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Cascading Effects of Contemporaneous Defaunation on Tropical Forest Communities Biological Conservation 163 (2013) 22–32 Contents lists available at SciVerse ScienceDirect Biological Conservation journal homepage: www.elsevier.com/locate/biocon Special Issue: Defaunation’s impact in tropical terrestrial ecosystems Cascading effects of contemporaneous defaunation on tropical forest communities Erin L. Kurten Department of Biology, Stanford University, Stanford, CA, USA article info abstract Article history: Defaunation, driven by hunting and habitat fragmentation, poses a threat to wildlife in tropical forests Received 21 October 2012 worldwide and is expected to have cascading effects on other organisms, particularly plant communities. Received in revised form 24 April 2013 This review summarizes empirical evidence from 42 studies on the indirect effects of defaunation on Accepted 26 April 2013 plants, focusing on altered plant–animal interactions, the resulting effects on plant population demogra- phy, and finally, community-level changes in plant composition and diversity. This review confirms, as previously documented, that larger-seeded species consistently experience reduced primary seed dis- Keywords: persal, and increased seedling aggregation around parent trees, as a result of defaunation. Reduced seed Defaunation predation and herbivory are also associated with defaunation, in some cases countering the negative Hunting Plant diversity effects of reduced dispersal. The net effects of these changes led to either higher or lower seedling recruit- Tropical forest ment, depending on plant species. Defaunated plant communities show consistent shifts toward lower Seed dispersal species richness, higher species dominance, and lower diversity. More research integrating effects of def- Seed predation aunation on all processes from seed dispersal through plant recruitment is required to mechanistically link altered species interactions to changes in recruitment and community composition. Ó 2013 Elsevier Ltd. All rights reserved. Contents 1. Introduction .......................................................................................................... 23 2. Methodology.......................................................................................................... 23 2.1. Identification of studies . ............................................................................. 23 2.2. Standardization of response variables for comparison . ............................................................. 23 2.3. Index of defaunation intensity . ............................................................................. 24 2.4. Seed size data . ................................................................................................ 24 3. Results and discussion . .......................................................................................... 24 3.1. What is defaunation? . ............................................................................. 24 3.2. Plant–animal interactions . ............................................................................. 24 3.2.1. Seed dispersal . .................................................................................. 24 3.2.2. Seed predation . .................................................................................. 26 3.2.3. Herbivory and trampling . .................................................................................. 27 3.3. Plant population demography . ............................................................................. 27 3.3.1. Recruitment . .................................................................................. 27 3.3.2. Seedling survival. .................................................................................. 28 3.3.3. Standing abundance . .................................................................................. 28 3.4. Plant community diversity . ............................................................................. 28 3.4.1. Community seedling density . .................................................................. 28 3.4.2. Diversity . .................................................................................. 28 3.4.3. Plant functional groups . .................................................................................. 29 3.5. Improving how we study defaunation . ............................................................................. 29 3.6. Linking species interactions, plant species recruitment, and biodiversity . .......................................... 30 4. Conclusions and future directions. ....................................................................... 30 E-mail addresses: [email protected], [email protected] 0006-3207/$ - see front matter Ó 2013 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.biocon.2013.04.025 E.L. Kurten / Biological Conservation 163 (2013) 22–32 23 Acknowledgements . .................................................................................... 30 Appendices. Supplementary material . .................................................................................... 30 References . ....................................................................................................... 30 1. Introduction Recent synthesis on the indirect effects of defaunation in trop- ical forests have focused on seed dispersal (Markl et al., 2012; Animal populations are currently in decline due to both unsus- McConkey et al., 2012) or seed predation (Stoner et al., 2007). tainable hunting and habitat fragmentation in tropical forests However, no review has examined how different plant–animal throughout Asia (Corlett, 2007), Africa (Fa and Brown, 2009) and interactions may be changing simultaneously, or evaluated the evi- Latin America (Peres and Palacios, 2007), a phenomenon that has dence linking those changes to altered recruitment or lower biodi- come to be known as defaunation (Dirzo and Miranda, 1991), or versity. This review synthesizes 42 studies of how plant–animal the ‘‘empty forest syndrome’’ (Redford, 1992), in extreme cases. interactions, plant population demography, and community diver- Defaunation does not impact all animal species in a community sity respond to defaunation, with the aim of evaluating how the ef- equally. Rather, vertebrates respond differently to the drivers of fects of defaunation on individual species at different stages of defaunation as a function of their body size. plant recruitment contribute to changes occurring at the popula- These responses have been articulated as a model by Wright tion or community level. In addition, I examine the heterogeneity (2003) and best demonstrated empirically in a comparison of in how defaunation is defined and studied by plant ecologists, as densities of more than 30 animal taxa at three levels of hunting it relates to synthesizing results across studies. pressure, using 101 sites in Amazonia (Peres and Palacios, 2007). Large-bodied species, such as ungulates and large primates, tend to be preferred game species, have large home ranges, and have 2. Methodology a higher age at first reproduction and low fecundity, traits which increase vulnerability to hunting and habitat loss (Cardillo et al., 2.1. Identification of studies 2005). Therefore, they decline monotonically as hunting and fragmentation intensify in a system (Peres and Palacios, 2007, Here I summarize the literature on indirect effects of tropical Appendix A). As large-bodied species begin to decline, med- defaunation through 2012. (See Appendix B for methodological de- ium-bodied species are initially expected to increase in abun- tails.) To be included, studies had to use comparative experimental dance, likely due to a relaxation of competitive and predation designs (e.g. defaunated vs. non-defaunated; exclosure vs. control), pressures (Wright, 2003)(Appendix A). However, as large-bodied with raw response variables reported for both defaunated and non- species become depleted or locally extinct, or as habitat frag- defaunated conditions. In total, 42 studies (Appendix C) met all cri- ments become increasingly smaller, this density compensation teria for inclusion. should cease, and medium-bodied species themselves experience the impacts of hunting and habitat loss, declining in abundance 2.2. Standardization of response variables for comparison accordingly (Appendix A). Finally, small-bodied species tend to be undesireable as game species, have small habitat require- Raw response values for seed dispersal, seed predation, herbiv- ments, relatively quick maturation, and high fecundity. These ory, recruitment, diversity, and species richness were compiled traits confer high tolerance to habitat loss and harvesting, even from text, tables, and figures. (See Appendix B for details.) The enabling some species (e.g. rats, squirrels and small monkeys) authors’ categorical characterizations of relative levels of defauna- to persist in urban, human-dominated environments. In addition, tion were used to categorize sites. Reference sites generally exhib- these species are also thought to benefit from reduced predation ited moderate to no defaunation, while more impacted sites and competition as larger species decline in the system (Wright, exhibited larger decreases in animal abundance and species rich- 2003). Therefore, these species are expected to increase mono- ness. These sites will hereafter be referred to as ‘‘non-defaunated’’ tonically in abundance as hunting and fragmentation intensify and ‘‘defaunated’’ respectively. When studies reported response
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