaunation, as well as their less vulnerable
              | competitors, interact with plants as seed dispersers, seed predators, seedling predators,
              | and herbivores, contemporaneous defaunation is likely to disrupt plant-vertebrate
              | interactions. Several papers have outlined in detail how species interactions and plant
              | communities are likely to change as a consequence of these disruptions (Wright 2003,
              | Dirzo et al. 2007, Muller-Landau 2007). Disruptions of seed dispersal are likely to
              | have negative effects on plant recruitment by preventing individuals from escaping
              | distance-dependent and density-dependent mortality (sensu Janzen 1970, Connell
              | 1971). Reduced seed dispersal may also prevent light-demanding species, or species
              | with other specific environmental requirements, from reaching sites favorable for
              | recruitment (Muller-Landau 2007, Brodie et al. 2009). Changes in seed predation,
              | seedling predation, and herbivory may have positive or negative effects on species
              | recruitment by altering seed and seedling survival (Wright 2003, Dirzo et al. 2007,
              | Muller-Landau 2007). Changes in seed predation and seedling predation may have
              | further indirect benefits for invertebrate seed predators and herbivores.
              |           Overall, the net effect of defaunation on plant diversity has been hypothesized
              | to be negative (Wright 2003, Muller-Landau 2007) This is both because it is thought
              | that species experiencing reduced seed dispersal will not persist if they cannot escape
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text          | distance-dependent or density-dependent mortality, and because seed predators and
              | herbivores will not suppress populations of competitively dominant species.
              |        Here we synthesize what is currently known about the indirect effects of
              | defaunation on tropical plants, in the context of hunting, forest fragmentation, and
              | animal exclosure. We divide our analysis into three sections, addressing effects on
              | plant-animal interactions, population demography, and community diversity. Our first
              | goal was to evaluate the extent to which the hypothesized changes mentioned above
              | are supported by empirical evidence. Our second goal was to focus on plant species
              | or community responses that show mixed responses to defaunation, and try to clarify
              | why such variability may exist. Our third goal was to identify areas of study which
              | have received little attention and warrant future attention.
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title         | METHODOLOGY
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text          | IDENTIFICATION   OF STUDIES     Here we summarize literature in the field as of 2009.
              | We identified studies primarily by searching literature databases for publications on
              | aspects of plant ecology with a “defaunation” or “hunting” component.                      We
              | supplemented this collection with other studies cited in that literature, as well as
              | unpublished theses of which we had knowledge.                  In total,   thirty-seven studies
              | comprise the quantitative portion of this review (Appendix 1).
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text          | STANDARDIZATION       OF RESPONSE VARIABLES              FOR    COMPARISON      Together, the
              | variation in study design, defaunation intensities compared, species studied, and
              | response variables measured introduce too much heterogeneity to conduct a formal
              | meta-analysis of responses (Hedges & Olkin 1985). Yet, we have attempted to present
              | a review which is quantitative rather than qualitative. We have done so by calculating
              | effect sizes for each response variable. The effect size estimator we use here is the
              | percent difference in the response variable reported between defaunated and non-
              | defaunated sites as follows:
              |                                                ோವ ିோಿವ
              |                                Effect size =             ∗ 100,
              |                                                 ோಿವ
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text          | where RD and RND are the magnitudes of the response variables in the defaunated and
              | non-defaunated sites, respectively. In cases where the denominator, RND, was zero, we
              | used the smallest possible non-zero value for RND (e.g. one seed, in the case of
              | absolute seed dispersal). When the minimum possible response could not be inferred
              | (e.g., a percent abundance), we conservatively estimated the effect size as 100 percent.
              | For example, where size class data were reported, sapling to seedling ratios were
              | calculated to allow for comparison of recruitment rates across studies.
              |        When studies reported response variables from multiple defaunated or non-
              | defaunated sites, the data were averaged to derive a single value for defaunated and
              | non-defaunated states. In studies of defaunation gradients, data on the abundance or
              | presence-absence of vertebrate species relevant to the study, as well as the authors’
              | categorical characterizations of the relative levels of defaunation were used to define
              | sites as “defaunated” or “non-defaunated” for purposes of comparison. In these cases,
              | sites experiencing the lowest levels of defaunation were often grouped with “no
              | defaunation” sites, while sites showing medium to high levels of defaunation
              | comprised the “defaunated” sites.
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text          | QUANTIFICATION OF DEFAUNATION INTENSITY            We attempted to compare effects as a
              | function of defaunation intensity. We restricted these analyses to Neotropical sites
              | (70% of studies) because more extensive and comparative data on vertebrate
              | communities was reported for this region. We selected twelve genera of mammalian
              | frugivores, granivores, and browsers that differ in body mass and sensitivity to
              | defaunation pressures: Tapir, Tayassu, Pecari, Odocoileus, Mazama, Ateles, Allouata,
              | Cebus, Agouti, Dasyprocta, Sciurus and Proechimys. These genera are wide-ranging
              | in the Neotropics, though the particular species may vary. Because some studies did
              | not report animal abundances or densities, but rather species presence or absence, we
              | calculated the degree of defaunation for each site as the percent of focal genera that
              | appeared to be locally extirpated in that site, though present historically.
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text          | SEED SIZE DATA     In several cases, the perturbations in plant-animal interactions as a
              | consequence of defaunation are hypothesized to vary as a function of seed size. We
              | therefore attempted to rank species by seed size in order to present the data in a way
              | that would address these hypotheses. In most cases, either seed mass or seed length
              | was reported.     In the case of Celtis durandii, one Astrocaryum species and one
              | unspecified Dipteryx species for which seed sizes were not reported, an approximate
              | seed size was estimated by assigning that species the value of a congeneric species
              | from another site. Species for which both length and mass were reported were used to
              | approximate a relative size rank for the species for which only mass or length were
              | reported.   Alternatively, we could have used published seed mass-seed length
              | correlations to estimate missing size parameters and used one measure of seed size to
              | assign size ranks. However, this would generally change the positions of only a few
              | species with unusual seed mass-to-seed length proportions (e.g. Gustavia superba),
              | and we felt that those species were better assigned a rank by considering the size
              | parameters in the context of the plant-animal interaction and the natural history of that
              | species.
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title         | PLANT-ANIMAL INTERACTIONS
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              | 
title         | Seed dispersal
text          | Seed dispersal is thought to promote plant recruitment in tropical forests by facilitating
              | escape from natural enemies (Janzen 1970, Connell 1971) and by helping species with
              | particular environmental requirements for germination and survival (e.g. light-
              | demanding species) reach favorable microhabitats (Muller-Landau 2007).              Seed
              | dispersal establishes the spatial distribution and diversity of species in the seed and
              | seedling banks.
              |        A single seed can be dispersed multiple times by different agents. Here we
              | refer to primary seed dispersal as physical removal from the parent tree and deposition
              | on the ground. Primary seed dispersal can be performed by biotic agents such as
              | primates, bats, and birds, or by abiotic agents such as wind. Once a seed has dispersed
              | from the parent tree, it may still disperse further. This we refer to here as secondary
meta          | 8              CHAPTER 1: CASCADING EFFECTS OF DEFAUNATION ON TROPICAL PLANTS
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              | 
              | 
text          | dispersal. We focus on secondary dispersal by biotic agents such as rodents, though in
              | some circumstances, water and gravity may also facilitate dispersal on the ground.
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              | 
text          | PRIMARY    SEED DISPERSAL         Seed dispersal by biotic agents should decrease as
              | defaunation intensity increases and the abundance of seed dispersers is reduced. This
              | should affect large-seeded species to a disproportionate degree for two reasons. First,
              | their predominate dispersal agents tend to be larger-bodied, and therefore more
              | vulnerable to defaunation (Peres & van Roosmalen 2002, Holbrook & Loiselle 2009).
              | There also appears to be less redundancy of seed dispersal agents for large-seeded
              | species, relative to smaller-seeded species (Peres & van Roosmalen 2002, Nuñez-Iturri
              | et al. 2008, Donatti et al. 2009). When seed dispersal has been directly measured,
              | either as the quantity of seeds removed by primary dispersers such as birds or
              | primates, or as the proportion of seed crop removed from a parent tree, seed dispersal
              | is lower in defaunated forests in almost all cases examined (Fig. 1.1). The magnitude
              | of the decrease appears to be moderately correlated with seed size.
              |        It is important to keep in mind that tropical seed mass distributions span more
              | than seven orders of magnitude (I.J. Wright et al. 2007). The species reported here
              | represent only the very upper range of that distribution and were generally selected for
              | study because they were most likely to show dispersal declines. Almost nothing is
              | known about how hunting alters biotic dispersal across the broader range of seed sizes
              | (Muller-Landau 2007).
              |        Two studies examining how perturbations of bird communities affect the
              | dispersal of smaller-seeded species (< 1 cm fruit diameter) have shown contrasting
              | results. Dispersal of Bocageopsis multiflora in defaunated sites was actually more than
              | 2-fold higher than in non-defaunated sites (Fig. 1.1). The cause of this increase is
              | unknown, but has been suggested to result from an increase in the relative abundance
              | of generalist, frugivorous birds in highly fragmented sites (Cramer et al. 2007). In the
              | case of Celtis durandii, a decrease in avian forest specialists that was not compensated
              | for by forests generalists appears to be responsible for in an overall decrease in seed
              | dispersal (Kirika et al. 2008).
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              | 
              | 
              | 
text          |               Genus & Source
              | Large      (Community), Tonga (26)
              |            Leptonychia, Tanzania (9)
              |            Dipteryx, Costa Rica (19)
              |          Duckeodendron, Brazil (10)
              |            Carapa, Costa Rica (19)
              |               Attalea, Panama (36)
              |                 Gustavia, Panama (3)
              |           Astrocaryum, Panama (36)
              |         Antrocaryon, Cameroon (35)
              |                 Virola, Panama (3)
              |         Choerospondias, Thailand (7)
              |                 Pouteria, Brazil (2)
              |                Pourouma, Brazil (2)
              |                  Virola, Ecuador (20)
              |                  Euterpe, Brazil (14)
              |              Bocageopsis, Brazil (10)
              | Small            Celtis, Uganda (22)
              |                                          -100     -50      0       50     100    150
              |                                                  % Difference in Seeds Dispersed
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              | 
text          |         FIGURE 1.1 Seed dispersal is lower in defaunated sites relative to non-defaunated
              |         sites in almost all cases. Species are ranked by seed size, with Leptonychia being
              |         largest (11.15 cm long) and Bocageopsis and Celtis being smallest (< 1 cm long).
              |         Numbers in parentheses denote the study number in Appendix 1.
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text          | SEED CACHING A special case of seed dispersal is the caching of seeds in the ground
              | by scatter-hoarding rodents. While individual cached seeds may be predated at a later
              | time, seeds that are not subsequently recovered are afforded protection from
              | invertebrate seed predators.       For some species, such as large seeded palms with
              | specialist bruchid beetle seed predators, seed survival is heavily dependent upon seed
              | caching by rodents.
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              | 
              | 
text          |         In most cases, seed caching was higher in defaunated sites relative to non-
              | defaunated sites (Fig. 1.2). This is likely due to the fact that the rodents primarily
              | responsible for seed caching in these forests, agoutis (Dasyprocta spp.) and squirrels
              | (Sciurus spp.) may actually benefit from a reduction in the abundance of predators and
              | larger-bodied competitors at low to medium levels of defaunation (Wright 2003, Dirzo
              | et al. 2007, Peres & Palacios 2007).             Therefore, while defaunation may have a
              | negative effect on primary dispersal, this negative effect often does not extend to
              | secondary seed dispersal by terrestrial rodents.
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              | 
text          |                Genus & Source
              | Large     Carapa, Costa Rica (18)
              |             Attalea, Panama (24)
              |        Astrocaryum, Panama (24)
              |         Lechthis, Costa Rica (18)
              |     Pentaclethra, Costa Rica (18)
              |         Astrocaryum, Brazil (17)
              |         Astrocaryum, Brazil (13)
              |       Minquartia, Costa Rica (21)
              |         Hymenaea, Venezuela (4)
              |           Welfia, Costa Rica (18)
              |            Otoba, Costa Rica (18)
              |           Virola, Costa Rica (18)
              |          Clarisia, Costa Rica (11)
              | Small     Virola, Costa Rica (11)
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text          |                                         -200 -100 0      100 200 300 400                         500
              |                                               % Difference in Seeds Cached
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              | 
text          |         FIGURE 1.2 Differences in seed caching rates in defaunated sites relative to non-
              |         defaunated sites. Species are ranked by size, with Carapa being the largest (20 g) and
              |         Virola the smallest (2 g).    Absence of bar indicates no difference. Numbers in
              |         parentheses denote the study number in Appendix 1.
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              | 
              | 
text          |         Defaunation gradients in Venezuela and Brazil were exceptions to the trend of
              | higher seed caching rates in defaunated forests (Asquith et al. 1999, Galetti et al.
              | 2006). In both of these cases, the defaunated sites were small fragments in which
              | agoutis were virtually absent. Consistent with the loss of this important terrestrial
              | seed disperser, seed caching in defaunated sites was lower than in non-defaunated sites
              | in these studies (Fig. 1.2). Squirrels do not compensate for the loss of agoutis (Donatti
              | et al. 2009).
              |         In contrast to primary dispersal, no relationship between seed size and
              | differences in caching rates were apparent between defaunated and non-defaunated
              | sites. This may again be due to the fact that agoutis are capable of handling large
              | seeds and fruits much larger than their relatively small gape size might suggest.
              | Therefore, in the Neotropics secondary dispersal of larger-seeded species may occur
              | despite some degree of defaunation, provided that agoutis persist in the site.
              |         Smaller-bodied scatter-hoarding rodents, such as squirrels, exist in Africa and
              | Asia, however to our knowledge, there is no functional equivalent to the agouti in
              | Paleotropical forests.    The larger Paleotropical rodents that do exist, such as
              | Cricetomys species, are larder-hoarding rodents that tend to take seeds to burrows
              | where they will not survive (Guedje et al. 2003).        Therefore, the seed dispersal
              | “buffer” that agoutis provide in the Neotropics is less likely to be present in other
              | systems.
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              | 
text          | SPATIAL    DISTRIBUTION OF SEEDS AND SEEDLINGS        The spatial distribution of seeds
              | and seedlings on the forest floor can also be an indicator of changes in seed dispersal.
              | In particular, if seed dispersal is lower in defaunated forests, one would expect to find
              | a greater proportion of seeds or seedlings undispersed under parent trees relative to
              | what is observed in non-defaunated forests. Likewise, one would expect to see fewer
              | seeds or seedlings at distances away from parent trees relative to non-defaunated
              | forests. Indeed for many species, seed or seedling numbers under parent trees were 2-
              | to 12-fold higher in defaunated sites relative to non-defaunated sites, and were lower
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              | 
              | 
text          | away from parent trees (Fig. 1.3). These patterns are consistent with the loss of biotic
              | dispersal agents.
              |        One notable exception is Hymenaea on land-bridge islands in Venezuela.
              | Hymenaea shows the highest increases in seed pods remaining under parent trees in
              | sites without agoutis relative to sites with agoutis. However, it is one of the few cases
              | in which seedling densities are actually lower under parent trees in defaunated forests
              | (Fig.1.3).   This is not due to distance or density dependent mortality effects as
              | mediated by specialist invertebrates or pathogens (Janzen 1970, Connell 1971).
              | Rather, Hymenaea relies on agoutis to open its seed pods so that seeds may germinate.
              | In sites lacking agoutis, the seeds cannot escape the seed pod, and seedling densities
              | are correspondingly low (Asquith et al. 1999).
              |        One study estimated changes in dispersal distances with defaunation. Cramer
              | et al. (2007) reported a 60 percent and 80 percent decrease in mean and maximum
              | dispersal distances respectively for the large-seeded Duckeodendron cestroides in
              | defaunated fragments, relative to continuous forest. In the same study, the smaller-
              | seeded Bocageopsis multiflora mean and maximum dispersal distances were not
              | significantly different. This suggests that large-seeded species may become more
              | spatially aggregated in defaunated forests.      Those plant species requiring special
              | microhabitats for germination and recruitment (e.g. light gaps) may have greater
              | difficultly reaching suitable sites. Meanwhile, smaller seeded species may be less
              | affected.
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              | 
text          |                   Genus & Source
              | Large Choerospondias, Thailand (7)
              |          Leptonychia, Tanzania (9)                                              Under Parent
              |              Balanites, Gabon (5)
              |              Attalea, Panama (37)
              |              Attalea, Panama (37)
              |              Attalea, Panama (36)
              |             Dysoxylum, India (31)
              |            Chisocheton, India (31)
              |         Astrocaryum, Panama (36)
              |          Hymenaea, Venezuela (5)
              |              Polyalthia, India (31)
              |          Hymenaea, Venezuela (4)
              |                Syagrus, Brazil (1)
              | Small Antrocaryon, Cameroon (35)
              |                                         -250 0       250 500 750 1000 1250 1500 2350 2600
              | Large           Attalea, Panama (37)
              |                 Attalea, Panama (37)                                             Away From
              |                 Attalea, Panama (36)                                               Parent
              |            Astrocaryum, Panama (36)
              |           Duckeodendron, Brazil (10)
              |                Dysoxylum, India (31)
              |               Chisocheton, India (31)
              |                 Polyalthia, India (31)
              | Small        Bocageopsis, Brazil (10)
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text          |       Seeds                              -100 -50 0       50 100 150 250 300 350
              |       Seedlings                            % Difference in Seed or Seedling Abundance
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text          |         FIGURE 1.3 The number or proportion of seeds or seedlings is generally higher
              |         immediate vicinity of parent trees and generally lower away from parent trees, in
              |         defaunated sites relative to non-defaunated sites. Species are ordered by seed size.
              |         Numbers in parentheses denote the study number in Appendix 1.
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              | 
              | 
text          | COMPENSATION       AMONG DISPERSAL AGENTS             An important question regarding seed
              | dispersal in tropical forests is whether a decrease in dispersal by the principle dispersal
              | agent may be compensated for by other dispersal agents. Comparisons of primate
              | diets suggest that smaller species of primates only disperse a nested subset of the plant
              | species that are dispersed by larger primates. Even when co-occurring dispersers
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              | 
              | 
text          | appear to have significant dietary overlap on the basis of species consumed, a
              | quantitative diet analysis reveals that dispersers differ in the fruit species that make up
              | the major portion of their diets (Poulsen et al. 2002).         This suggests that even
              | dispersers with diet overlap may not compensate for one another. Similarly, among
              | frugivores that feed on Virola, alternative dispersers do not shift their diet preferences
              | enough to compensate for the loss of the principle dispersers (Holbrook & Loiselle
              | 2009).
              |          Decreases in primary seed dispersal summarized here (Fig. 1.1) suggest that
              | this lack of compensation among primary dispersal agents may be fairly general, at
              | least for larger-seeded species. There are no studies that directly investigate the
              | degree to which an increase in secondary dispersal by terrestrial vertebrates (e.g. Fig
              | 1.2) may compensate for reduced dispersal by birds and primates. However, in cases
              | where species have lost their primary dispersal agent, the number of seeds and
              | seedlings remaining under adult trees in defaunated sites is often higher than in non-
              | defaunated sites (Fig. 1.3). These data provide indirect evidence that, at least in the
              | cases studied, terrestrial seed dispersers do not fully compensate for loss of principle
              | avian and primate dispersers. It is possible, however, that terrestrial dispersers are
              | partially compensating for the loss of other dispersers, and that the observed changes
              | in seed and seedling densities under and away from parents would be even more
              | extreme in the absence of terrestrial dispersal.
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title         | Seed Predation
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text          | PRE-DISPERSAL    SEED PREDATION      Beckman and Muller-Landau (2007) investigated
              | effects of defaunation on pre-dispersal seed predation for two species of contrasting
              | seed size in central Panama. They found that pre-dispersal seed predation by
              | mammals was significantly lower in the defaunated sites for the larger-seeded
              | Oneocarpus mapora. Authors did not observe mammalian pre-dispersal seed
              | predation of small-seeded Cordia bicolor. Pre-dispersal seed predation by insects
              | between sites was not significantly different for either species.
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              | 
              | 
text          | POST-DISPERSAL       SEED PREDATION   After primary dispersal, seeds may be predated
              | upon by terrestrial mammals such as rodents, peccaries, pigs and deer. The majority of
              | studies comparing seed predation rates between defaunated and non-defaunated sites
              | have performed manipulative experiments, setting out arrays of seeds and monitoring
              | the fates of those seeds. However a few studies of species with slowly decomposing
              | endocarps have looked at “standing” rates of seed predation in the field (Wright et al.
              | 2000, Wright & Duber 2001, Galetti et al. 2006). In 22 of the 31 cases, seed predation
              | rates were lower in defaunated sites, while in nine cases, seed predation rates were
              | higher (Fig. 1.4).
              |        In a conceptual model, larger-seeded species were hypothesized to experience
              | higher seed predation rates in moderately defaunated forests relative to non-
              | defaunated forests (Dirzo et al. 2007). At severe intensities of defaunation, however,
              | large-seeded species were hypothesized to experience lower seed predation rates,
              | relative to sites with moderate to no defaunation. These changes in seed predation
              | rates were posited to be in response to changes in the abundance of seed predators of
              | medium body size.
              |        Using our estimates of defaunation intensity for Neotropical sites, we
              | examined how differences in seed predation rates for different plant species varied
              | with defaunation intensity.     These empirical data do not generally support the
              | hypothesis that seed predation of larger seeds in moderately defaunated sites is higher
              | than non-defauanted sites, while being lower in highly defaunated sites. (Fig. 1.4).
              | Among the largest-seeded species studied, seed predation increased and decreased in
              | about the same number of cases across all levels of defaunation examined.
              |        The conceptual model also hypothesized that seed predation rates of smaller
              | seeded species would increase monotonically with increasing defaunation intensity, as
              | small rodents experienced release from competition and predation.              However
              | empirical data suggest that seed predation rates are generally lower for smaller-seeded
              | species in defaunated sites, regardless of defaunation intensity (Fig. 1.4).
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              | 
              | 
text          |                                                    250
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              | 
              | 
              | 
text          |                   % Difference in Seed Predation
              |                                                    200
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text          |                                                    150
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text          |                                                    100
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text          |                                                     50
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text          |                                                      0
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text          |                                                     -50
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text          |                                                    -100
              |                                                           0.0      20.0     40.0   60.0   80.0   100.0   120.0
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text          |                                                                 Defaunation Intensity in Defaunated Site
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              | 
text          |        FIGURE 1.4 Differences in seed predation rates as a function of the intensity of
              |        defaunation in the defaunated sites. Circle sizes indicate the relative seed size of the
              |        plant species.
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text          | INVERTEBRATE SEED PREDATION                                               It has been suggested that a reduction in vertebrate
              | seed predation may benefit invertebrate seed predators in two ways.                                                      First,
              | invertebrates experience a release from competition for seed resources (Muller-Landau
              | 2007). Secondly, larvae developing in seeds may experience decreased mortality due
              | to the reduction of seed predation by vertebrates (Silvius 2002).                                                Through these
              | mechanisms, defaunation may lead to higher abundances of invertebrates, and thereby
              | higher rates of invertebrate seed predation.
              |        Few studies have investigated how defaunation indirectly alters invertebrate
              | seed predation rates. Consistent with expectation, bruchid beetle seed predation of
              | palms was higher in defaunated sites for every species investigated (Fig. 1.5).
              | However, in most cases, the absolute increase in invertebrate seed predation rates only
              | partially compensated for the decreases in vertebrate seed predation (Wright et al.
              | 2000, Wright & Duber 2001, but see Galetti et al. 2006).
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              | 
              | 
text          |                   Genus & Source
              |                  Attalea, Panama (37)
              |                  Attalea, Panama (36)
              |              Astrocaryum, Brazil (17)
              |             Astrocaryum, Panama (36)
              |                    Syagrus, Brazil (1)
              |                    Syagrus, Brazil (1)
              |                                                 0        500       1000      1500
              |                                             % Difference in Invertebrate
              |                                                   Seed Predation
              |        FIGURE 1.5 Seed predation rates by invertebrates for four species of palms are
              |        higher in defaunated sites relative to non-defaunated sites. Species are ranked by
              |        size, with Attalea being the largest and Syagrus the smallest. Numbers in parentheses
              |        denote the study number in Appendix 1.
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              | 
title         | Herbivory & Trampling
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              | 
text          | Few observational studies have evaluated differences in herbivory or trampling as a
              | consequence of defaunation.         Dirzo & Miranda (1991) an absence of vertebrate
              | herbivory in Los Tuxtlas, a defaunated site. Alves-Costa (2004) categorized herbivory
              | of the palm Syagrus romanzoffiana into classes by percent damage and also found that
              | the frequency individuals experiencing little to no herbivory was 66% higher in
              | defaunated sites.
              |        Mortality by trampling has not been evaluated for live seedlings in the context
              | of defaunation, however trampling has been evaluated with seedling models.                     In
              | Bolivia, “trampling” of seedling models by vertebrates was 75 percent lower in
              | defaunated forests (Roldán and Simonetti 2001).
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              | 
title         | POPULATION DEMOGRAPHY
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              | 
text          | RECRUITMENT         Reduced seed dispersal in defaunated forests has been hypothesized
              | to have negative impacts on plant recruitment by preventing individuals from escaping
              | distance-dependent     and density dependent             mortality (Muller-Landau 2007).
              | Empirically, plant recruitment has been reported either in terms of new seedlings
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              | 
              | 
text          | entering the population in a determined length of time, or as the ratio of juvenile plants
              | to seedlings. Authors could define seedlings variously as first year germinants or by
              | size class. In about half of cases, recruitment was about 2-fold higher in defaunated
              | forests than in non-defaunated forests, both for seedlings and saplings (Fig. 1.6). In
              | the other half of cases, recruitment is lower in defaunated forests.
              |        There have been virtually no investigations into why recruitment rates change.
              | The variation in changes in recruitment do not seem to be consistently related to the
              | degree of defaunation across studies, loss of particular dispersers or loss of particular
              | seed predators. Changes in vertebrate seedling predation and herbivory, as well as
              | distance and density dependent mortality as mediated by invertebrate herbivores and
              | pathogens (Janzen 1970, Connell 1971), can be responsible for altered seedling
              | recruitment. However, no studies have recorded herbivory rates or causes of plant
              | mortality, so no definitive data exists on how each of these mechanisms contribute to
              | the changes in recruitment observed. One study of Syagrus found that sapling
              | recruitment near the parent tree was slightly lower in defaunated forests, while
              | recruitment far from the parent tree was more than 2-fold higher in defaunated forests
              | (Alves-Costa 2004). This may be because non-vertebrate natural enemies are more
              | than compensating for the loss of vertebrate herbivores near the parent trees, but not at
              | far distances, for this species. However, no data exist with which to evaluate this
              | explanation.
              |        It is also possible, in some cases, that differences in recruitment are not
              | actually due to defaunation.     In some studies of seedling recruitment, only one
              | defaunated site and one non-defaunated site were compared.              This opens the
              | possibility that some differences in recruitment were due to other environmental
              | factors that vary across the landscape, such as precipitation or edaphic conditions. The
              | driver of defaunation is another potential source of variation. In some cases, hunting
              | was the cause of defaunation, altering primarily the animal community. However in
              | other studies fragmentation or a combination of fragmentation and hunting was the
              | cause of defaunation. As fragmentation alters many aspects of the microclimate, it is
              | possible that changes in seedling recruitment are due to the effects of fragmentation on
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              | 
              | 
text          | microclimate, rather than or in addition to the effects of a reduction in herbivore
              | abundance.
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              | 
text          |                 Genus & Source
              |                Attalea, Panama (36)                                     Seedlings
              |          Dipteryx, Peru/Panama (34)
              |            Astrocaryum, Brazil (17)
              |           Astrocaryum, Panama (36)
              |                  Syagrus, Brazil (1)
              |                                                                          Saplings
              |          (Community), Malaysia (31)
              |            Leptonychia, Tanzania (9)
              |                 Balanites, Gabon (5)
              |             Astrocaryum, Brazil (17)
              |            Syagrus (near), Brazil (1)
              |              Syagrus (far), Brazil (1)
              |                                        -100    0 100 200 300 400 500
              |                                               % Difference in Recruitment
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              | 
text          |        FIGURE 1.6 Plant recruitment does not respond consistently to defaunation across
              |        species for either seedlings or saplings. Numbers in parentheses denote the study
              |        number in Appendix 1.
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              | 
text          | SEEDLING SURVIVAL As with recruitment, responses of seedling survival to
              | defaunation are quite variable (Fig. 1.7). Asquith et al. (1997) found that differences
              | in seedling survival could vary among species within the same study system. Survival
              | was lowest on highly defaunated islands in Lake Gatun, Panama for two of the three
              | species tested. Exclosure experiments verified that spiny rats, free of competition
              | from larger mammals, reach population sizes 10-fold greater on these islands relative
              | to the non-that sites (Adler 1996), and are responsible for the increased mortality. The
              | third species, which did not show a difference in survival between sites, Virola
              | surinamensis, experienced 100% mortality at both defaunated and non-defaunated
              | sites (Asquith et al. 1997).
              |        Differences in survival rates can also be variable within a species in the same
              | region, likely due to differences in the defaunation intensities being compared. Two
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              | 
              | 
text          | studies have compared the survival of Gustavia superba in defaunated sites in the
              | Lake Gatun region of central Panama. In one case, the defaunated site was hunted
              | relative to the non-defaunated site, but the animal community was not so impoverished
              | as to lead to a competitive release of small rodents. In that study, G. superba had
              | higher survival rates in the defaunated sites. However, when the defaunated sites were
              | islands with only high populations of spiny rats present, survival of G. superba was
              | lower in the defaunated site. This difference in the degree of defaunation intensity
              | evaluated in the two studies, and compensatory changes in abundance of non-hunted
              | species, are likely to account for the contrasting responses in seedling survival, and
              | illustrate that changes in seedling survival as a consequence of defaunation may not
              | change monotonically.
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              | 
text          |              Genus & Source
              |             Dipteryx, Panama (3)
              |             Gustavia, Panama (3)
              |       Dipteryx, Peru/Panama (33)
              |                Syagrus, Brazil (1)
              |                Virola, Panama (3)
              |            Gustavia, Panama (32)
              |      Pentaclethra, Costa Rica (18)
              |                                     -75    -50     -25    0     25     50     75    100 125
              |                                                  % Difference in Seedling Survival
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              | 
text          |          FIGURE 1.7 Seedling survival does not show consistent changes as a consequence of
              |          defaunation, even within sites (e.g. study 4) or species (e.g. Gustavia superba in
              |          Panama). Numbers in parentheses denote the study number in Appendix 1.
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              | 
text          | STANDING ABUNDANCE Seedling densities do not respond uniformly to defaunation.
              | Species that are dispersed and predated upon by scatterhoarding rodents tend to
              | increase in abundance in defaunated sites (Fig. 1.8). Likewise the increase in seedling
              | abundance of the elephant dispersed Balanites wilsoniana, despite reduced seed
              | dispersal, was attributed to low seed and seedling predation in the defaunated site
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              | 
              | 
text          | (Babweteera et al. 2007). Meanwhile, species that are bird dispersed have lower
              | abundances in non-defaunated sites.
              |        These data suggest, for species which are rodent dispersed and predated, any
              | increases in distance-dependent or density-dependent mortality by invertebrates or
              | pathogens, as a consequence of reduced dispersal, do not compensate for reductions in
              | vertebrate seed and seedling predation, resulting in a net increase in survival for these
              | species. The same does not appear to be true for bird dispersed species, although there
              | is no theoretical reason why these species should not experience high reductions in
              | vertebrate seed predation.
              |        All studies involving rodent dispersed species were conducted on palm species,
              | most of which are preferred food species for agoutis, a dominant Neotropical seed
              | predator. More studies in Neotropical forests are required to determine if these
              | species are unique in experiencing a net benefit from defaunation, or if other species
              | preyed upon by agoutis also increase in abundance in defaunated sites. These studies
              | should include species that have birds or primates as their primary dispersal agents.
              |        In contrast to the rodent-dispersed palms, little is known about the seed
              | predators of the bird-dispersed species studied. However, at least two of the three
              | studies of bird-dispersed species were conducted in Paleotropical forests with different
              | assemblages of seed predators. Studies of vertebrate seed and seedling predation in
              | the Paleotropics may determine whether differences observed between rodent-
              | dispersed species and bird-dispersed species may be due to differences in the seed and
              | seedling predator community, rather than differences between species with different
              | dispersal agents per se.
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              | 
text          |             Genus & Source
              |        Astrocaryum, Brazil (17)                                 Rodent Dispersed
              |             Dipteryx, Peru (33)
              |              Syagrus, Brazil (1)
              |       Astrocaryum, Bolivia (29)
              |              Syagrus, Brazil (1)
              |            Attalea, Panama (36)
              |            Attalea, Panama (37)
              |       Astrocaryum, Panama (36)
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text          |                                                                   Bird Dispersed
              |          Chisocheton, India (31)
              |            Polyalthia, India (31)
              |           Dysoxylum, India (31)
              |             Euterpe, Brazil (14)
              |        Leptonychia, Tanzania (9)
              |                                 -100          0         100        200     300
              |                                                               Elephant Dispersed
              |             Balanites, Gabon (5)
              |                                  -400       0        400        800      1200
              |                                          % Difference in Seedling Densities
              |        FIGURE 1.8 Differences in seedling densities in defaunated sites relative to non-
              |        defaunated sites. Numbers in parentheses denote the study number in Appendix 1.
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              | 
text          | LINKING   DISPERSAL AND SEEDLING RECRUITMENT              It is clear, by several measures,
              | that seed dispersal decreases as a consequence of defaunation (Figs. 1.1 & 1.3), though
              | effects on seed caching are variable (Fig. 1.2). What is less clear is whether decreased
              | dispersal translates to decreases in plant recruitment.           Investigators focusing on
              | decreased seed dispersal as a consequence of defaunation often suggest that decreased
              | dispersal will result in decreases in seed and seedling survival and plant recruitment.
              | This is because undispersed seeds are assumed to be unable to escape distance-
              | dependent and/or density-dependent mortality (Janzen 1970, Connell 1971).
              |        However, there are several problems with this assumption. First, there are
              | many species for which distance- and/or density-dependent mortality have not been
              | detected (Hyatt et al. 2003, Uriarte et al. 2005). Secondly, spatial data on seedling
              | densities also show that reduced seed dispersal does not generally lead to great
              | decreases in seedling abundances under parent trees in defaunated forests (Fig. 1.3).
              | This suggests that though seed and seedling mortality may be higher under parent
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              | 
              | 
text          | trees, the higher number of seeds that fall below the parent tree in defaunated forests
              | compensate for this higher mortality and seedling densities under parent trees remain
              | relatively similar to those observed in non-defaunated forests. Finally, as seen above,
              | vertebrate seed and seedling predation rates may also vary with defaunation (Figs. 1.4
              | & 1.5). Seedling density data suggest that reduced rates of vertebrate seed predation
              | result in increased survival rates that more than compensate for any increases in
              | distance-dependent or density-dependent mortality by non-vertebrates, at least for
              | rodent-dispersed species and species like B. wilsoniana (Fig. 1.6). Taken together,
              | these data suggest that the assumed negative effects of reduced seed dispersal on plant
              | recruitment as a consequence of hunting may not be general, but rather manifest
              | themselves only in species which (1) experience strong natural enemy-mediated,
              | negative density-dependent mortality (2) rely exclusively upon a few, large-bodied,
              | hunted vertebrates for seed dispersal, and (3) do not experience a demographic benefit
              | of reduced seed predation by rodents with increasing defaunation intensity.
              |        Interestingly, there are few studies that actually investigate changes in
              | dispersal and seedling recruitment simultaneously in a single species. In the case of
              | the large seeded palm Attalea butyracea in Central Panama, seed dispersal is reduced
              | in defaunated forests (Wright & Duber 2001). In addition, the intensity of bruchid
              | beetle seed predation does increase with proximity to the parent tree, and the effect
              | intensifies with defaunation. However, increased bruchid beetle seed predation did
              | not fully compensate for the decrease in vertebrate seed predation associated with the
              | defaunation, and seedling densities of the palm were higher in defaunated sites,
              | despite the decrease in seed dispersal.
              |        Brodie et al. (2009) modeled the effects of decreased dispersal on seedling
              | recruitment for Choerospondias axillaris in Thailand and did find evidence that
              | decreased dispersal would translate to decreased recruitment in this species. However
              | this was because defaunation deprived C. axillaris of favorable regeneration sites,
              | since C. axillaris seems to depend on light gaps for regeneration and could not
              | disperse to gaps without its vertebrate disperser (Brodie et al. 2009). It was not a
              | consequence of distance-dependent or density-dependent mortality.
meta          | 24               CHAPTER 1: CASCADING EFFECTS OF DEFAUNATION ON TROPICAL PLANTS
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              | 
              | 
title         | COMMUNITY DIVERSITY
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              | 
text          | SEEDLING    DENSITY      Seedling or herb density at the community level is consistently
              | higher where exclosure experiments (Ickes et al. 2001, Royo & Carson 2005) or
              | defaunation due to hunting and fragmentation (Dirzo & Miranda 1991) completely
              | eliminate vertebrate herbivory (Fig. 1.9).               Interestingly, at many moderately
              | defaunated sites, community seedling densities are lower, relative to non-defaunated
              | sites.   It may be that terrestrial herbivores initially increase in abundance as a
              | consequence of a release from predation, and perhaps competition.                        However,
              | decreased seedling densities at the community level are in contrast to higher seedling
              | densities of many individual species in defaunated sites (Fig. 1.8). This discrepancy
              | further highlights the need to understand how defaunation alters plant recruitment
              | across a broader range of species, and to reconcile changes in recruitment at the
              | species level with changes at the community-level.
              |                  Site & Source
              |                     Uganda (8)                                Forest comparison
              |                     Uganda (8)                                Exclosure study
              |                    Panama (38)
              |                    Bolivia (29)
              |                    Panama (30)
              |                       Peru (27)
              |                   Malaysia (21)
              |                    Panama (30)
              |                   Malaysia (21)
              |                    Mexico (12)
              |                               -100      -50      0      50     100     150
              |                                       % Difference in Seedling Density
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              | 
text          |          FIGURE 1.9 Community level seedling and herb densities generally increase in
              |          cases of high defaunation but decrease in others. Numbers in parentheses denote the
              |          study number in Appendix 1.
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              | 
text          | DIVERSITY Several short-term exclosure studies have shown that species richness
              | initially increases with herbivore removal (Fig. 1.10a). However, this appears to be an
              | effect of increased stem densities increasing the likelihood that rare species will be
              | present inside the exclosures. In an exclosure experiment in Panama, rare herbs
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              | 
              | 
text          | increased 2-fold (Royo & Carson 2005) (Fig. 1.10b). However, defaunation also
              | appears to increase species dominance as well (Fig. 1.10b). Diversity indices appear
              | to mask the changes in community composition that occur in exclosure experiments,
              | because the effects of increased species richness and increased dominance tend to
              | cancel each other out, such that exclosures show only small decreases in indices of
              | diversity.
              |         In forest comparisons, species richness was generally lower. Unlike short-term
              | exclosure experiments, defaunated forests have experienced decades of defaunation,
              | likely allowing competitively dominant plant species to outcompete rarer and less
              | dominant species, reducing diversity.       Consistent with this hypothesis, species
              | dominance was higher in the cases that reported it (Fig. 1.10b). Responses in diversity
              | indices were mixed (Fig. 1.10c), again suggesting that these indices may be less
              | informative than directly evaluating changes in species richness and dominance.
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              | 
text          | PLANT   FUNCTIONAL GROUPS        Nuñez-Iturri et al. (2007, 2008) and Wright et al.
              | (2007) both found little difference in total species richness between defaunated and
              | non-defaunated sites. However, the lack of differences in species richness belied
              | important changes in plant community composition. Species with abiotic or unhunted,
              | biotic dispersal agents consistently show higher abundance in hunted sites (Wright et
              | al. 2007, Nuñez-Iturri et al. 2008, Terborgh et al. 2008). In contrast, species dispersed
              | by game animals show decreased abundance in defaunated sites. Consistent with this
              | finding, lianas, which tend to be abiotically dispersed (Hardesty & Muller-Landau
              | 2005, Wright et al. 2007), were higher in relative abundance in defaunated sites in
              | central Panama (Wright et al. 2007).
meta          | 26                  CHAPTER 1: CASCADING EFFECTS OF DEFAUNATION ON TROPICAL PLANTS
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              | 
text          |        Site & Source                              A    Site & Source                             B
              |           Mexico (12)                                    Panama (30)
              |       (game) Peru (28)                                      Brazil (1)
              |       (game) Peru (27)                                   Panama (30)
              |             Uganda (8)                                   Panama (30)
              |               Peru (28)                                   Mexico (12)
              |             Uganda (8)                                                   100 200 500 600 700
              |                                                                          0
              |            Bolivia (29)                                          % Difference Species Dominance
              |            Bolivia (29)
              |                                                         Site & Source                            C
              |            Panama (38)
              |                                                          Mexico (12)
              |               Peru (27)
              |                                                         Malaysia (21)
              |          Malaysia (21)
              |                                                         Colombia (25)
              |            Panama (30)
              |                                                          Panama (38)
              |      (abiotic) Peru (28)
              |                                                                      -80    -40       0       40
              |  (non-game) Peru (27)                                                  % Difference in Diversity
              |        Colombia (25)
              |      (abiotic) Peru (27)
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text          |                       -75 -50 -25 0 25 50 75                                       Forest comparison
              |                       % Difference Species Richness                                Exclosure study
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text          |           FIGURE 1.10 Diversity responses to defaunation. (a) species richness, (b) species
              |           dominance, and (c) species diversity (Shannon-Weiner, Simpson, or Fisher’s α
              |           indices). Peruvian richness differences are generally for groups with different dispersal
              |           agents; dominance for the Panama study is similarly for subsets of common and rare
              |           herbs. Numbers in parentheses denote the study number in Appendix 1.
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              | 
text          |           The studies found important differences in community seed mass responses.
              | In Peru, the relative abundance of large seeded species was lower in defaunated sites,
              | while in Panama, the community mean seed mass was higher in defaunated sites
              | (Wright et al. 2007, Nuñez-Iturri et al. 2008). The discrepancy appears to be due to
              | differences in faunal communities between Peru and Panama. In the Peruvian study,
              | defaunation greatly reduces populations of large primate dispersers, while not greatly
              | affecting the relatively low populations of seed predators such as agoutis. In contrast,
              | defaunation in Panama, defaunation greatly reduces agouti populations, but does not
              | greatly affect seed dispersal by large primates, as these animals are rare or absent even
              | in the non-defaunated sites.
              |           Studies of the effects of defaunation effects on other functional traits are rare.
              | Both a forest comparison study in Panama and an exclosure study in Panama found
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              | 
              | 
text          | that community median leaf mass per area and leaf laminar toughness in the seedling
              | community did not change in response to defaunation (Ch. 2). However, saplings (40-
              | 100 cm) in the exclosure experiment did have lower community mean leaf toughness,
              | and higher community mean leaf nitrogen relative to controls (Ch. 3). Wood density
              | was the only functional trait that had different responses to defaunation in the forest
              | comparison and exclosure studies. This is likely due to the fact that primary dispersal
              | is altered in the forest comparison, but not in the exclosure study (Ch. 2).
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              | 
title         | WHAT IS DEFAUNATION?
text          | The heterogeneity in response to defaunation, particularly at the level of plant
              | population dynamics and community composition, suggest that more precision is
              | needed in characterizing exactly what is meant by defaunation, including its drivers
              | and the effects on the particular mammal community being studied. Among the
              | studies reported there, there was variation in the levels of defaunation in both “non-
              | defaunated” and “defaunated” forests across studies. In some cases, sites with similar
              | species compositions would be considered “non-defaunated” in one study, and
              | “defaunated” in another.
              |        Unfortunately, terms such as “hunted”, “fragmented,” or “disturbed” are
              | usually used to classify sites into treatments, but do not correspond to a specific
              | change in a vertebrate community. This problem could be addressed by reporting a
              | robust characterization of the vertebrate community. Often, studies did not actually
              | report differences in either abundances of key species (e.g. a particular seed disperser)
              | or the vertebrate community as a whole.      In other cases, the presence or absence of
              | species were reported, but not animal abundances. Reporting presence/absence data
              | will not capture situations in which animals such as rodents or smaller primates
              | actually increase in population size as defaunation reduces the predation and
              | competition they experience. In other cases, a species may be present, but in such rare
              | numbers so as to be functionally extinct.
              |        Though estimating animal abundances is labor-intensive, we suggest that
              | further clarity and progress in understanding the effects of defaunation on plant
meta          | 28             CHAPTER 1: CASCADING EFFECTS OF DEFAUNATION ON TROPICAL PLANTS
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              | 
              | 
text          | communities will rely on exactly this level of precision in characterizing sites used in
              | comparative studies.
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              | 
title         | HETEROGENEITY AMONG STUDIES
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              | 
text          | Understanding the heterogeneity and sources of potential bias in the studies examined
              | here is important both for understanding the limitations and generality of the data, as
              | well as identifying areas for further research. Research on effects of defaunation on
              | plants has predominantly focused on Neotropical mammals.           Over 70 percent of
              | studies were conducted in the Neotropics, while only 15 percent and 10 percent of
              | studies were conducted in Africa and Asia respectively, with the remaining 5 percent
              | conducted in Australia and Polynesia. As this review has demonstrated, responses to
              | defaunation can be quite variable even within the Neotropics, where faunal
              | communities are relatively similar. More studies in the Paleotropics are needed to
              | understand how plant responses to defaunation in these forests may differ from those
              | observed in Neotropical forests.
              |        Only 15 percent of studies reported effects of avian defaunation, with the
              | remainder examining effects of mammalian defaunation.          Many of those studies
              | focused on rodents and/or primates.       Despite the fact that many of the larger
              | vertebrates such as peccaries, pigs, deer, tapir and elephants are most vulnerable to
              | defaunation, only a few studies investigated the effects of losing these animals from
              | the community.     Future studies should seek to understand the impacts of losing
              | relatively understudied groups of vertebrates, as well as understanding how losses of
              | dispersers, seed predators, and herbivores may synergize.
              |        It is also important to note that forest comparisons generally had low
              | replication. The majority of studies only had one non-defaunated site, and sometimes
              | only one defaunated site. We suggest that a better understanding of patterns and
              | mechanisms could come from increasing the number of study sites examined, and
              | including a range of defaunation intensities within a single study, with better
              | quantification of the differences in vertebrate communities. We suspect that many of
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              | 
              | 
text          | the interactions and patterns discussed in this review do not vary linearly with animal
              | abundance, but rather, change in a step-wise or threshold dependent manner as key
              | interaction partners are removed from a system. Studying gradients of defaunation
              | intensity would allow scientists to better elucidate the levels of defaunation at which
              | changes in key interactions occur, and perhaps allow for the reconciliation of
              | discrepancies in responses among studies.
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              | 
title         | CONCLUSIONS
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              | 
text          | It is now well documented that larger-seeded species experience reduced dispersal,
              | and increased aggregation around parent trees as a result of defaunation. However the
              | overall consequences for species recruitment appear variable. More work is required
              | to link reduced dispersal to subsequent stages of the seedling recruitment process to
              | determine whether reduced dispersal poses a general threat to the persistence of large-
              | seeded species. Responses to defaunation at the community level are also variable,
              | and future studies should work to reconcile the changes observed that the species
              | interaction or population levels with changes in composition at the community level.
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              | 
              | 
text          | APPENDIX 1.1 Reference information and raw data for response variables for studies
              | referenced in figures. Ndef = value for non-defaunated site(s); Def = Value for
              | defaunated site(s); % ∆ = Percent change from non-defaunated site to defaunated site.
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              | 
text          | No   Reference                        Site        Response Variable                     Ndef   Def     %∆
              | 1    Alves-Costa (2004)               Brazil      Diaspores predated (%)                31.2   12.6    -60
              | 1    Alves-Costa (2004)               Brazil      Insect seed predation (near)          10.7   23.4    119
              | 1    Alves-Costa (2004)               Brazil      Insect seed predation (far)           1.6    24.2    1376
              | 1    Alves-Costa (2004)               Brazil      Seed density                          0.16   0.18     8
              | 1    Alves-Costa (2004)               Brazil      Seedlings under parent                0.06   0.72    1187
              | 1    Alves-Costa (2004)               Brazil      Juvenile:Seedling (near)              2.33   1.16    -50
              | 1    Alves-Costa (2004)               Brazil      Juvenile:Seedling (far)               2.65   9.51    259
              | 1    Alves-Costa (2004)               Brazil      Seedling density                      26.8   46.8     75
              | 1    Alves-Costa (2004)               Brazil      No. species/No. plants                0.23   0.14    -37
              | 1    Alves-Costa (2004)               Brazil      Frequency of low herbivory            24.1   40.0     66
              | 1    Alves-Costa (2004)               Brazil      No. new plants                        41.2   118.4   187
              | 1    Alves-Costa (2004)               Brazil      Seedling mortality (%)                40.1   42.7     6
              | 2    Andresen (2003)                  Brazil      % Pouteria seeds buried                40    32.5    -19
              | 2    Andresen (2003)                  Brazil      % Pourouma seeds buried                36     19     -47
              | 3    Asquith et al. (1997)            Panama      Seed removal                          0.01   0.05    900
              | 3    Asquith et al. (1997)            Panama      Seedling survival                     0.21   0.07    -69
              | 3    Asquith et al. (1997)            Panama      Seed removal                          0.01   0.08    700
              | 3    Asquith et al. (1997)            Panama      Seed dispersal                        0.56   0.24    -58
              | 3    Asquith et al. (1997)            Panama      Seedling survival                     0.49   0.22    -56
              | 3    Asquith et al. (1997)            Panama      Seed removal                          0.00   0.00     0
              | 3    Asquith et al. (1997)            Panama      Seed dispersal                        0.54   0.19    -65
              | 3    Asquith et al. (1997)            Panama      Seedling survival                     0.00   0.00     0
              | 4    Asquith et al. (1999)            Venezuela   Pod removal                           1.00   0.14    -86
              | 4    Asquith et al. (1999)            Venezuela   Seed removal                          0.92   0.60    -35
              | 4    Asquith et al. (1999)            Venezuela   Seed caching                          0.17   0.00    -100
              | 4    Asquith et al. (1999)            Venezuela   Seed density under parent             4.0    100.0   2400
              | 4    Asquith et al. (1999)            Venezuela   Seedling density under parent         22.0    1.8    -92
              | 5    Babweteera et al. (2007)         Gabon       Juvenile density                       85    1169    1275
              | 5    Babweteera et al. (2007)         Gabon       Sapling:Seedling                      0.21   0.00    -98
              | 5    Babweteera et al. (2007)         Gabon       Pole:Seedling                         0.08   0.01    -92
              | 5    Babweteera et al. (2007)         Gabon       Prob. Juvenile's under conspecific    58.0   89.0     53
              | 6    Beckman & Muller-Landau (2007)   Panama      Primary seed removal                  42.0   24.1    -43
              | 6    Beckman & Muller-Landau (2007)   Panama      Predispersal seed predation           55.0   25.0    -55
              | 6    Beckman & Muller-Landau (2007)   Panama      Secondary seed removal                0.0    10.6    100
              | 6    Beckman & Muller-Landau (2007)   Panama      Primary seed removal                  21.6   14.6    -32
              | 6    Beckman & Muller-Landau (2007)   Panama      Predispersal seed predation           7.0     7.0     0
              | 6    Beckman & Muller-Landau (2007)   Panama      Predispersal seed predation           20.0    0.0    -100
              | 6    Beckman & Muller-Landau (2007)   Panama      Secondary seed removal                80.0   10.8    -87
              | 7    Brodie et al. (2009)             Thailand    Proportion fruits under adults        0.19   0.68    252
              | 7    Brodie et al. (2009)             Thailand    Seeds dispersed                       0.15   0.01    -91
              | 8    Chapman & Onderdonk (1998)       Uganda      Seedling density, non-valley sites    12.5    5.5    -56
              | 8    Chapman & Onderdonk (1998)       Uganda      Seedling richness, non-valley sites   5.0     3.1    -39
              | 8    Chapman & Onderdonk (1998)       Uganda      Seedling density, valley bottom       2.5     1.3    -50
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              | 
              | 
text          | 8    Chapman & Onderdonk (1998)   Uganda       Seedling richness, valley bottom    1.3     1.0    -23
              | 9    Cordeiro and Howe (2003)     Tanzania     Seed dispersal                     12.8     3.0    -76
              |                                                Proportion indiv under adults
              | 9    Cordeiro and Howe (2003)     Tanzania     (<10 m)                            57.3    88.5    54
              | 9    Cordeiro and Howe (2003)     Tanzania     Juvenile:Seedling                   0.4     0.3    -27
              | 9    Cordeiro and Howe (2003)     Tanzania     Seedling abundance                 163.7   96.7    -41
              | 10   Cramer et al. (2007)         Brazil       Seeds dispersed                    48.0    16.0    -67
              | 10   Cramer et al. (2007)         Brazil       Seeds dispersed                     5.0    12.0    140
              | 10   Cramer et al. (2007)         Brazil       Ave. dispersal distance             7.5     3.0    -60
              | 10   Cramer et al. (2007)         Brazil       Ave. dispersal distance            23.0    18.0    -22
              | 10   Cramer et al. (2007)         Brazil       Max. dipersal distance             20.0     4.0    -80
              | 10   Cramer et al. (2007)         Brazil       Max. dipersal distance             17.0    18.0     6
              | 10   Cramer et al. (2007)         Brazil       Seeds away from parent             27.0     1.0    -96
              | 10   Cramer et al. (2007)         Brazil       Seeds away from parent              8.0     6.0    -25
              | 11   DeMattia et al. (2004)       Costa Rica   Seeds destroyed                    100.0   93.6     -6
              | 11   DeMattia et al. (2004)       Costa Rica   Seeds destroyed                    68.8    65.6     -5
              | 11   DeMattia et al. (2004)       Costa Rica   Seeds destroyed                    100.0   84.1    -16
              | 11   DeMattia et al. (2004)       Costa Rica   Seeds destroyed                    31.2    15.6    -50
              | 11   DeMattia et al. (2004)       Costa Rica   Seeds destroyed                    93.8    75.0    -20
              | 11   DeMattia et al. (2004)       Costa Rica   Seeds destroyed                    28.0    12.2    -57
              | 11   DeMattia et al. (2004)       Costa Rica   Seeds destroyed                    18.5    24.5    33
              | 11   DeMattia et al. (2004)       Costa Rica   Seeds cached                       25.0     3.1    -88
              | 11   DeMattia et al. (2004)       Costa Rica   Seeds cached                       3.07    9.22    200
              | 12   Dirzo & Miranda (1991)       Mexico       Herbivory                          0.27    0.00    -100
              | 12   Dirzo & Miranda (1991)       Mexico       Seedling density                   22.6    52.8    134
              | 12   Dirzo & Miranda (1991)       Mexico       Seedling species richness          6.65    2.30    -65
              | 12   Dirzo & Miranda (1991)       Mexico       Seedling diversity                 3.71    1.07    -71
              | 12   Dirzo & Miranda (1991)       Mexico       Seedling species dominance         14.0     2.0    -86
              | 13   Donatti et al. (2009)        Brazil       Seeds predated                     0.18    0.03    -83
              | 13   Donatti et al. (2009)        Brazil       Seeds cached                       0.33    0.13    -61
              | 14   Fadini et al. (2009)         Brazil       Seed dispersal                      1.6     0.9    -42
              | 14   Fadini et al. (2009)         Brazil       Seed predation                     99.7     7.4    -93
              | 14   Fadini et al. (2009)         Brazil       Seedling density                   1000     80     -92
              | 15   Farwig et al. (2006)         Kenya        seed removal                       0.97    1.57    62
              | 16   Fleury & Galetti (2006)      Brazil       Seed predation                     15.8    48.0    203
              | 16   Fleury & Galetti (2006)      Brazil       Seed predation                     15.8     0.0    -100
              | 17   Galetti et al. (2006)        Brazil       Seed predation (%)                  6.9     0.3    -96
              | 17   Galetti et al. (2006)        Brazil       Seed caching (%)                   12.2     3.4    -72
              | 17   Galetti et al. (2006)        Brazil       Seed predation (%)                 38.4     2.0    -95
              | 17   Galetti et al. (2006)        Brazil       Seed predation (%)                 34.4    69.6    102
              | 17   Galetti et al. (2006)        Brazil       Seedling density                   148.2   34.5    -77
              | 17   Galetti et al. (2006)        Brazil       Seedling:Adult                     6.96    0.35    -95
              | 17   Galetti et al. (2006)        Brazil       Sapling:Seedling                   1.98    10.07   409
              | 18   Guariguata et al. (2000)     Costa Rica   Secondary seed removal             0.41    0.13    -67
              | 18   Guariguata et al. (2000)     Costa Rica   Secondary seed removal             0.31    0.37    20
              | 18   Guariguata et al. (2000)     Costa Rica   Secondary seed removal             0.88    0.94     7
              | 18   Guariguata et al. (2000)     Costa Rica   Secondary seed removal             0.59    0.91    56
              | 18   Guariguata et al. (2000)     Costa Rica   Secondary seed removal             0.66    0.88    33
              | 18   Guariguata et al. (2000)     Costa Rica   Secondary seed removal             0.87    0.38    -56
              | 18   Guariguata et al. (2000)     Costa Rica   Secondary seed removal             0.98    0.40    -59
meta          | 32                  CHAPTER 1: CASCADING EFFECTS OF DEFAUNATION ON TROPICAL PLANTS
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              | 
              | 
text          | 18   Guariguata et al. (2000)     Costa Rica   Secondary seed predation          0.41    0.13    -67
              | 18   Guariguata et al. (2000)     Costa Rica   Secondary seed predation          0.31    0.37    20
              | 18   Guariguata et al. (2000)     Costa Rica   Secondary seed predation          0.77    0.91    18
              | 18   Guariguata et al. (2000)     Costa Rica   Secondary seed predation          0.55    0.91    64
              | 18   Guariguata et al. (2000)     Costa Rica   Secondary seed predation          0.57    0.78    38
              | 18   Guariguata et al. (2000)     Costa Rica   Secondary seed predation          0.73    0.38    -48
              | 18   Guariguata et al. (2000)     Costa Rica   Secondary seed predation          0.95    0.40    -58
              | 18   Guariguata et al. (2000)     Costa Rica   Seed caching                      0.00    0.00    0
              | 18   Guariguata et al. (2000)     Costa Rica   Seed caching                      0.00    0.00    0
              | 18   Guariguata et al. (2000)     Costa Rica   Seed caching                      0.03    0.11    300
              | 18   Guariguata et al. (2000)     Costa Rica   Seed caching                      0.01    0.03    400
              | 18   Guariguata et al. (2000)     Costa Rica   Seed caching                      0.10    0.09    -7
              | 18   Guariguata et al. (2000)     Costa Rica   Seed caching                      0.00    0.13    100
              | 18   Guariguata et al. (2000)     Costa Rica   Seed caching                      0.00    0.03    100
              | 18   Guariguata et al. (2000)     Costa Rica   Tertiary seed removal/predation   0.50    0.81    63
              | 18   Guariguata et al. (2000)     Costa Rica   Tertiary seed removal/predation   1.00    0.80    -20
              | 18   Guariguata et al. (2000)     Costa Rica   Tertiary seed removal/predation   1.00    1.00    0
              | 18   Guariguata et al. (2000)     Costa Rica   Seedling survival                 0.00    0.07    100
              | 19   Guariguata et al. (2002)     Costa Rica   Seeds dispersed                   0.11    0.03    17
              | 19   Guariguata et al. (2002)     Costa Rica   Seeds dispersed                   0.00    0.02    -67
              | 20   Holbrook & Loiselle (2009)   Ecuador      Seeds removed (primary)           89.4    66.8    -25
              | 21   Ickes, K., et al. 2001.      Malaysia     Seedlings                         75.5    117.5   56
              | 21   Ickes, K., et al. 2001.      Malaysia     Sapling density                   107.1   142.3   33
              | 21   Ickes, K., et al. 2001.      Malaysia     Mortality                         10.0     8.7    -13
              | 21   Ickes, K., et al. 2001.      Malaysia     Recruits                          14.9    48.8    228
              | 21   Ickes, K., et al. 2001.      Malaysia     Species richness                  50.6    55.7    10
              | 21   Ickes, K., et al. 2001.      Malaysia     Diversity                         45.8    39.7    -13
              | 21   Ickes, K., et al. 2001.      Malaysia     Liana proportion of stems         25.9    30.5    18
              | 22   Kirika et al. (2008)         Uganda       Seed dispersal                    14124   3714    -74
              | 23   Kurten (2010a)               Panama       seed mass                         0.21    0.32    58
              | 23   Kurten (2010a)               Panama       SLA                               20.0    22.4    12
              | 23   Kurten (2010a)               Panama       Leaf toughness                    1.49    1.49    0
              | 23   Kurten (2010a)               Panama       Wood density                      0.65    0.64    -2
              | 24   Kurten (2010b)               Panama       Secondary seed predation          0.50    0.81    63
              | 24   Kurten (2010b)               Panama       Secondary seed predation          0.90    0.85    -5
              | 24   Kurten (2010b)               Panama       Secondary seed predation          0.53    0.11    -79
              | 24   Kurten (2010b)               Panama       Secondary seed predation          0.00    0.00    0
              | 24   Kurten (2010b)               Panama       Seed caching                      1.16    1.33    15
              | 24   Kurten (2010b)               Panama       Seed caching                      0.83    1.16    40
              | 25   Lizcano (2006)               Colombia     Richness                          8.02    11.24   40
              | 25   Lizcano (2006)               Colombia     Shannon Index                     0.82    0.75    -9
              | 26   McConkey & Drake (2006)      Tonga        Seed dispersal                    0.34    0.03    -90
              | 27   Nuñez-Iturri et al. (2007)   Peru         Sapling richness - total          47.4    50.4    6
              | 27   Nuñez-Iturri et al. (2007)   Peru         Sapling richness -large mammal    16.6     7.8    -53
              | 27   Nuñez-Iturri et al. (2007)   Peru         Sapling richness - nongame        27.1    36.6    35
              | 27   Nuñez-Iturri et al. (2007)   Peru         Sapling richness - abiotic        3.70    6.00    62
              | 27   Nuñez-Iturri et al. (2007)   Peru         Sapling density - total           78.3    90.0    15
              | 27   Nuñez-Iturri et al. (2007)   Peru         Sapling density -large mammal     26.8    11.3    -58
              | 27   Nuñez-Iturri et al. (2007)   Peru         Sapling density - nongame         45.5    67.8    49
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              | 
text          | 27   Nuñez-Iturri et al. (2007)   Peru       Sapling density - abiotic         5.91   10.98    86
              | 28   Nuñez-Iturri et al. (2008)   Peru       Species richness (primate disp)   1.60   0.60    -63
              | 28   Nuñez-Iturri et al. (2008)   Peru       Species richness (abiotic disp)   1.40   1.80     29
              | 28   Nuñez-Iturri et al. (2008)   Peru       Species richness                  145    100     -31
              | 28   Nuñez-Iturri et al. (2008)   Peru       Density (primate disp)            1.90   0.90    -53
              | 28   Nuñez-Iturri et al. (2008)   Peru       Density (abiotic)                 3.60   11.30   214
              | 29   Roldan & Simonetti (2001)    Bolivia    Seed predation                    0.43   0.64     49
              | 29   Roldan & Simonetti (2001)    Bolivia    Trampling survival                0.78   0.90     15
              | 29   Roldan & Simonetti (2001)    Bolivia    Seedling density                  4.21   3.92     -7
              | 29   Roldan & Simonetti (2001)    Bolivia    Species richness                  35.0   34.0     -3
              | 29   Roldan & Simonetti (2001)    Bolivia    Seedling spp:Adult spp            0.61   0.59     -5
              | 29   Roldan & Simonetti (2001)    Bolivia    Seedling composition              4.21   3.92     -7
              | 30   Royo & Carson (2005)         Panama     Species richness                  16.8   13.1    -22
              | 30   Royo & Carson (2005)         Panama     Herb Density                      1.21   1.19     -2
              | 30   Royo & Carson (2005)         Panama     Density dominants                 0.42   0.35    -17
              | 30   Royo & Carson (2005)         Panama     Density rare                      0.34   0.16    -53
              | 30   Royo & Carson (2005)         Panama     Cover                             7.90   5.90    -25
              | 30   Royo & Carson (2005)         Panama     Cover of dominants                2.65   1.50    -43
              | 31   Sethi & Howe (2009)          India      Total seedlings                   2.55   0.76    -70
              | 31   Sethi & Howe (2009)          India      Seedlings under parent            0.37   0.60     64
              | 31   Sethi & Howe (2009)          India      Seedlings away from parent        2.19   0.16    -93
              | 31   Sethi & Howe (2009)          India      Total seedlings                   2.17   0.81    -62
              | 31   Sethi & Howe (2009)          India      Seedlings under parent            0.99   0.35    -65
              | 31   Sethi & Howe (2009)          India      Seedlings away from parent        1.18   0.46    -61
              | 31   Sethi & Howe (2009)          India      Total seedlings                   4.16   0.81    -80
              | 31   Sethi & Howe (2009)          India      Seedlings under parent            2.96   0.58    -81
              | 31   Sethi & Howe (2009)          India      Seedlings away from parent        1.20   0.24    -80
              | 32   Sork (1987)                  Panama     Secondary seed predation          0.94   0.41    -56
              | 32   Sork (1987)                  Panama     seedling survival                 0.69   0.97     42
              |                                   Peru/
              | 33   Terborgh & Wright (1994)     Panama     Seed predation                    0.35   0.82    136
              |                                   Peru/
              | 33   Terborgh & Wright (1994)     Panama     Seedling density                  38.3   29.3    -23
              |                                   Peru/
              | 33   Terborgh & Wright (1994)     Panama     Seedling recruitment              0.25   0.96    276
              |                                   Peru/
              | 33   Terborgh & Wright (1994)     Panama     Seedling mortality                0.20   0.29     43
              | 34   Terborgh et al. (2008)       Peru       Recruit. Bird dispersed           0.23   0.24     4
              | 34   Terborgh et al. (2008)       Peru       Recruit. Bat dispersed            0.10   0.11     16
              | 34   Terborgh et al. (2008)       Peru       Recruit. Lg. primate dispersed    0.25   0.19    -24
              |                                              Recruit. Sm. arboreal mammal
              | 34   Terborgh et al. (2008)       Peru       dispersed                         0.33   0.24    -26
              |                                              Recruit. Terrestrial mammal
              | 34   Terborgh et al. (2008)       Peru       dispersed                         0.04   0.02    -50
              | 34   Terborgh et al. (2008)       Peru       Recruit. Wind disp.               0.05   0.17    278
              | 35   Wang et al. (2007)           Cameroon   Diaspore under adult              10.0   50.0    400
              | 35   Wang et al. (2007)           Cameroon   Seed dispersal                    0.98   0.58    -41
              | 36   Wright et al. (2000)         Panama     Seed predation                    90.8   47.7    -47
              | 36   Wright et al. (2000)         Panama     Seed predation                    0.03   0.34    1033
              | 36   Wright et al. (2000)         Panama     Seed density under parent         180    2749    1427
              | 36   Wright et al. (2000)         Panama     Seed density away from parent     2.65   1.79    -32
              | 36   Wright et al. (2000)         Panama     Prop. seeds dispersed             0.93   0.39    -58
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              | 
text          |  36   Wright et al. (2000)        Panama    Seedling density                      0.0    0.0    300
              |  36   Wright et al. (2000)        Panama    Seedlings:Adult                      11.0    28.9   163
              |  36   Wright et al. (2000)        Panama    Seed predation                       91.7    21.7   -76
              |  36   Wright et al. (2000)        Panama    Seed predation                        0.1    0.3    460
              |  36   Wright et al. (2000)        Panama    Seed density under parent            910     1290   42
              |  36   Wright et al. (2000)        Panama    Seed density away from parent         4.4    2.8    -37
              |  36   Wright et al. (2000)        Panama    Prop. seeds dispersed                 0.9    0.1    -93
              |  36   Wright et al. (2000)        Panama    Seedling density                      0.1    0.2    129
              |  36   Wright et al. (2000)        Panama    Seedlings:Adult                      113.8   92.5   -19
              |  37   Wright et al. (2001)        Panama    Seed density under parent tree       24.6    35.7   46
              | 37    Wright et al. (2001)        Panama    Seed density away from parent        0.9     0.2    -81
              |                                             tree
              | 37    Wright et al. (2001)        Panama    Seedling density under parent         0.0    0.1    282
              |                                             Seedling density away from
              |  37   Wright et al. (2001)        Panama    parent                                0.0    0.1    282
              |  37   Wright et al. (2001)        Panama    Seedling density (total)              0.0    0.1    282
              |  37   Wright et al. (2001)        Panama    Seed predation-rodents                0.8    0.4    -46
              |  37   Wright et al. (2001)        Panama    Seed predation-bruchid                0.1    0.4    266
              |  38   Wright et al. (2007)        Panama    Community mean seed mass              90     100    11
              |  38   Wright et al. (2007)        Panama    Prop. seedlings (hunted disperser)    0.7    0.4    -40
              | 38    Wright et al. (2007)        Panama    Prop. seedlings (unhunted             0.2    0.4    75
              |                                             disperser)
              | 38    Wright et al. (2007)        Panama    Proportion lianas                     0.1    0.4    150
              | 38    Wright et al. (2007)        Panama    Seedling density                     15.2    9.4    -38
              | 38    Wright et al. (2007)        Panama    Seedling Richness                    70.7    69.8   -1
              | 38    Wright et al. (2007)        Panama    Seedling S-W Diversity                2.6    3.2    23
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              | 
              | 
title         | Chapter 2
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title         | Reduced seed dispersal as a
              | consequence of hunting lowers
              | community-level wood density in a
              | Neotropical forest
text          | Authors: Erin L. Kurten, S. Joseph Wright, Andrés Hernandéz , Walter P. Carson
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title         | Abstract
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text          | Defaunation alters interactions between plants and their seed dispersers and predators,
              | and is sometimes associated with decreased diversity at the community level. A more
              | cryptic plant response to defaunation is an altered distribution of life histories and
              | functional traits in the community. In this study, we censused 12,769 seedlings in a
              | long-term terrestrial mammal exclosure experiment (LTEE) in Central Panama to
              | examine how vertebrate seed dispersers and seed predators shape relative abundances
              | of species classified by dispersal mode, growth forms, seed mass, leaf mass per area
              | (LMA), leaf toughness, and wood density. We then compared exclosure results with
              | data from a natural comparison of 38,250 seedlings in nearby hunted and unhunted
              | sites. The exclosure experiment excludes terrestrial seed predators and herbivores but
              | not seed dispersers such as primates, birds, and bats. In contrast, the hunting
meta          | 36         CHAPTER 2: CONSEQUENCES OF HUNTING FOR SEED DISPERSAL AND WOOD DENSITY
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              | 
              | 
text          | comparison reduces the abundance of all three groups. We tested the hypotheses that
              | (1) where seed dispersal is disrupted, species with unhunted dispersal modes, and
              | lianas, which are abiotically dispersed, are favored, (2) where seed predation is
              | reduced, larger-seed plant species are favored, and (3) where herbivory is reduced,
              | species with lower LMA, leaf toughness, and wood density are favored. Consistent
              | with our expectations, dispersal-driven changes in the relative abundance of growth
              | forms or dispersal mode classes were not observed in the terrestrial mammal exclosure
              | experiment, while higher median seed mass as a consequence of reduced seed
              | predation was observed. In contrast to our hypothesis, leaf functional traits did not
              | differ as a consequence of defaunation either in the forest comparison or in the LTEE.
              | Interestingly, wood density responses differed between our two experiments. Species
              | dispersed by mammals and large birds had significantly higher mean wood density
              | than wind dispersed species, suggesting that seed dispersal, rather than seedling
              | herbivory, may mediate decreases in community median wood density in hunted
              | forests.
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title         | Introduction
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text          | Over-hunting has caused severe declines, and even local extirpations, of hunted
              | wildlife populations in tropical forests throughout Latin America (Peres & Palacios
              | 2007), Africa (Fa & Brown 2009), and Asia (Corlett 2007). Defaunation perturbs
              | plant interactions with the frugivores, granivores, and herbivores that play critical
              | roles in establishing the composition and spatial distribution of seedlings in tropical
              | forest seedling banks. Reduced seed dispersal in hunted forests results in higher
              | proportions of undispersed seeds under parent trees of species reliant on hunted biotic
              | dispersal agents (Wright & Duber 2001, Cordiero & Howe 2003, Babweteera et al
              | 2007, Sethi & Howe 2009). Vertebrate seed predation rates may increase or decrease,
              | depending on the severity of defaunation and the size of the seeds and seed predators
              | affected (Guariguata et al. 2000, Galetti et al. 2006, Dirzo et al. 2007). Vertebrate
              | herbivory rates can also be drastically reduced (Dirzo and Miranda 1991). The net
              | effect of these perturbations can be the loss of plant diversity (Dirzo and Miranda
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              | 
              | 
text          | 1991, Chapman & Onderdonk 1998), with up to 66% of species failing to recruit in the
              | most extreme case documented.
              |        Other important changes may also be occurring in the plant community even if
              | species richness is unaffected. Species with hunted dispersal agents, such as primates
              | or large birds, consistently decrease in abundance in hunted forests, while species with
              | abiotic or unhunted dispersal agents increase (Wright et al. 2007b, Nuñez-Iturri et al.
              | 2008, Terborgh et al. 2008). Lianas, the majority of which are abiotically dispersed in
              | this forest (Hardesty & Muller-Landau 2005), also increase in abundance in hunted
              | sites (Wright et al. 2007b). Where dispersal of large, primate-dispersed seeds is
              | disrupted by local extirpation of ateline monkeys, the relative abundance of those plant
              | species is lower than in sites where ateline monkeys are present (Nuñez-Iturri et al.
              | 2008). In sites where hunting decreases rodent seed predator populations, the median
              | seed mass of the seedling community is higher than in unhunted sites (Wright et al.
              | 2007b).
              |        In this study, our first goal was to move beyond investigations of dispersal
              | mode classes and seed mass to examine the effect of defaunation on other functional
              | traits. Lower abundances of browsers and other seedling predators in hunted sites
              | should lead to reduced vertebrate herbivory and seedling predation. Leaf mass per
              | unit area (LMA), low leaf laminar toughness (hereafter referred to as “toughness”),
              | and wood density are correlated with palatability to vertebrates or seedling survival
              | (Wardle et al. 2002, Alvarez-Clare & Kitajima 2007). We hypothesized that species
              | with low leaf area per unit mass, low leaf laminar toughness, and lower wood density
              | should be favored in hunted sites.
              |        A weakness of many forest comparison studies in defaunation work is that they
              | lack replication of hunted and unhunted forests. Even when there is replication,
              | differences in climate, soils, forest age, fragmentation or other anthropogenic factors
              | may covary with hunting intensity in comparative studies, making it difficult to
              | attribute the patterns observed to hunting alone. Therefore, a second goal of this study
              | was to validate results from forest comparisons with data from a long-term exclosure
              | experiment (LTEE). We conducted this study in Central Panama, where a hunting
meta          | 38         CHAPTER 2: CONSEQUENCES OF HUNTING FOR SEED DISPERSAL AND WOOD DENSITY
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              | 
              | 
text          | defaunation gradient has been previously documented (Wright et al. 2007b). Within
              | the unhunted, protected sites, a terrestrial mammal exclosure experiment has been
              | ongoing for the past fifteen years (Royo & Carson 2005).
              |        Because hunting typically disrupts multiple plant-animal interactions
              | simultaneously, it can be difficult to determine the relative influence of lost seed
              | dispersers, seed predators, or herbivores on resulting seedling communities in
              | comparative studies. A third goal of this study was to improve the extent to which
              | changes in the seedling community could be attributed to changes in particular
              | interactions. Unlike the hunted forest comparison, our LTEE excludes terrestrial seed
              | predators and herbivores from exclosure plots, but does not alter the abundance of
              | primary dispersal agents such as primates and most large birds. By comparing results
              | between the forest comparison and exclosure approaches, we can identify which
              | changes in the seedling community are due to changes in seed dispersal and which are
              | due to changes in seed or seedling predation. .
              |        We predicted that seedling communities in exclosures would have higher
              | median seed massas a consequence of lower seed predation, consistent with the forest
              | comparison (Wright et al. 2007). In contrast to the forest comparison experiment, we
              | predicted the LTEE would not show differences in the relative abundances of dispersal
              | mode classes or growth forms. We expected that median LMA, toughness and wood
              | density would be lower in exclosure plots relative to paired plots open to terrestrial
              | mammals, and in hunted forests relative to unhunted forests, as a consequence of
              | reduced herbivory.
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              | 
title         | Methods
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              | 
text          | Study sites. The Barro Colorado National Monument (BCNM) is a group of islands
              | and mainland peninsulas located in Lake Gatun in the Republic of Panama. Because
              | of forest guard patrol and researcher presence, activity of poachers is virtually
              | nonexistent on Barro Colorado Island (BCI) itself and is highly reduced on Gigante
              | (GIG) and other peninsulas. The Parque Nacional Soberanía (PNS) is a protected area
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              | 
              | 
text          | contiguous with the BCNM, which is not actively patrolled. Intensity of poaching
              | within the PNS varies with accessibility, but is much greater than within the BCNM
              | (Wright et al. 2000).
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              | 
text          | Exclosure experimental design.      Between late-1993 and mid-1994, eight pairs of
              | fenced, exclosure plots and open, control plots were established within the BCNM
              | (Royo & Carson 2005). Paired fenced and unfenced plots are 30 m x 45 m and are
              | approximately 5 m apart.       Exclosure fences are constructed of 12.7 x 12.7 cm
              | galvanized steel fencing 2.2 m tall and buried 0.25 m deep. A secondary 1.3 x 1.3 cm
              | mesh surrounds the lower 70 cm and also extends 0.25 m below ground. Twenty-
              | eight 0.5 x 0.5 m subplots were established in each of the 16 plots in a stratified
              | random fashion to census seedlings.        To avoid fence effects, no subplots were
              | established within a 5-7 m buffer zone of a plot edge. Within each subplot, each plant
              | less than 50 cm in height was tagged, measured, and identified. Seedling census data
              | were collected in 2006.
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              | 
text          | Exclosure effectiveness. To assess differences in the animal communities between
              | open and exclosure treatments, Reconyx RC-55 infrared cameras (Reconyx, Inc.,
              | Holmen, WI) were used to monitor mammal activity in the 16 plots between August
              | and October 2008. Each plot was monitored at 6-7 locations, for a total of 41 camera
              | trap days per plot. A camera trigger was counted as a new “visit” if (1) it was a
              | different species than the prior trigger, or (2) if 60 minutes had elapsed between
              | triggers (Di Bitetti et al. 2008). We chose this method of quantification because
              | unmarked individuals of most mammals in this community cannot be distinguished by
              | photograph, and because this measure of activity likely describes animal impact on
              | each plot more accurately than abundance. Because it was difficult to accurately
              | count individuals for social animals such as peccaries (Tayassu tajacu) and coatis
              | (Nasua narica), activity by these species was analyzed as the number of visits by
              | social groups rather than visits by individuals.
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              | 
              | 
text          | Hunting intensity comparison. At 9 protected sites (BCNM) and 11 intensely hunted
              | sites (PNS), all adult trees larger than 20 cm diameter at breast height (dbh) within a 1
              | ha plot were mapped and identified by Condit et al. (2002) and Wright et al. (2007b).
              | Between June and December 2004, all woody plants less than 50 cm tall in an 8 x 8 m
              | subplot were censused by Wright et al. (2007b). Seedling plots were at the center of
              | each tree plot, or as close as possible in three plots in which tree falls occurred
              | between adult and seedling censuses. A total of 38250 individuals comprising 312
              | identified species were recorded (Wright et al. 2007b).
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              | 
text          | Plant traits. Wright et al. (2010) determined life history traits, dry seed mass, leaf
              | mass per area (LMA), laminar toughness, and wood density for species in central
              | Panama. In this study, dry seed mass was measured as endosperm plus embryo mass
              | after oven drying to constant mass at 60ºC. Leaf mass per unit area was measured on
              | shade leaves as the mass of a standard-sized leaf disc after oven drying to constant
              | mass at 60ºC divided by the area of the disc. Laminar toughness was measured as the
              | force necessary to cut across a leaf, perpendicular to the midvein (Lucas et al. 2000).
              | Wood specific gravity, or mass after drying at 100ºC per unit volume, was used as the
              | unit of wood density. Data on dispersal agents have been assembled from published
              | studies and long-term personal observations.
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              | 
text          | Analyses. We used a MANOVA to test whether mammal activity differed between
              | open and control plots for each vertebrate species observed. Paired t-tests were used
              | to test for differences in the relative abundance of growth forms, dispersal mode
              | classes, and functional traits. For the hunting comparison, an ANCOVA was used to
              | determine whether the correspondence of functional traits between seedling and adult
              | communities differed with hunting. Statistical analyses were performed with SYSTAT
              | © 11.0 (Richmond, CA, U.S.A.) and R version 2.7.2 (R Development Core Team,
              | 2008).
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              | 
              | 
title         | Results
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              | 
text          | EXCLOSURE     EFFECTIVENESS.                   Fenced plots excluded non-climbing, terrestrial
              | granivores and herbivores from exclosures, including agoutis (Dasyprocta punctata),
              | paca (Agouti paca), deer (Mazama Americana and Odocoileus virginianus), and
              | peccaries (T. tajacu) (Fig. 1). Most climbing animals appeared to be undeterred by the
              | exclosure treatment.           Spiny rats (Proechimys steerei) showed higher activity in
              | exclosures than controls, perhaps responding to a lack of competition for food, greater
              | cover, or a reduction in ocelet abundance (Felis pardalis) in the exclosures. Most
              | birds were not affected by the exclosures, a notable exception being tinamous, which
              | are seed predators (Erand et al. 1991).
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              | 
text          |                                    0
              |                     Agouti                                                                  ***
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text          |                                0           20            40            60             80          100
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text          |                   Anteater
              |                                    0
              |                  Armadillo
              |                                    0
              |                   Capuchin
              |                      Coati†
              |                                    0
              |                       Deer
              |                                    0
              |                     Mouse
              |                                    0
              |                      Ocelot                *
              |                  Opposum
              |                                    0
              |                                                      *
              |                        Paca                                                 **
              |                                    0
              |                   Peccary†                                                                  **
              |                                    0
              |                      Rabbit
              |                   Spiny Rat
              |                    Squirrel
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text          |                                    0
              |                   Tinamou
              |                Birds (other)
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text          |                                0       2         4            6       8          10        12     14
              |                                                               Visits/plot
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              | 
              | 
              | 
text          |        FIGURE 2.1. Total visits per plot by species for control plots (dark grey) and exclosure
              |        plots (light grey). Zeros denote no individuals observed in exclosures. *** p < 0.001,
              |        ** p < 0.01, * p < 0.05, 
 p < 0.1; † groups, not individuals
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              | 
              | 
              | 
text          | DISPERSAL                          AGENTS                           & LIFEFORMS. A total of 12,769 seedlings of 322 species were
              | recorded in the 2006 LTEE seedling census. Of those, dispersal agents were known
              | for 247 species (76.7%) and 12575 stems (98.5%), and growth form was known for
              | 241 species (74.8%) and 12468 stems (97.6%). Consistent with our expectations,
              | there was no difference in the proportions of seedlings with different dispersal agents
              | (hunted: t = 1.161, P = 0.2651; unhunted t = 1.861, P = 0.089) (Fig. 2) or growth
              | forms (free-standing: t = 1.7131, P = 0.1096) (Fig. 3) in the LTEE.
              |                                     1.0
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              | 
              | 
              | 
text          |                                                                            Hunted           Mixed          Unhunted
              |                                     0.8
              |          Proportion of seedlings
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text          |                                     0.6
              |                                     0.4
              |                                     0.2
              |                                     0.0
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              | 
              | 
              | 
text          |                                                                        Open Excl          Open Excl        Open Excl
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text          |                                                                                     Treatment by Disperser
              |        FIGURE 2.2. Proportion of seedlings by dispersal mode class is not significantly
              |        different between treatments in exclosure experiment.
              |                                                                      1.0
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              | 
              | 
              | 
text          |                                                                                 Climbing        Free Standing
              |                                           Proportion of seedlings
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text          |                                                                      0.8
              |                                                                      0.6
              |                                                                      0.4
              |                                                                      0.2
              |                                                                      0.0
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              | 
              | 
              | 
text          |                                                                                 Open Excl           Open Excl
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text          |                                                                                Treatment by Growth form
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text          |        FIGURE 2.3. Proportion of seedlings by life form is not significantly different
              |        between treatments in exclosure experiment.
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              | 
              | 
              | 
text          | SEED MASS. In the LTEE, seed dry mass was known for 166 (51.6 %) of species and
              | 10866 (85.1%) of stems. Exclosures removed all but the smallest seed predators. The
              | reduction in agouti activity was particularly dramatic (Fig. 4). Consistent with these
              | findings, as well as results from the forest comparison (Wright et al. 2007b), median
              | seed mass was 44% higher in exclosure plots, relative to controls (t = 2.315, P =
              | 0.02261).
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text          |                                              250
              |                  Diaspore Dry mass (mg)
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text          |                                              200
              |                                              150
              |                                              100
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              | 
              | 
              | 
text          |                                                            Open                 Excl
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              | 
text          |                                                                   Treatment
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text          |        FIGURE 2.4.                        (A) Median seed mass is significantly higher in exclosures (p <
              |        0.02261).
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              | 
text          | LEAF TRAITS.    LMA and laminar toughness were known for 11,173 stems (87.5%)
              | and 10,904 stems (85.4%) respectively in the LTEE, and for 33,839 stems (87.5 %)
              | and 29,962 stems (77.5 %) respectively in the hunting experiment. Exclosure and
              | hunting treatments were expected to reduce the number of terrestrial vertebrate
              | seedling predators in a way analogous to seed predators. A reduction in vertebrate
              | herbivores was expected to favor species with low LMA and small laminar toughness.
              | Contrary to expectation, neither the exclosure nor the hunting experiment showed
              | significant differences in median LMA or laminar toughness, nor was there a
              | significant difference between protected and hunted sites when the correspondence
meta          | 44            CHAPTER 2: CONSEQUENCES OF HUNTING FOR SEED DISPERSAL AND WOOD DENSITY
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              | 
              | 
text          | between seedling and adult communities was evaluated by ANCOVA (data not
              | shown).
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              | 
text          | WOOD DENSITY. Adult wood specific gravity was known for 208 species (64.6% %)
              | and 11,620 stems (91.0 %) in the LTEE, and for 239 species (63.2 %) and 28,488
              | stems (73.3 %) in the hunting experiment. Stem tissue density is strongly positively
              | correlated with seedling survival in this forest (Alvarez-Clare & Kitajima 2007). If
              | greater stem tissue densities confer a protective effect against herbivores, we would
              | expect higher wood density species to be favored in open plots relative to exclosures,
              | and protected sites relative to hunted sites. Median wood densities were greatly
              | reduced in hunted site seedling communities, relative to both protected site seedling
              | communities (pooled variance t=3.86, P = 0.0011, one-tailed test) (Fig. 5a), and their
              | surrounding adult communities (F1,18 = 16.2, p < 0.001) (Fig. 5b). However, the
              | LTEE showed no differenced in median wood density (t = 0.024, P = 0.49) (Fig. 5a).
              |                                                                                                                                  0.65
              |                                                                                         Wood density of tree seedlings (g/cm3)
              |                                               0.65
              |               Wood Specific Gravity (g/cm3)
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              | 
              | 
              | 
text          |                                                      A                                                                                    B
              |                                                          Exclosure           Hunting
              |                                                                                                                                  0.60
              |                                               0.60
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              | 
              | 
              | 
text          |                                                                                                                                  0.55
              |                                               0.55
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              | 
              | 
              | 
text          |                                                                                                                                  0.50
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              | 
text          |                                                                                                                                  0.45
              |                                               0.50
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              | 
              | 
              | 
text          |                                                                                                                                         0.45   0.50   0.55   0.60   0.65
              |                                                          Open   Excl   Protect   Hunt                                             Wood density of canopy trees (g/cm3)
              |                                                                  Treatment
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text          |      FIGURE 2.5. (A) Median wood density is not significantly different between treatments in the
              |      exclosure experiment (p = 0.0238), but is significantly lower in hunted sites relative to
              |      protected sites (p = 0.0011). White and grey boxes indicate analogous treatments (B) Seedling
              |      median wood density is lower than adult median wood density for tree species in hunted sites
              |      (dark circles) but not in protected sites (light triangles) (F1,18 = 16.2, p < 0.001). The dashed
              |      line represents is the 1:1 line at which adult and seedling communities have the same median
              |      values.
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              | 
text          |          We tested whether differences in primary dispersal may be responsible for the
              | discrepancy in wood density responses, as it was for differences in dispersal mode and
              | growth form. We used an ANOVA to compare mean wood densities across dispersal
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              | 
              | 
text          | mode classes. Interestingly, species with unhunted dispersal agents had significantly
              | lower mean wood density than either species with hunted dispersal modes, or species
              | dispersed by agents in both categories (ANOVA, F2,                                                                                      277,   p = 0.0017) (Fig. 6a).
              | Specifically, wind dispersed species had significantly lower wood densities compared
              | to both mammal and large bird dispersed species (ANOVA, F6, 461, p = 0.0057) (Fig.
              | 6b).
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              | 
text          |                                                                                                                    0.7
              |                                       1.0
              |  Mean Wood Specific Gravity (g/cm3)
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              | 
              | 
              | 
text          |                                                                                                                          B
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              | 
              | 
              | 
text          |                                                                               Mean Wood Specific Gravity (g/cm3)
              |                                              A   a
              |                                                           a
              |                                                                    b                                               0.6          ab
              |                                                                                                                                          a
              |                                                                                                                                                 ab
              |                                                                                                                                                         a     ab
              |                                       0.8
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              | 
              | 
              | 
text          |                                                                                                                           ab                                        b
              |                                                                                                                    0.5
              |                                       0.6
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              | 
              | 
              | 
text          |                                                                                                                    0.4
              |                                       0.4
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              | 
              | 
              | 
text          |                                                                                                                    0.3
              |                                       0.2
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              | 
              | 
              | 
text          |                                                                                                                    0.2
              |                                       0.0
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              | 
              | 
              | 
text          |                                                                                                                    0.1
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text          |                                               Hunted   Mixed    Unhunted                                           0.0
              |                                                                                                                          Bat   Bird     L.Bird Explo   Mam   Water Wind
              |                                                  Dispersal Mode Class
              |                                                                                                                                       Dispersal Agent
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              | 
              | 
              | 
text          |                                             FIGURE 2.6. (A) Species with unhunted dispersal agents have lower WSGs. (B)
              |                                             Wind dispersed species have significantly lower mean wood density than both
              |                                             mammal and large bird dispersed species. Bars with same letter were not
              |                                             significantly different in post hoc comparisons.
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              | 
title         | Discussion
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              | 
title         | Hunting, vertebrate abundance, and plant functional diversity
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              | 
text          | This study demonstrates that hunting effects change in the seedling community of
              | tropical forests primarily by perturbing biotic seed dispersal and vertebrate seed
              | predation. Increases in lianas and reductions in species with hunted biotic dispersal
              | agents were observed in the hunting experiment, where primary dispersers were
              | reduced (Wright et al. 2007b), but not in the LTEE, where primary dispersers were not
              | manipulated (Figs. 2 and 3). Activity of seed predators was dramatically reduced in
              | the LTEE, and here we observed increases in median seed mass (Fig. 4). This result is
meta          | 46         CHAPTER 2: CONSEQUENCES OF HUNTING FOR SEED DISPERSAL AND WOOD DENSITY
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              | 
              | 
text          | consistent with larger-seed species experiencing an escape from vertebrate seed
              | predation (Dirzo et al., 2007), and lends strong support to the view that changes in
              | seed predator abundance are responsible for the increases in median seed mass
              | observed in hunted forests relative to protected forests (Wright et al. 2007b).
              |        Leaf traits showed no differences in both the LTEE and the hunting
              | experiment. This suggests that the reduction of vertebrate herbivores by hunting does
              | not have a strong impact on changes in seedling community composition at early
              | stages of plant recruitment.
              |                Wood density responses to herbivore reduction differed between the
              | LTEE and hunting experiment. The likeliest explanation for the discrepancy is that, as
              | with differences in dispersal mode and growth form responses between our
              | experiments, differences in wood density responses are dispersal-driven. To test this
              | post hoc hypothesis, we evaluated whether dispersal mode classes differ in their mean
              | wood densities. Consistent with our hypothesis that experimental differences in wood
              | density responses are due to differences in dispersal, wood density was significantly
              | lower for species with unhunted dispersal agents than for species having either hunted
              | dispersal agents, or a combination of the two (Fig. 6).
              |        In contrast to the hunting experiment, the LTEE shows higher spiny rat activity
              | in the defaunated treatment. As spiny rats are known to be significant seedling
              | predators in the absence of other competitors (Asquith et al. 1997), it is also possible
              | that they may be compensating for the reduction in other seedling predators inside the
              | exclosures. However several lines of evidence contradict this putative explanation.
              |        First, if spiny rats were compensating for other herbivores inside the exclosure
              | as in the study of Asquith et al. (1997), we would expect overall seedling densities to
              | be similar in open and exclosure plots, but instead, seedling densities in exclosures are
              | about 2-fold higher than in open plots (data not shown). The herbivory study on
              | islands which indicated that spiny rats alone can achieve seedling predation rates as
              | high as communities with relatively intact mammal fauna were conducted on islands
              | in which spiny rat densities are among the highest rodent densities ever documented
              | (Adler 1996), but our study does not replicate these high densities. In addition,
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              | 
              | 
text          | herbivory by spiny rats cannot explain why wood density responses differ between
              | experiments, but leaf traits did not.
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              | 
text          |        Our evidence for a link between seed dispersal and community wood density is
              | an interesting result because Brodie and Gibbs (2009) recently proposed that
              | reductions in seed dispersal as a consequence of defaunation may result in shifts in
              | mean wood density at the community level.           However, the mechanism that they
              | proposed assumed that seed mass was positively correlated with wood density across
              | species in tropical forests, which is true neither generally, nor for our site specifically
              | (Wright et al. 2010).      Here we show that dispersal likely mediates changes in
              | community wood density distributions via an alternative mechanism, namely that low
              | and high wood density plant species are disportionately associated with dispersal
              | mode agents that are favored and disfavored respectively by hunting.
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              | 
text          | Implications of defaunation for carbon sequestration in tropical forests.
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              | 
text          |        Our results suggest that there may be important links between hunting,
              | frugivore abundance, and the ability of future tropical forests to sequester carbon.
              | Disruption of seed dispersal by game animals has the potential to alter the ability of
              | forests to store carbon by (1) decreasing the abundance of trees relative to lianas
              | (Wright et al. 2007b), and (2) shifting wood density distributions in the community
              | toward lower wood density species (Fig 5a).
              |        Higher liana relative abundance may reduce carbon storage at the ecosystem
              | level in two ways. Lianas compete with trees for light, displace tree leaf mass (Kira &
              | Ogawa 1971), and lower tree growth.         One recent study from Amazonia estimated
              | that above ground competition from lianas was responsible for reductions in tree
              | growth that reduced carbon sequestration by the equivalent of 0.25 Mg C ha-1 yr-1 (van
              | der Heijden & Phillips, 2009). Growth of the lianas themselves amounted to 0.07 Mg
              | C ha-1 yr-1, which did not compensate for reductions in tree growth. The authors
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              | 
              | 
text          | therefore estimated that competition from lianas reduced carbon sequestration at the
              | ecosystem level by net amount of 0.18 Mg C ha-1 yr-1 or 71%.
              |        The consequences of lowering community mean wood density for carbon
              | storage depend on the relationship between wood density and tree volume in a
              | particular forest. Three Panamanian forests in the region, including BCI, exhibit a
              | weak, but negative relationship between plot mean wood density and plot biomass
              | (Stegen et al. 2009). This suggests that the reduction in community wood density in
              | our study site may actually lead to higher forest biomass, and partially compensate for
              | any reduction resulting from the relative reduction in free-standing stems. However,
              | forests exhibiting positive wood density-biomass relationships could experience a
              | decrease in carbon sequestration potential under the same scenario of reduced plot
              | wood density.
              |        The phenomenon of over-hunting in tropical forests is widespread and severe.
              | If the changes in carbon storage potential represented by shifting seedling
              | communities in this study are as wide-spread as over-hunting itself, the potential
              | impact may be great. However, many questions must be answered before we can
              | understand the magnitude of the impact that hunting may have on the ability of
              | tropical forests to sequester carbon.
              |        First, to our knowledge, this is the first study demonstrating that tropical tree
              | wood densities are associated with dispersal mode classes, and in a way that would
              | respond to hunting. Studies investigating the generality of this association would
              | represent the first step in predicting whether the changes observed in our site would
              | apply pan-tropically. Secondly, here we report changes in the seedling community,
              | but better models of forest dynamics are needed to understand the extent to which
              | those changes will propagate to the adult community. Third, how lianas alter carbon
              | storage at the ecosystem level is poorly understood, and in particular we do not
              | understand how liana competition with trees varies as a function of liana abundance.
              | Finally, as noted by Stegen et al. (2009), there are many unanswered questions
              | pertaining to how changes in wood density distributions translate to changes in
              | biomass at the plot level.
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              | 
              | 
text          |            Hunting is not the only cause of defaunation. Frugivores, granivores, and
              | herbivores may also decrease in abundance as a result of habitat fragmentation and
              | loss (Asquith et al. 1999, Galetti et al. 2006, Terborgh et al. 2006, Cramer et al.
              | 2007).      As with hunting, decreases in abundance with intensity of habitat loss
              | disproportionately affect larger-bodied animals. Therefore, even in the absence of
              | hunting, other sources of defaunation may be expected to have similar indirect effects
              | on plant community functional trait composition and ecosystem services in tropical
              | forests.
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              | 
title         | Acknowledgements
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              | 
text          | We extend our gratitude to the Autoridad Nacional del Ambiente (ANAM) for
              | permitting us to conduct research within the Parque Nacional Soberanía.        David
              | Brassfield, Didimo Ureña, and Joana Balbuena conducted the seedling censuses in the
              | hunting experiment. A competitive research grant from the Smithsonian Tropical
              | Research Institute funded seedling censuses in hunted and protected forests. The
              | Smithsonian Tropical Research Institute, the U.S. Department of Defence Legacy
              | Fund, and the U.S. Agency for International Development funded canopy tree
              | censuses at hunted and protected forests. NSF grant DEB 9527729 funded the LTEE.
              | NSF DEB-0808338, the Theresa Heinz Environmental Scholars program, and the
              | STRI short-term fellowship program provided support to E. Kurten.
              | 50   CHAPTER 2: CONSEQUENCES OF HUNTING FOR SEED DISPERSAL AND WOOD DENSITY
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              | 
              | 
              | 
title         | Chapter 3
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title         | Terrestrial mammalian herbivores
              | influence the distribution of defense
              | and nutrient traits in a Neotropical
              | forest
              | Erin. L. Kurten, Walter P. Carson
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title         | ABSTRACT
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text          | Mammalian herbivores are known to be important regulators of plant community
              | composition in tropical savannas and temperate systems. However, their impact on
              | tropical communities beyond their impact as seedling predators has remained largely
              | unexplored, perhaps because of the assumed importance of insect herbivory for
              | tropical plants beyond the seedling stage. In this study, we censused 35,069 saplings
              | in a long-term terrestrial mammal exclosure experiment in Central Panama to
              | determine whether mammalian herbivores had the ability to regulate the abundances
              | of species differing in wood density, specific leaf area (SLA), leaf toughness, and leaf
              | nitrogen. We found that community mean leaf toughness decreased in exclosures over
              | time, while community mean leaf nitrogen increased.           These differences were
              | primarily due to an increased abundance of species possessing favored traits, rather
              | than species turnover as a consequence of herbivore exclusion. No community-level
              | differences were observed for mean wood density or specific leaf area. We also found
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              | 
              | 
text          | that intraspecific leaf toughness was lower in exclosures. Our results suggest that
              | mammalian herbivores are important for shaping plant functional trait distributions
              | well beyond the seedling stage, and that their effects on the sapling community are
              | distinct from their effects on the seedling community.
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              | 
title         | INTRODUCTION
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text          | Mammalian herbivores are known to be important top-down regulators of plant
              | community composition in many ecosystems (Olff & Ritchie 1998, Parker et al.
              | 2006). In tropical forests, mammals are recognized as significant seedling predators
              | (Barone and Coley 1996). However their importance as herbivores in later stages of
              | plant recruitment has been less studied.
              |        One study in peninsular Malaysia found that native pigs (Sus scrofa) uproot or
              | snap 500 saplings per female pig in their reproductive nest building (Ickes et al. 2001).
              | Experimental exclusion of pigs resulted in sapling density increasing by 32 percent,
              | relative to open controls in just two years (Ickes et al. 2001). Lizcano (2006) excluded
              | large mammalian herbivores, including mountain tapir (Tapirus pinchaque) and
              | brocket deer (Mazama spp.), in montane tropical forests in Columbia and discovered a
              | 2-fold increase in understory plant biomass in two years.
              |        These two studies found higher species richness in exclosures, as may be
              | expected with higher stem densities, but no differences in species diversity indices.
              | The discrepancy between species richness and species diversity indices is explained by
              | the fact that species dominance often increases in mammal exclosures as well. The
              | positive and negative influences of increased species richness and dominance
              | respectively on the diversity index of an exclosure community can cancel each other
              | out, leading to the diversity index of an exclosure community being similar to that of a
              | control community.
              |        In other ecosystems, herbivore exclosure not only results in changes in plant
              | density and diversity, but also in plant functional trait composition. This is because,
              | although mammals are generalist herbivores relative to many insects, they still exhibit
              | diet preferences. In one temperate forest, browsers selected species lower in defense
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              | 
              | 
text          | compounds (e.g. leaf phenolics, condensed tannins, fiber, lignin) (Wardle et al. 2002),
              | and in a sub-humid grassland, grazers preferred taller-growing species (Diaz et al.
              | 2001).
              |          However, at the community level, evolutionary history and present day
              | intensity of herbivory interact with diet preferences to produce mixed effects on
              | functional trait composition.      In cases where species have evolved naïve of
              | mammalian herbivores, introduced browsers change species composition in favor of
              | species with lower average tissue quality (Wardle et al. 2002). The same occurs in
              | intensely grazed grasslands (Chaneton et al. 1988). In cases where plant communities
              | have evolved with mammalian herbivores, herbivory results in communities of species
              | with higher average tissue quality, both in the presence of native herbivores
              | (McNaughton 1985), as well as domestic herbivores that are not grazing at intensive
              | levels (Cingolani et al. 2002).
              |          In contrast to other ecosystems, mammals in tropical forests are perceived to
              | be relatively unimportant herbivores. Mammals are responsible for about one quarter
              | of all herbivory in tropical forests. As generalists, they are perceived to have less of a
              | selective influence in shaping plant community composition and plant anti-herbivore
              | defense than specialist invertebrate herbivores (Coley and Barone 2003). However,
              | tropical forest mammals are important seedling predators. Therefore, the primary aim
              | of this study was to test whether mammalian herbivores could indeed have effects on
              | plant functional trait composition in tropical forests similar to those seen in temperate
              | forests by influencing the composition of the younger cohorts of the plant community.
              |          We conducted this study in the Barro Colorado National Monument in central
              | Panama, where a terrestrial mammal exclosure experiment has been ongoing for the
              | past fifteen years (Royo & Carson 2005). We predicted that if mammalian herbivores
              | were important for determining sapling functional trait distributions, exclosure would
              | favor species that are faster growing (typically species with low wood density and
              | high specific leaf area, or SLA), less defended (low leaf toughness) and which have
              | higher nutrient leaves (higher leaf nitrogen). Our second goal was to evaluate the
              | hypothesis that differences in traits between treatments developed both as a
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              | 
              | 
text          | consequence of species turnover as well as increases in abundance of favored species
              | already common to both treatments.
              |        A final goal of this study was to examine whether the traits of the species
              | themselves changed intraspecifically with mammal exclusion. In temperate systems,
              | changes in mammalian herbivory induce changes in photosynthetic rates (Oleksyn et
              | al. 1998, Nabeshima et al. 2001), photosynthetic efficiency (Retuerto et al. 2004), leaf
              | toughness (Shimazaki & Miyashita 2002). In tropical savanna, megaherbivores
              | influence the concentrations of condensed tannins in Acacia (Ward & Young 2002).
              | Though herbivory rates in tropical forests are much higher overall in comparison to
              | temperate forests (Coley & Barone 1996), suggesting that perhaps constitutive anti-
              | herbivore defenses should be ubiquitous. However, several tropical species alter their
              | defense in response to herbivory, and it has been suggested that the lack of more
              | tropical examples of plasticity in defense are due to lack of study rather than
              | biological differences between temperate and tropical plants (Karban & Baldwin
              | 1997). We therefore examined whether the defense trait we examined, leaf toughness,
              | may decrease intraspecifically in response to mammal exclusion.
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              | 
title         | METHODS
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              | 
text          | Study sites. The forest in Central Panama surrounding Lake Gatun is semi-deciduous
              | moist forest. We conducted our experiment on Barro Colorado Island (BCI) and on
              | the Gigante Peninsula, within the Barro Colorado National Monument (BCNM). The
              | BCI has relatively high abundances of vertebrate herbivores affected by mammal
              | exclosure, compared to other Neotropical forests, including deer (Mazama Americana
              | and Odocoileus virginianus), collared peccary (Tayassu tajacu), agoutis (Dasyprocta
              | punctata), pacas (Agouti paca), rabbits (Silvilagus brasiliensis). This is due to a
              | combination of factors, including a lack of resident large felines on the island,
              | protection from poaching, and other environmental factors. Tapir (Tapirus bairdii) are
              | also present on BCI, but are rare.
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              | 
              | 
text          | Exclosure experimental design. Between late-1993 and mid-1994, eight pairs of
              | fenced, exclosure plots and open, control plots were established within the BCNM
              | (Royo & Carson 2005). Four pairs of plots are on (BCI) and the remaining four pairs
              | are on the mainland Gigante Penninsula. Fenced and unfenced plots are 30 m x 45 m
              | and are approximately 5 m apart. Exclosure fences are constructed of 12.7 x 12.7 cm
              | galvanized steel fencing 2.2 m tall and buried 0.25 m deep. A secondary 1.3 x 1.3 cm
              | mesh surrounds the lower 70 cm and also extends 0.25 m below ground. A 5-7 m
              | buffer zone at the plot edge, and bisecting the plot, allowed for access and the
              | avoidance of fence effects. Exclosures excluded the species mentioned above, but did
              | not exclude climbing mammals such as squirrels and spiny rats, nor did they exclude
              | arboreal mammals such as monkeys (Fig. 2.1). Monitoring data suggest that birds
              | were not altered by the exclosures, with the possible exception of tinamous (Fig. 2.1).
              | Though tortoises occur on our study site and are likely to be excluded by the fences,
              | they are small and rare, and generally not considered to have an effect on our study
              | results.
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text          | Plant censuses. In 1994 and 2003, all woody juveniles (“saplings”) taller than 40 cm
              | or larger than 3 mm diameter at 20 cm in height and not in the buffer zone were
              | identified, measured and marked.
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              | 
text          | Plant traits. We sampled leaves from up to six individual saplings of each tree
              | species in each of the eight plots occurring on BCI. Specific leaf area was measured
              | on shade leaves of saplings as the fresh lamina area divided by the mass of a whole
              | leaf with petiole after oven drying to constant mass at 60ºC (Cornelissen et al. 2003).
              | Leaf samples were dried at 65ºC, ground using a ball grinder, and analyzed on an
              | NA1500 elemental analyzer (Carlo Erba Instruments, Italy) for total N and C. Leaf
              | toughness was measured as the force necessary to punch a 3mm diameter hole the leaf
              | lamina with a force gauge, avoiding leaf veins to the extent possible (Sagers &Coley
              | 1995). Wright and colleagues (2007b) determined dry seed mass and adult tree wood
              | specific gravity (2010) for both free standing species and lianas in central Panama.
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              | 
              | 
text          | Analyses. Trait correlations were conducted to assess whether traits in this study were
              | orthogonal to one another, and thus likely to respond independently to herbivory.
              | Community mean trait values were calculated in three ways. First, we calculated the
              | grand means of the traits at the species level, and used these species means to
              | determine the average trait value of the species occurring in each plot. We next
              | repeated this analysis, but weighted the species’ trait means by species’ abundances in
              | the plots. Finally, we calculated species trait means separately for exclosure and open
              | communities, and recalculated the abundance-weighted plot means using these
              | treatment-specific species trait values.
              |        Linear mixed models were used to evaluate whether changes in community
              | mean trait values over time differed between treatments. Exclosure and time were
              | treated as fixed factors and the exclosure-control pair were treated as a random factor
              | nested within time. Our experiment tested for an exclosure-time interaction, and
              | significance values reported here refer to that interaction. All analyses were conducted
              | in R (R Development Core Team, 2008).
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title         | RESULTS
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text          | SPECIES TRAITS Functional traits were measured for 38.5-76.4 percent of species in
              | the experiment and 58.8-91.6 percent of stems in the experiment (Table 3.1). Traits
              | correlations were largely not significant, with the exceptions of SLA-leaf toughness
              | and SLA-leaf nitrogen (Table 3.2). However, the correlation coefficients for these two
              | relationships were still low (r2 = 0.325 and r2 = 0.231 respectively), and our results did
              | not show these trait pairs responding in a coordinated fashion (Fig. 3.1 & 3.2).
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              | 
text          |        TABLE 3.1. The number of species and stems for which traits were measured.
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text          |                                   No. Spp      % Spp      No. Stems      % Stems
              |                   Total            369           -         35,069           -
              |           Wood specific gravity    282          76.4       32,113         91.6
              |            Specific Leaf Area      154          41.7       23,342         66.6
              |             Leaf Toughness         152          41.2       23,322         66.5
              |              Leaf Nitrogen         142          38.5       20,633         58.8
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              | 
text          |        TABLE 3.2. R2 values for pair-wise correlations between species mean trait
              |        values evaluated in this study. The sign in parenthesis denotes whether the
              |        relationship was positive or negative. All correlations are significant (p <
              |        0.001).
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text          |                        Wood specific gravity        SLA         Toughness
              |              SLA            0.031 (-)
              |           Toughness         0.004 (-)             0.325 (-)
              |            Nitrogen          0.11 (-)             0.231 (+)       0.081 (-)
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              | 
              | 
              | 
text          | EFFECTS   OF   SPECIES OCCURRENCE In 1993, approximately 87 percent of species
              | occurring in the experiment were present in both treatments. In 2003, 75 percent of
              | species occurring in the experiment were present in both treatments. Therefore, when
              | we averaged the trait means of the species occurring in each plot, we observed that the
              | changes in plot trait means over time did not differ between treatments for any of the
              | traits measured (Fig. 3.1).
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              | 
              | 
              | 
text          |         Wood Specific Gravity (g/cm3)
              |                                         0.60                                                   22
              |                                                  1994          2003                                    1994        2003
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              | 
              | 
              | 
text          |                                                                         Mean SLA (mg/mm2)
              |                                         0.59                                                   21
              |                                         0.58                                                   20
              |                                         0.57                                                   19
              |                                         0.56                                                   18
              |                                         0.55                                                   17
              |                                         0.54                                                   16
              |                                                Open Excl    Open Excl                                Open Excl   Open Excl
              |                                          A           Treatment                                 B           Treatment
              |         Mean Leaf Toughness (g/mm2)
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              | 
              | 
              | 
text          |                                          34
              |                                                  1994          2003                            2.6     1994        2003
              |                                                                         Mean % Leaf Nitrogen
              |                                          33
              |                                                                                                2.4
              |                                          32
              |                                                                                                2.2
              |                                          31
              |                                                                                                2.0
              |                                          30
              |                                                                                                1.8
              |                                          29
              |                                                                                                1.6
              |                                          28
              |                                                Open Excl    Open Excl                                Open Excl   Open Excl
              |                                          C           Treatment                                 D           Treatment
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text          |        FIGURE 3.1. Changes in plot-level trait means, not weighted by species
              |        abundance, did not differ significantly between treatments for (A) wood
              |        density, (B) SLA, (C) leaf toughness or (D) leaf nitrogen.
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text          | EFFECTS             OF                    SPECIES ABUNDANCE        Stem densities increased by 46% in exclosures
              | from 1994 to 2003, but did not increase in open plots (data not shown). When we
              | averaged the trait means of the species occurring in each plot, and weighted traits by
              | species abundance, we did observe differences between treatments for some traits.
              | We predicted that exclosures would favor species with lower wood density, lower
              | SLA, lower leaf toughness, and higher leaf nitrogen. We did not see significant
              | differences between treatments in wood density (Fig. 3.2A) or SLA (Fig. 3.2B).
              | However, changes in leaf toughness (Fig. 3.2C) and leaf nitrogen (Fig. 3.D) over time
              | were significantly different between treatments. Consistent with our expectations,
              | exclosures had lower community mean leaf toughness and higher community mean
meta          |                                                                                                                                  59
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              | 
              | 
text          | leaf nitrogen in 2003, relative to open plots. However these differences did not exist
              | when the experiment was initiated in 1994 (Fig. 3.2 C & D).
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              | 
              | 
text          |         Wood Specific Gravity (g/cm3)
              |                                         0.60                                                  24
              |                                                  1994        2003                                     1994         2003
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              | 
              | 
              | 
text          |                                                                        Mean SLA (mg/mm2)
              |                                         0.59                                                  22
              |                                         0.58                                                  20
              |                                         0.57                                                  18
              |                                         0.56                                                  16
              |                                         0.55                                                  14
              |                                         0.54                                                  12
              |                                                Open Excl   Open Excl                                Open Excl    Open Excl
              |                                          A           Treatment                                B           Treatment
              |         Mean Leaf Toughness (g/mm3)
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              | 
              | 
              | 
text          |                                          38                                                   2.6
              |                                                  1994        2003      Mean % Leaf Nitrogen           1994         2003
              |                                          36                                                   2.4
              |                                                                  *                                                    *
              |                                          34                                                   2.2
              |                                          32                                                   2.0
              |                                          30                                                   1.8
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text          |                                          28                                                   1.6
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text          |                                          26                                                   1.4
              |                                                Open Excl   Open Excl                                Open Excl    Open Excl
              |                                          C           Treatment                                D           Treatment
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              | 
text          |        FIGURE 3.2. Changes in abundance-weighted, plot-level trait means did not
              |        differ significantly between treatments for (A) wood density or (B) SLA, but
              |        did differ significantly between treatments for (C) leaf toughness and (D) leaf
              |        nitrogen. (* p = 0.06 , time x treatment interaction)
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              | 
text          | INTRASPECIFIC DIFFERENCES IN                               LEAF TRAITS                        Because we sampled leaf traits in both
              | open and exclosure plots, we could examine how intraspecific differences in trait
              | means contributed to the differences between treatments at the community level. For
              | one trait, leaf toughness, we found that determining species trait means separately for
              | open and exclosure treatments, and using those treatment-specific species trait means
              | to calculate plot-level means, resulted in an enhanced difference between treatments at
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              | 
              | 
text          | the plot-level in the later time point (Fig. 3.3), relative to using grand trait means for
              | species (Fig. 3.2C).
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text          |                                                       38
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              | 
              | 
text          |                         Mean Leaf Toughness (g/mm2)
              |                                                              1994               2003
              |                                                       36
              |                                                       34                         *
              |                                                       32
              |                                                       30
              |                                                       28
              |                                                       26
              |                                                            Open   Excl     Open Excl
              |                                                                     Treatment
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text          |        FIGURE 3.3. Intraspecific differences in species’ mean leaf toughness between
              |        open and exclosure plots increase the difference in treatment-level mean leaf
              |        toughness in 2003. (* p = 0.004, time x treatment interaction)
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text          |        For species having at least two leaf samples from each treatment type, 61.8%
              | of species had lower leaf toughnesses in exclosures relative to controls (binomial test,
              | N = 76, p = 0.025). This bias was even stronger when the sample was limited to
              | species with treatment mean toughnesses based on at least eight leaf samples, with
              | 73.9% of species having lower leaf toughnesses in exclosures (binomial test, N = 23,
              | p = 0.017).
              |        Because sample sizes among species and between treatments was unbalanced,
              | a MANOVA approach could not be taken to assess whether treatment means within a
              | species were significantly different. Therefore, using the latter subset of species
              | above, a two-way ANOVA was applied. The association of exclosure treatment with
              | lower mean leaf toughness with species was also significant using this approach
              | (Table 3.3).
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              | 
              | 
text          |            TABLE 3.3. Effect of species and exclosure on variation in leaf
              |            toughness. N = 23 species, each of which had at least eight leaf
              |            toughness samples from each of the two treatment types.
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text          |             Effect                  df      SS      MS        F        p
              |             Species                 22    207.4    9.425    165.2   < 0.001
              |             Exclosure               1     0.305    0.305    5.352    0.021
              |             Species x Exclosure     22    1.292    0.059    1.029    0.425
              |             Residuals              604    34.467   0.057
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              | 
              | 
title         | DISCUSSION
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text          | Regulation of plant functional trait composition by mammalian herbivores
              | In this study, we demonstrate that terrestrial mammals influence understory functional
              | trait distributions in tropical forests. They do so primarily by suppressing populations
              | of species with traits that are correlated with high nutrition and low defense.
              | Consistent with our predictions that reduced herbivory should favor species with low
              | defense and high nutrient content, community mean leaf toughness decreased over
              | time in exclosures over time (Fig. 3.2C), and community mean leaf nitrogen increased
              | in exclosures over time (Fig 3.2D), while open control plots did not show equivalent
              | changes.
              |        Wood density is associated with seedling survival in the presence of herbivores
              | in this forest (Alvarez-Claire & Kitajima 2007, 2009). Browsers and grazers have also
              | been shown to select species with higher SLA in other systems (Wardle et al. 2002,
              | Cingolani et al. 2002).     However, neither of these traits changed in response to
              | mammal exclosure. This could be because, at the sapling stage in tropical forests, the
              | low light conditions of the forest understory also favor low SLA, high wood density
              | species and perhaps this environmental factor constrains the community response to
              | herbivory with respect to those traits.
              |        We did not find that changes in functional traits at the community-level were
              | the result of divergences in species presence-absence between exclosure and open
              | plots. The sapling community established prior to the imposition of the exclosure
              | treatments, and therefore two treatments started out with very similar communities.
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              | 
              | 
text          | Over longer time scales, competitively dominant species may outcompete less
              | competitive species in the exclosure treatment, resulting in lower species richness,
              | particularly of species which are better defended but slower growing. However, we
              | did not observe decreases in species richness in the time-frame of this experiment
              | (data not shown).
              |        Seed and seedling predators are also excluded from the exclosure communities.
              | Therefore, it is reasonable to question whether the effects we observed are due
              | exclusively to herbivore exclusion. Two lines of evidence allow us to attribute our
              | results to herbivores. First, long-term studies of seedling growth in central Panama
              | suggest that all individuals in this size class established before the experimental
              | treatments were imposed (S.J. Wright, pers. comm.). Therefore, saplings in both
              | treatments should have been exposed to the same seed and seedling predation agents.
              |        Consistent with the assumption that saplings established prior to exclusion of
              | seed and seedling predators, community mean seed mass does not differ between
              | treatments for the sapling community (data not shown). This is in contrast to the
              | seedlings in the exclosure communities, which did establish under conditions of seed
              | and seedling predator exclusion, and as a result have higher community mean seed
              | mass than seedlings in open control communities (Fig. 2.4).
              |        These two lines of evidence suggest that exclusion of seed and seedling
              | predators are not responsible for the exclosure effects observed in the sapling
              | community, leaving only herbivory as a possible explanation.
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              | 
title         | Intraspecific differences in leaf toughness
text          | The majority of species in the experiment showed lower mean leaf toughness inside
              | the exclosure, relative to open plots. When these intraspecific differences in species
              | leaf toughness were accounted for (Fig. 3.3), treatment differences in plot level leaf
              | toughness in 2003 were 66 percent larger than when a grand mean for the species leaf
              | toughness was applied (Fig. 3.2C). This result suggests that in the case of leaf
              | toughness, the trait values measured for juvenile tropical plants may vary with the
              | degree of herbivory experienced.
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              | 
              | 
text          |        There are several possible explanations for the intraspecific divergence in leaf
              | toughness. First, it is possible that, within species, genotype or environment produces
              | variation in leaf toughness, and individuals with lower leaf toughness survive at a
              | lower rate in open plots than in exclosures . Support for this mechanism can be found
              | in studies of insect herbivory on plant genotypes which differ in their expression of
              | qualitative defense traits (Kessler & Baldwin, 2001, Silfer et al. 2009).
              |        An alternative explanation is that plants are relaxing their investment in
              | mechanical defenses when they no longer experience mammalian herbivory.
              | Hundreds of plant species are known to increase investment in defense when exposed
              | to herbivory, and subsequently attenuate that defense when herbivory levels are lower
              | (Karban & Baldwin 1997).           However few studies have documented reduced
              | investment in defense upon reduction of mammalian herbivory.                   In Acacia
              | drepanolobium decreases in spine length or spinescence are detectable after 22 months
              | (Young & Okello 1998), decreases in condensed tannin concentrations are detectable
              | after 24-36 months (Ward & Young 2002) and reduced investment in indirect defenses
              | occur within several years (Huntzinger et al. 2004).
              |        Regardless of the mechanism, the fact that mammalian herbivores may play a
              | role in altering leaf toughness intraspecifically in tropical plants is unexpected. Insects
              | are thought to be responsible for three quarters of herbivory in tropical forests, and
              | also the source of the strongest selection pressures plants receive to develop anti-
              | herbivore defenses in this system (Barone & Coley 2002). The experimental plots in
              | which we measured leaf toughness did not manipulate insects, and it is plausible that
              | plants in both treatments could have experience high rates of invertebrate herbivory,
              | and therefore shown no attenuation in defense traits.        Yet, it appears that insect
              | herbivores could not compensate for mammalian herbivores in maintaining high
              | intraspecific leaf toughness when mammals were excluded.
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              | 
title         | Implications for tropical defaunation
text          |        In many temperate forests, populations of native or introduced large
              | mammalian herbivores are not regulated in a top-down fashion by predators. As a
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              | 
              | 
text          | result, these communities currently experience intense levels of herbivory, low rates of
              | plant recruitment and often decreases in species richness and diversity (Wardle et al.
              | 2002, Rooney 2001).        However, tropical forests are undergoing the opposite
              | perturbation. Throughout the tropics, mammalian herbivores are being unsustainably
              | hunted (Peres & Palacios 2007, Corlett 2007, Fa & Brown 2009). Preferred game
              | species of animals are often large-bodied herbivores, such as elephants, tapir, pigs,
              | peccaries and deer.
              |        Understanding how and why such perturbations in herbivore abundance alter
              | plant species diversity and functional composition will help conservation biologists
              | identify potential interventions to conserve plant species threatened indirectly by
              | defaunation.    However, because most studies examining changes in functional
              | diversity have been conducted in temperate forests, where the perturbation
              | experienced by plant communities is increased rates of herbivory, little empirical data
              | exists with which to evaluate how tropical forests may respond to decreased rates of
              | herbivory by native herbivores as a consequence of defaunation.
              |        The biomass of terrestrial mammalian herbivores in tropical forests is quite
              | low, relative to other ecosystems (Bodmer 1989, Leigh et al. 1982). In addition,
              | insects are thought to account for approximately 75 percent of overall herbivory in
              | tropical forests. Taken together, these data might suggest that observed reductions in
              | terrestrial mammalian herbivore populations in tropical forests may not have large
              | impacts on sapling community composition.           However, this study demonstrates
              | reduced herbivory as a consequence of tropical defaunation is likely to cause an
              | increase in dominance of sapling species with higher leaf nitrogen and lower leaf
              | toughness. Leaves with higher leaf nitrogen and lower concentrations of defense
              | compounds typically have higher decomposition rates. Therefore, it is conceivable
              | that if changes in the sapling community propagate to alter canopy composition,
              | defaunation may alter nutrient cycling in tropical forests.
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              | 
              | 
title         | ACKNOWLEDGEMENTS
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text          | D. Ackerly, L. Curran, R. Dirzo and P. Vitousek provided constructive criticism which
              | improved this work. The Smithsonian Tropical Research Institute granted permission
              | to conduct this work, and provided logistical support. D. Turner provided assistance
              | with leaf nitrogen analysis. J. Wright provided seed mass and wood density data.
              | Many thanks go to L. Jimenez, C. Sarmiento, S. Rebellon, A. Calderón, R.
              | Bethancourt for help in the field and lab. A. Hernandez and O. Valdes provided
              | indispensible help with species identification. NSF DEB-0808338, the Theresa Heinz
              | Environmental Scholars program, and the STRI short-term fellowship program
              | provided support to E. Kurten.
              | 66   CHAPTER 3: EFFECTS OF MAMMALIAN HERBIVORES ON SAPLING TRAITS
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              | 
              | 
              | 
title         | Chapter 4
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text          | Hunting does not alter seed
              | predation rates as a function of seed
              | size in a Neotropical forest
              | Erin L. Kurten
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title         | ABSTRACT
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text          | This study tested the hypothesis that vertebrate seed predation rates vary with seed
              | size and with hunting intensity in tropical forests, corresponding to direct impacts of
              | hunting on vertebrate species of differing size classes. Seed fate of seeds from species
              | with mean fresh seed masses ranging from 0.002 to 62.4 g was compared between a
              | protected and nearby hunted forest in central Panama. Transect survey data verified
              | that higher hunting intensity corresponded with lower abundances of key mammalian
              | seed predators. Seed arrays of a subset of species were monitored with camera traps
              | to verify the identities of animals responsible for seed removal. In this system, there
              | was only weak support for a relationship between seed predation rates and seed size,
              | and no evidence that this relationship changed at high hunting intensity. There was
              | also no evidence that seed predator body size varied with seed size, as agoutis
              | (Dasyprocta punctata) were responsible for most of the verified removal for five plant
              | species examined, ranging from 1.95 to 62.4 g in fresh seed mass.
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              | 
              | 
title         | INTRODUCTION
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text          | Overharvesting of bushmeat is a pervasive threat to biodiversity across the tropics (Fa
              | & Peres 2001, Peres & Palacios 2007, Corlett 2007). This defaunation not only
              | directly lowers vertebrate abundance in hunted forests, but initiates trophic cascades
              | which perturb the plant, insect, and pathogen communities as well. Preferred game
              | species of animals are usually large-bodied vertebrates, such as ateline monkeys, tapir,
              | peccary and deer, as well as large birds, and in some cases reptiles, in the context of
              | Neotropical forests. Understanding how and why such cascading perturbations alter
              | species diversity and functional composition in the plant community is important for
              | understanding the role mammals play in maintaining the diversity of tropical forests,
              | as well as identify potential interventions to conserve plant species threatened by the
              | negative indirect effects of defaunation.
              |        Several studies have documented reduced seed dispersal as a consequence of
              | hunting in tropical forests, particularly for larger-seed species (e.g. Wright et al. 2000,
              | Guariguata et al. 2000, Guariguata et al. 2002, Galetti et al. 2006, Wang et al. 2007,
              | Brodie et al. 2009, Fadini et al. 2009, Holbrook & Loiselle 2009). These studies
              | suggest that reduced dispersal should result in reduced recruitment of large-seeded
              | species, in particular those that rely on large-bodied mammals vulnerable to hunting
              | for their seed dispersal (Peres & van Roosmalen 2002, Nuñez-Iturri et al. 2008,
              | Terborgh et al. 2008).
              |        However, in most cases, reduced dispersal due to hunting has not been
              | explicitly linked to subsequent reductions in seedling recruitment. While one study
              | modeled the potential reduction in seedling recruitment, based on estimates of reduced
              | dispersal to and differential survival in different microhabitats (Brodie et al. 2009),
              | only one set of studies of which I am aware measured seed dispersal, seed predation,
              | and seedling recruitment for the same species in both protected and hunted sites
              | (Wright et al. 2000, Wright & Duber 2001). Wright and colleagues (2000, 2001)
              | focused on two large-seeded palm species, members of genera which are widespread
              | in the Neotropics. They found seed dispersal to be indeed reduced, and seedling
              | densities near parent trees to be higher, as one would predict to be associated with
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              | 
              | 
text          | hunting. However, contrary to what has been hypothesized in the seed dispersal
              | literature, recruitment of Attalea and Astrocaryum palms was actually higher in the
              | hunted sites (Wright et al. 2000, 20001). The reason for this unexpected increase in
              | recruitment was that hunting reduced the intensity of vertebrate seed predation, and
              | this reduction was not fully compensated for by invertebrates.     (Cramer et al. 2003)
              | suggested a similar reduction in seed predation was responsible for higher recruitment
              | of the African species Balanites wilsoniana in defaunated sites, despite lower dispersal
              | by elephants, however seed predation rates were never measured (Babweteera et al.
              | 2007).
              |          It is clear from this example that a better understanding of the consequences of
              | hunting for seed predation is necessary for providing context to the studies
              | documenting reduced seed dispersal. In studies which have measured seed predation
              | in sites with differing intensities of hunting, rates of vertebrate seed predation have
              | often been lower in hunted sites (Terborgh & Wright 1994, Wright et al. 2000, Wright
              | & Duber 2001, Guariguata 2000, Beckman & Muller-Landau 2007, but see Roldán &
              | Simonetti 2001).
              |          Even less clear is how perturbations in seed predation rates as a consequence
              | of hunting may vary with seed size. Because larger-seeded species are expected to
              | disproportionately experience reduced seed dispersal, understanding how seed
              | predation changes with hunting across a range of seed sizes is important for
              | understanding whether or not the potentially negative demographic consequences of
              | reduced seed dispersal of larger-seeded species is intensified, maintained, or
              | compensated for by alterations in seed predation across species (Stoner et al. 2007).
              | However, most studies which have measured seed predation rates under various
              | hunting regimes have focused on one or two plant species (e.g. Terborgh & Wright
              | 1994, Wright et al. 2000, Roldán & Simonetti 2001, Wright & Duber 2001, Galetti et
              | al. 2006, Beckman & Muller-Landau 2007, Donatti et al. 2009). Due to the variation
              | in location, mammal community composition, and degree of defaunation in the sites
              | studied, these data cannot be directly compared to assess how seed predation rates
              | change with defaunation intensity as a function of seed size.           Guariguata and
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              | 
              | 
text          | colleagues (2000) measured seed predation rates of seven species, but focused
              | primarily on small-seeded timber species. .
              |        In 2007, Dirzo and colleagues published a model of how vertebrate seed
              | predation could be expected to vary with seed size and intensity of vertebrate
              | defaunation in tropical forests (Fig. 4.1). At low levels of hunting, vulnerable, large-
              | bodied animals drastically decrease in abundance or become locally extirpated. In
              | response to this competitive release, as well as a likely reduction in predation by
              | felines, medium-sized seed predators initially become more abundant, until they
              | become the primary game species at moderate levels of hunting. At the highest
              | intensities of defaunation, even medium-sized seed predators have become rare. Small
              | rodents increase steadily with increasing hunting intensity, as they experience a
              | reduction in competition and predation.
              |        In this model, predation intensity of larger-seeded species mirrors the changes
              | in abundance of medium-bodied seed predators (e.g. 4-20 kg body mass in
              | Neotropical communities), while predation of smaller-seeded species increases as
              | small bodied seed predator (< 1 kg) biomass increases. As a result, the relative
              | proportion of larger and smaller seeds comprising the seedling bank is expected to
              | shift as defaunation intensity increases. This model was important for clarifying how
              | seed predation is likely to vary by seed-size, and how this relationship is dependent
              | upon the defaunation context.
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              | 
text          |                                                       Large vertebrates
              |                                         A
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              | 
text          |                Seed predator Biomass
              |                                                       Mid-sized vertbrates
              |                                                       Small rodents
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text          |                                              BCI
              |                                                                  PNS
              |                                                                                                          C           No Def.
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              | 
              | 
              | 
text          |                                                                               Seed predation Intensity
              |                                                                                                                     High Def.
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              | 
              | 
              | 
text          |                                         B                     Large Seeds
              |              Seed predation Intensity
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              | 
text          |                                                               Small Seeds
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              | 
              | 
              | 
text          |                                                                                                          Small                  La rge
              |                                                                                                                  Seed Size
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              | 
              | 
text          |                                 None               Moderate            High
              |                                             Defaunation Intensity
              |        FIGURE 4.1. Model of how seed predation should vary with seed
              |        mass as a function of defaunation intensity in a Neotropical forest
              |        (modified from Dirzo et al. 2007). (A) Changes in large, medium and
              |        small vertebrate seed predator abundance with increasing defaunation
              |        intensity. The approximate positions of BCI and PNS along the
              |        defaunation gradient shown here are based on mammal transect
              |        surveys. (B) Seed predation intensity of large and small seeded species
              |        on a biomass basis is correlated with the abundance of medium- and
              |        small-bodied seed predators respectively. (C) As defaunation
              |        intensifies, the relationship between seed predation rates and seed size
              |        goes from positive to negative.
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text          |        With this study, I aimed to test several assumptions and hypotheses inherent in
              | this model. The first assumption I tested was that larger-seeded species experience
              | higher seed predation intensity than smaller seeded species at all but the highest levels
              | of defaunation intensity. The second assumption of the model I tested was that larger-
              | seeded species tend to be consumed by large- and medium-bodied vertebrates.
              | Likewise, smaller-seeded species tend to be consumed by smaller-bodied vertebrates.
              | A third hypothesis implicit in the model is that at high levels of defaunation intensity,
              | where the number of large- and medium-bodied vertebrates is highly reduced, larger-
              | seeded species experience reduced seed predation, relative to less defaunated sites. A
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              | 
              | 
text          | fourth prediction of the model is that smaller-seeded species experience increased seed
              | predation as defaunation intensity increases, as populations of small bodied vertebrates
              | increase in response to competitive release and reduced predation. There is a great
              | interest in determining the extent to which other vertebrates or natural enemies can
              | compensate for the loss of a primary seed predator.
              |        To test these hypotheses, seeds of 13 species spanning the range of 0.002 to
              | 64.2 g mean fresh seed mass were monitored in arrays in both a protected forest and a
              | nearby hunted forest. Fate of seeds was monitored for four weeks. To           examine
              | whether larger- and smaller-seeded species indeed had larger- and smaller-bodied
              | seed predators respectively, the seed arrays on BCI were monitored with camera traps
              | for five species ranging from 1.95 to 64.2 g fresh mean seed mass for one week, and
              | the the agents of seed removal were recorded.
              |        To assess whether other vertebrates might compensate for the loss of a
              | principle seed predator, I monitored two large-seeded palm species with camera traps
              | in both sites. This allowed me to determine if and how the species of vertebrate seed
              | disperser differed between the protected and hunted sites, in particular if smaller
              | vertebrates compensated for the removal of larger vertebrates. I also recorded the
              | source of mortality for all species when seeds were killed by invertebrates and
              | pathogens, to examine whether those agents could also compensate for the loss of
              | larger bodied seed predators.
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              | 
title         | METHODS
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              | 
text          | Study sites. The forest in Central Panama surrounding Lake Gatun is semi-deciduous
              | moist forest. I examined the effects of defaunation by hunting by comparing protected
              | and hunted forests in this area (Fig. 4.2). Barro Colorado Island (BCI) was chosen as
              | the protected forest site, and could be regarded as a moderately defaunated site. Due
              | to its size (15 km2), the island no longer supports white-lipped peccary, and has
              | visiting, rather than resident, jaguar (Panthera onca) and puma (Puma concolor).
              | Other large mammals, such as tapir (Tapirus bairdii) and spider monkeys (Ateles
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              | 
              | 
text          | geoffroyi), were locally extirpated and historically reintroduced (Enders 1939,
              | Terwilliger 1978, Milton & Hopkins 2005). However today, activity of poachers is
              | virtually nonexistent on BCI due to the monitoring by forest guards and Panamanian
              | police. The last confirmed incident of poaching on BCI occurred in 1989 (Wright et
              | al. 2007).   Consistent with an absence of poachers, researchers on BCI do not
              | encounter evidence of hunting, and wildlife is common to see.
              |        Adjacent to the Barro Colorado National Monument (BCNM) is the Parque
              | Nacional Soberanía (PNS). PNS is a protected area, however the region of the park in
              | which the study was conducted is not actively patrolled. This is due to both fewer
              | forest guards at the park, a lack of vehicles to access the study area, which is more
              | than 20 km from the park headquarters. Consistent with a lack of protection, various
              | evidence of hunting activity was encountered while conducting this study, including
              | spent shells, campfires, litter, gun shots, hunting dogs, experimental vandalism, and in
              | one case, encountering a hunting party.
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              | 
              | 
text          |                         BCNM
              |                         PNS
              |                         trails
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              | 
              | 
              | 
text          |                        N
              |                                                 0             5 km
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              | 
text          |        FIGURE 4.2. Map of Lake Gatun study area in central Panama. Seed
              |        predation experiments were conducted in areas demarcated by trails.
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              | 
              | 
text          | Mammal census. Diurnal mammal transect surveys were conducted from mid-August
              | to mid-December in 2008. Once per week in each site, an observer surveyed a 5 km
              | transect between the hours of 6:30 AM and 11:30 AM, walking at a speed of 1 km/hr.
              | Surveys were not conducted during rain. Observers recorded the species and age
              | (adult or juvenile) of all mammals sighted, and measured initial detection distance
              | with a Nikon ProStaff 550 range finder (Nikon Inc., Melville, NY). Because of the
              | time and difficulty involved in counting individuals in troupes of primates, these
              | species were recorded in units of groups. Because most species had few observations
              | in PNS, and the parameters that density estimators require could not be accurately
              | estimated for that site, I report animal abundances (individuals/km or groups/km),
              | rather than densities.
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              | 
text          |      TABLE 4.1. Mean fresh seed masses of study species. BCI and PNS
              |      columns denotes species used in each site. Most species are free standing
              |      growth forms. C. turczanninowii and T. richardii are lianas.
              |        Species                       Family          Seed mass (g)   BCI    PNS
              |        Apeiba tibourbou              Tiliaceae          0.0057         X      X
              |        Protium tenuifolium           Burseraceae         0.18          X
              |        Cupania latifolia             Sapindaceae         0.19                 X
              |        Chamaedorea tepejilote        Arecaceae           0.49          X      X
              |        Connorus turczanninowii       Conneraceae         0.49          X
              |        Thevetia ahouai               Apocynaceae         1.11                 X
              |        Oneocarpus mapora             Arecaceae           1.95          X
              |        Virola surinamensis           Myristicaeae        2.43          X
              |        Calophyllum longifolium       Clusiaceae          5.48          X
              |        Astrocaryum standleyanum      Arecaceae           9.84          X      X
              |        Gustavia superb               Lecythidaceae       16.0          X
              |        Attalea butyracea             Arecaceae           16.2          X      X
              |        Tontelea richardii            Celastraceae        64.2          X
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              | 
text          | Seed preparation. Thirteen woody plant species ranging from 0.002 to 64.2 g mean
              | fresh seed mass were selected for this study (Table 4.1), representing 76 % of the
              | range in fresh seed mass for this area on a log scale. While these species are common
              | to both BCI and PNS, heavy insect and/or pathogen infestation of some species in
              | PNS prevented collection of viable seeds in this site. Because of protected area rules,
              | seeds could not be moved between sites. Therefore, eleven species were examined on
              | BCI and six species in PNS, with four species common to both sites, spanning almost
              | the entire range of seed size in the study.
              |           Seeds appearing rotten, insect-damaged, or otherwise unviable were not
              | included in the experiment. To remove confounding effects of differing seed pulps, all
              | seeds were cleaned of pulp or mucilage. After pulp removal, mass, width and length
              | were measured for seeds of all species but Apeiba tibourbou. Apeiba seed mass for
              | BCI was previously recorded (Wright et al. 2007). A thread was attached to all but
              | the smallest seeds (A. tibourbou and P. tenuifolium), so that I could recover the seeds
              | and record their fate.
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              | 
              | 
text          | Seed predation experiment. A randomized block design was used to compare seed
              | predation rates in the two sites.    Within each forest, six blocks were delineated.
              | Within each block, each species was placed on the forest floor in an array of 6-8 seeds
              | in a different random location. For G. superba on BCI and C. tepelijote in PNS, only
              | four arrays were used, as few seeds unattacked by insects were available. Because A.
              | tibourbou and P. tenuifolium, were small and not marked with thread, these species
              | were set out in shallow mesh trays with 6-8 seeds per tray. Data reported here is from
              | a total of 732 seeds.
              |        Experiments were conducted between mid-July and mid-September 2009.
              | Seeds were monitored for four weeks, during which seed fate and agent of mortality
              | were recorded. Classes of seed fate were: unmoved (intact), cached, moved but not
              | buried (intact), predated by vertebrates, predated by insects, and killed by pathogens.
              | Seeds which were removed and only the thread recovered were presumed predated. .
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              | 
text          | Assessment of seed predator identity. The arrays of 5 species with masses ~2 g or
              | larger were monitored with Reconyx RC-55 infrared cameras on BCI for the first
              | week. Only half of the Virola arrays were monitored due to camera limitation. In
              | addition, the arrays of two of the larger-seeded species, A. standleyanum and A.
              | butyracea were monitored in PNS. More species were not monitored in PNS due to
              | concerns over equipment loss. As a conservative assignment of seed predator identity,
              | the species of seed predator was only recorded when the removal of a marked seed
              | was clearly visible in the image. Instances of probable seed removal, but in which
              | camera angle, position of the animal, or clarity of the image prevented a clear
              | determination of the event, were not assigned to a particular animal species.
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              | 
text          | Analyses. The relationships between mean seed mass and mean seed mortality in the
              | two sites was assessed via an ANCOVA, with site as the fixed factor and log-
              | transformed mean seed mass as the covariate. Differences in seed caching rates
              | between sites were evaluated with a t-test for both palm species. All analyses were
              | conducted in R (R Development Core Team, 2008).
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              | 
              | 
title         | RESULTS
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text          | Mammal census. Diurnal mammal transect surveys, conducted from mid-August to
              | mid-December in 2008, verified differences in degree of defaunation between BCI and
              | PNS, which approximately correspond to moderate and intense degrees of defaunation
              | respectively (Fig. 4.3.)
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              | 
title         |                     Medium-bodied
              |                   Dasyprocta punctata
              |                   Cebus capuchinus
              |                   Alouatta palliata
              |         Species
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              | 
              | 
              | 
text          |                     Large-bodied
              |                   Ateles geoffroyi ‡
              |                   Mazama americana
              |                   Odocoileus virginianus *
              |                   Pecari tajacu
              |                                                                                     BCI
              |                   Tapirus bairdii ‡                                                 PNS
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text          |                                              0.0   0.2    0.4       0.6       0.8         1.0
              |                                                          Individuals per km
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              | 
text          |        FIGURE 4.3. Animal abundances in BCI and PNS as assessed by trail
              |        census in 2008. Above are species of medium body size known to
              |        maintain or increase their population density with moderate hunting,
              |        but decrease with intense hunting (Peres and Palacios 2007). Below
              |        are large-bodied animals that have been historically present in the sites
              |        and which are known to be most vulnerable to hunting. At both BCI
              |        and PNS, most large-bodied mamals are rare or locally extinct.
              |        However, medium-sized mammals are highly abundant in BCI,
              |        whereas they are also quite rare in PNS, indicating the two sites are
              |        moderately and intensely hunted, respectively. † locally extirpated in
              |        PNS; ‡ locally extirpated in BCI, reintroduced, and currently rare;
              |        *present and rare at both sites, not observed in this census.
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              | 
text          | Seed predation intensity. Relationships between seed mortality and seed size were
              | evaluated by ANCOVA, with site being a fixed factor.                  Seed mortality over all
              | species, when all sources of mortality were pooled, was not correlated with seed mass
              | (F1,13 = 1.47, p = 0.25), and this did not differ between sites (F1,13 = 0.69, p = 0.42)
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              | 
              | 
text          | (Fig. 4.4a). For the subset of species with verified vertebrate seed predation , there
              | was not significant (F1,12 = 1.45, p = 0.25) (Fig 4.4b) Apeiba, which appeared to have
              | no vertebrate seed predators at either site. was excluded from the model. ). Also,
              | contrary to the model (Fig. 4.1), the effect of site was not signficant (F1,13 = 0.11, p =
              | 0.74) (Fig. 4.4b).                             Mortality caused by invertebrates and fungal pathogens was
              | negatively correlated with seed mass across all species (F1,13 = 21.1, p > 0.001).
              | Again, this relationship did not differ by site (F1,13 = 0.19, p = 0.67).
              |                                                                          Mortality by
              |                                             All Sources                  Vertebrates        Invertebrates & pathogens
              |  Proportion seeds killed
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              | 
              | 
              | 
text          |                            1.0
              |                                                            A                            B                          C
              |                            0.8
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text          |                            0.6
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text          |                            0.4
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text          |                            0.2
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text          |                            0.0
              |                                  -6    -4     -2   0   2   4   -6   -4     -2   0   2   4 -6    -4   -2   0   2    4
              |                                       BCI                            Log(Seed mass)
              |                                       PNS
              |                            FIGURE 4.4. Seed predation rates as a function of seed size on BCI and in PNS.
              |                            (A) Across all species there was a negative, but non-significant, relationship
              |                            between seed mass and seed mortality. (B) Seed mass and vertebrate seed
              |                            predation were not correlated when analysis was restricted to species with verified
              |                            vertebrate seed predators. (Points for Apeiba slightly offset for visualization.) (C)
              |                            Seed mass and seed mortality by invertebrates and fungal pathogens were
              |                            negatively correlated (includes Apeiba). No differences were observed between
              |                            sites.
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              | 
text          |                            Scatter-hoarding rodents do not just predate seeds. For two of the large seeded
              | palms, seed caching by scatter-hoarding rodents is critical for escaping seed predation
              | by bruchid beetles. I predicted that caching of Attelea and Astrocaryum would be
              | lower in the hunted site, as the primary seed caching agent, the agouti (Dasyprocta
              | punctata), was less abundant at that site (Fig. 4.3), unless compensated for by
              | squirrels. Contrary to this prediction, the number of seeds cached did not differ
              | between sites for either species (Attalea: t = -0.129, p = 0.55, one-tailed test;
              | Astrocaryum: t = -0.412, p = 0.66, one-tailed test). (Fig. 4.5). This equivalence
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              | 
text          | between sites appears not to be due compensation by squirrels, in as far as every seed
              | caching event for which the agent could be verified by camera trap was committed by
              | an agouti (data not shown).
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              | 
text          |                                     2.5
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              | 
text          |                                     2.0
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text          |                      Seeds Cached
              |                                     1.5
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              | 
text          |                                     1.0
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              | 
text          |                                     0.5
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              | 
text          |                                     0.0
              |                                           BCI   PNS           BCI   PNS
              |                                            Attalea           Astrocaryum
              |                                                  Sites by Species
              |         FIGURE 4.5. Number of seeds cached per array of eight seeds for two
              |         large seeded palms did not differ between BCI and PNS.
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text          | Seed predator identity. Camera trap monitoring of seeds in the first week on BCI
              | revealed D. punctata, to be the primary agent of seed removal for all species (Fig.
              | 4.6).   Seed removal by spiny rats (Proechimys steerei) and squirrels (Sciurus
              | granatensis) accounted for little of the seed predation and varied by plant species (Fig.
              | 4.6). Data from BCI do not appear support the hypothesis that seed predator size is
              | correlated with seed size.
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              | 
text          |                     50                                                                                50
              |                                                                         Not taken
              |                                                                         Unknown
              |                                                                         Squirrel
              |                                                                         Spiny rat                     40
              |                     40                                                  Agouti
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              | 
              | 
              | 
text          |                                                                                     Number of seeds
              |   Number of seeds
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              | 
              | 
              | 
text          |                                                                                                       30
              |                     30
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              | 
text          |                                                                                                       20
              |                     20
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              | 
text          |                                                                                                       10
              |                     10
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text          |                                                                                                        0
              |                     0
              |                                                                                                            BCI     PNS     BCI      PNS
              |                          Oneocarpus   Virola   Astrocaryum   Attalea   Tontelea
              |                                                                                                              Attalea        Astrocaryum
              |                                       Species ranked by mass                                                     Sites by Species
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              | 
text          |                           FIGURE 4.6. Identity of species removing seeds during first week of
              |                           experiment. (Left) On BCI five species ranging in mass from 1.95 g
              |                           (Oneocarpus) to 64.2 g (Tontelea) were primarily removed by
              |                           agoutis, and showed no relationship between seed size and seed
              |                           predator body size. (Right) Seed removal of large-seeded palms at
              |                           BCI and PNS. Removal of Attelea was higher in PNS, but
              |                           Astrocaryum removal did not differ between sites. Seed predation
              |                           by small mammals was higher in PNS for Attalea, and higher in BCI
              |                           for Astrocaryum.
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text          |                          A comparison of palm seed dispersal in BCI and PNS revealed that the seed
              | removal of Attelea in PNS was more than 4-fold higher in the hunted site, contrary to
              | expectation. Verified Attelea predation by D. punctata was similar in both sites, while
              | seed predation by small mammals, primarily squirrels, was much higher in the hunted
              | site. Astrocaryum removal in the first week was 100% in both sites, with confirmed
              | removals by D. punctata being slightly higher in the hunted site, and removals by P.
              | steerei being slightly higher in the protected site (Fig. 4.6).
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              | 
title         | DISCUSSION
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text          | Hunting is a pervasive threat to biodiversity in tropical forests. Decreases in plant
              | diversity as high as 66% have been documented as an indirect consequence of hunting.
              | Yet the mechanisms by which that diversity is lost are poorly understood, as is their
              | context dependence. This study aimed to test some basic assumptions about plant-
              | seed predator interactions in the context of seed size, as well as hypotheses as to how
              | those interactions may change as a consequence of defaunation. This information is
              | useful for understanding how vertebrate seed predators shape community level
              | distributions of seed size, and to predict how and why plant community composition
              | may change with increasing hunting intensity.
              |        This discussion focuses primarily on plant-seed predator interactions.
              | However, as several of the animals relevant to this discussion are also recognized to be
              | secondary seed dispersers, much of the discussion which follows is equally relevant to
              | seed dispersal.
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              | 
text          | Seed size and vertebrate seed predation intensity. Overall, this study found little
              | support for the model assumption that vertebrate seed predation rates are correlated
              | with seed mass, either positively in moderately defaunated sites, or negatively in
              | highly defaunated sites. Other seed traits, as well as natural history, may be more
              | important for determining seed predation rates than seed mass per se. For instance, of
              | the three of largest seed-species in this study, the Astrocaryum and Attelea exhibited
              | the highest rates of seed removal, whereas Gustavia exhibited one of the lowest.
              | Relative to Gustavia, the palm seeds have an endosperm that is high in fat content, and
              | therefore energy rich for their weight. The rodents are well adapted to the primary
              | defense of these palms against seed predators: a woody endocarp. While the thin seed
              | coat of Gustavia would appear to make it more vulnerable to vertebrate seed
              | predators, it may exhibit chemical defenses that make them less desirable to
              | rodents(e.g. Forget 1992). Indeed, it was not uncommon on BCI and PNS to see bits
              | of Gustavia pulp with a pile of intact seeds of the forest floor, the result of agoutis
              | consuming the fruit flesh and discarding the seeds (E. Kurten, pers. obs.). However,
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              | 
              | 
text          | there are circumstances in which Gustavia seed predation has been higher (Sork 1987,
              | Forget 1992).
              |         The natural history of the two palm species also make them preferable for
              | hoarding.    A. standleyanum and A. butyracea germinate after 8 and 12 months
              | respectively. Therefore, they are likely to persist intact as hoarded seeds until the
              | period of low fruit availability from November through February (Foster 1982). In
              | contrast, Gustavia germinates within 1-2 weeks of fruit fall (E. Kurten, pers. obs.).
              | While the seeds remain attached to the establishing seedling for many more months,
              | seeds and cotyledons are vulnerable to consumption by other seedling predators, and
              | seed energy stores become reduced over time. By November, Gustavia seedlings are
              | no longer of interest to agoutis on BCI (Forget 1992). Therefore, in contrast to the
              | palms, Gustavia is not a species useful for provisioning rodents through the period of
              | low fruit availability.
              |         Comparison of the large-seeded palm species and Gustavia illustrates how
              | variability in seed consumption by vertebrates among seeds of similar size is likely to
              | be introduced by a variety of differences in nutritive value, defense traits, and
              | germination strategy. Variation in these traits will likely cause deviations in
              | consumption rates from what may be predicted by seed size and optimal foraging
              | theory alone.
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              | 
text          | Seed predator identity. Camera-based observations for five species preyed upon by
              | vertebrates showed little support for the model assumptions that the seed predator
              | body size is correlated with the size of the seed. While enclosure and exclosure
              | experiments have demonstrated that small rodents prefer small seeded species to
              | taxonomically related larger seeds, and can exert a large, and disproportionate seed
              | predation pressure on smaller seeded species (Dirzo et al. 2007, Mendoza & Dirzo
              | 2007), this study suggests that when seeds are available to the entire community of
              | potential seed predators, the importance of smaller mammals, even for relatively
              | smaller seeds, is diminished. In particular, agoutis appear to be a highly important
              | seed predator and secondary seed disperser in this system.
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              | 
              | 
text          |         There may be other circumstances, however, in which the relationship between
              | seed size and seed predator biomass may be stronger. It is notable that, despite the
              | fact that peccaries are well-documented seed predators of palms such as Astrocaryum
              | and Attelea in many parts of the Neotropics (Beck 2006), no observations of predation
              | of these two species by peccaries were observed in this study. This is likely due to the
              | fact that larger-bodied seed predators such as peccaries and brocket deer tend to
              | consume fruits and seeds under fruiting trees, where fruit and seed densities are
              | highest and foraging most efficient. In contrast, the seed arrays in this experiment best
              | mimicked the situation in which a few seeds have already been dispersed away from
              | the parent tree. Rodents such as agoutis and squirrels, will also forage under fruiting
              | trees. However, as scatter-hoarding species, they are behaviorally more likely than
              | larger seed predators to search for, find and consume small, isolated patches of seeds
              | on the forest floor.
              |         In addition to dispersal context, the composition of the mammal community is
              | likely influential in determining the strength of any relationship between seed size and
              | seed disperser size. For example, in forests such as Cocha Cashu, Peru, agoutis are
              | much less abundant (Terborgh & Wright 1994), and therefore less likely to
              | demonstrate a high importance as seed predators and seed dispersers across a range of
              | species, as seen on BCI. BCI is also lacking an abundance of terrestrial vertebrates at
              | the two extremes of seed predator body size. White-lipped peccaries (T. pecari) have
              | been locally extinct for more than half a century on BCI, and tapirs are rare. At the
              | other extreme, in parts of Mexico and Belize, mice such as Peromyscus and
              | Heteromys can be significant seed predators of some species (Coates-Estrada &
              | Estrada 1988, Klinger and Rejmanek 2009), whereas rodents smaller than spiny rats
              | (P. steerii) are rare on BCI.
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              | 
text          | Seed predation and defaunation. Despite large differences in abundances of key seed
              | predators such as collared peccaries and agoutis, decreased vertebrate seed predation
              | rates of larger-seeded species were not generally observed between BCI and PNS, nor
              | did smaller-seeded species generally show increases in seed predation rates in the
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              | 
              | 
text          | hunted site relative to the protected site. Rates of seed caching of large-seeded palms,
              | critical for seedling recruitment in those species, also did not differ between sites.
              | These data corroborate the work of Wright and colleagues (2001) with respect to
              | large-seeded palms, and extend it to a broader spectrum of species.
              |        Rather than seed predation, and secondary seed dispersal, varying linearly with
              | agouti abundance in this system, it may be useful to consider the possibility of seed
              | predator thresholds. In particular, lower populations of agoutis as a consequence of
              | hunting may serve to decrease competition for fruit and seed resources among agoutis
              | locally, but within certain limits, may not interfere with seed dispersal and seed
              | predation rates from the perspective of the plant. However, if hunting reduces agouti
              | populations below a particular threshold in abundance, there are no longer enough
              | animals to adequately maintain levels of seed predation and dispersal.
              |        Conceptualizing the disruption of plant-seed predator interactions in terms of
              | thresholds is similar to the model proposed by Galetti and colleagues (2006), in which
              | Astrocaryum seed predation rates are a sigmoidal or logistic, rather than linear,
              | function of agouti abundance. Data from two defaunation gradients suggest this may
              | be the case (Fig. 4.7). In Panama, sites with agouti densities 60%-80% lower than
              | BCI still had high rodent seed predation rates equivalent to or higher than those
              | observed on BCI, but where agouti densities were further reduced, seed predation rates
              | dropped dramatically (Wright et al. 2001). Likewise in Brazil, sites with agouti
              | abundances 80% lower than the maximum density observed still maintained agouti
              | seed predation rates approximately equal to those observed in the sites with the highest
              | agouti abundance (Donatti et al. 2009).
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              | 
              | 
text          |                                                    100   Above threshold
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              | 
              | 
              | 
text          |                        Rodent seed predation (%)
              |                                                          Below threshold
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text          |                                                    80
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              | 
text          |                                                     60
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              | 
text          |                                                     40
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              | 
text          |                                                     20
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              | 
text          |                                                      0
              |                                                           A         B      C    D      E
              |                                                                     Literature Study
              |          FIGURE 4.7. Published studies examining seed predation of
              |          large-seeded palms by rodents, primarily agoutis, across
              |          defaunation gradients consistently find that high rates of seed
              |          predation are maintained despite reductions in agouti densities up
              |          to 80% of maximum observed densities. Below this threshold,
              |          seed predation rates drop 48-96%. (A) Galetti et al. (2006),
              |          Astrocaryum aculeatissimum, under parent trees; (B) Donatti et
              |          al. (2009), A. aculeatissimum, controlled experiment; (C) Galetti
              |          et al.(2006), ), A. aculeatissimum, controlled experiment; (D)
              |          Wright et al. (2000), Astrocaryum standleyanum, “dispersed”
              |          seeds; (E) Wright et al. (2000), Attalea butyracea, “dispersed”
              |          seeds.
              |        At a community level, evidence has been found both for large, mammal- or
              | primate-dispersed species decreasing in abundance in association with hunting
              | (Nunez-Iturri et al. 2008, Terborgh et al. 2008), and community mean seed mass
              | increasing in association with hunting (Wright et al. 2007, Ch. 2). Differences in the
              | mammalian community context, in the relative levels of defaunation being compared,
              | and differences in the traits and natural histories of plant species driving the
              | community level patterns may all be contributing to such discrepancies in community
              | level response to hunting.
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              | 
              | 
title         | CONCLUSIONS
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              | 
text          | Overall, this empirical test of a theoretical model (Dirzo et al. 2007) of how seed
              | predation rates should vary as a function of seed size and defaunation intensity found
              | little general support for the model. In this system, there was only weak support for a
              | relationship between seed mass and vertebrate seed predation rate, and no evidence
              | that seeds were increasingly predated upon by larger-bodied seed predators as seed
              | size increased by species. Furthermore, despite large differences in the abundances of
              | key seed predators between a hunted and protected site, no differences were seen in
              | vertebrate seed predation, or seed caching by agoutis.      This work highlights the
              | importance of considering both plant natural history and mammal community context
              | when trying to predict the indirect effects of hunting on plant recruitment. It also is
              | consistent with accumulating evidence that the functional roles that seed predators and
              | seed dispersers play in tropical forests may not be linearly correlated with their
              | abundance in a system, but rather, may be threshold-dependent.
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title         | ACKNOWLEDGEMENTS
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text          | The author is grateful to the Autoridad Nacional del Ambiente (ANAM) of Panama
              | for permission to conduct work in Parque Nacional Soberanía, and to the Smithsonian
              | Tropical Research Institute (STRI) for permission to conduct this work on BCI, and
              | for providing logistical support. I would like to thank J. Wright for seed mass data
              | and advice about sites. N. Beckman also provided useful advice in the planning stages
              | of this experiment. The Fondo Peregrino–Panamá, in particular A. Muela, provided
              | logistical support at the site in the Parque Nacional Soberanía. Many thanks go to C.
              | Sherman, R. Bethancourt and R. Acosta for their hard work in the field and the lab,
              | and to S. Rebellon for help with pilot work. D. Brassfield and O. Calderón provided
              | help with species identification. I would like to thank O. Arosemena at STRI for her
              | help with permitting, and all the staff on BCI whose help made conducting this work
              | easier. R. Dirzo and C. Donatti provided comments which improved the manuscript.
              | This project was made possible with funding from NSF DEB-0808338.
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              | 
              | 
              | 
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