Cascading Effects of Contemporaneous Defaunation on Tropical Forest Communities

Biological Conservation 163 (2013) 22–32

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Biological Conservation

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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 demography, 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]

Acknowledgements ...... 30 Appendices. Supplementary material ...... 30 References ...... 30

1. Introduction Recent synthesis on the indirect effects of defaunation in tropical 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 in a system (Appendix A). variables from multiple defaunated or non-defaunated sites, a Because many of the animals most vulnerable to defaunation, mean value for each category was used to summarize responses as well as their less vulnerable competitors, are seed dispersers, and avoid introducing additional variability from individual sites. seed predators, seedling predators, and herbivores, defaunation Sites experiencing the lowest levels of defaunation were grouped is likely to disrupt plant–vertebrate interactions (Emmons, with ‘‘no defaunation’’ sites, while sites showing medium to high 1989; Redford, 1992; Wright, 2003). Such disruptions are ex- levels of defaunation comprised the ‘‘defaunated’’ sites. pected to negatively impact some plant species while benefitting To enable more direct comparisons of effects, I calculated effect others, and lead to an overall loss of tropical forest plant diver- sizes for each response variable. The effect size estimator used here sity. Plant species with hunted dispersers are expected to expe- is the percent difference in the response, as follows: Effect rience reduced seed dispersal, particularly the largest-seeded size = 100 Ã (RD À RND)/RND, where RD and RND are the magnitudes plant species. Changes in seed predation, seedling predation, of the response variables in the defaunated and non-defaunated and herbivory may have positive or negative effects on species sites, respectively. (See Appendix B for additional details.) An effect recruitment, depending on a plant species’ traits (Wright, 2003; size of zero indicates no difference between RD and RND. Positive Dirzo et al., 2007; Muller-Landau, 2007). Overall, the net effect values indicate that the response variable was higher in the defau- of defaunation on plant diversity has been hypothesized to be nated condition; negative values indicate that the response vari- negative (Wright, 2003; Muller-Landau, 2007), because species able was lower in the defaunated condition. Due to the degree of experiencing reduced seed dispersal will experience greater den- heterogeneity introduced to the dataset by the variation in study sity-dependent mortality, and because seed predators and herbi- design, defaunation intensities compared, and species studied, no vores will not suppress populations of competitively dominant meta-analysis of responses was conducted (cf. Hedges and Olkin, species. 1985). Negative results cannot reliably be attributed to true biolog- 24 E.L. Kurten / Biological Conservation 163 (2013) 22–32

A munity, disproportionally affecting larger-bodied species (Galetti and Dirzo, 2013). However, there is little consensus as to how to define or measure defaunation empirically. The 42 studies reviewed here variously use animal densities, species occurrences, the occurrence of a species of interest (e.g. large primates, agoutis), or proxies of defaunation (e.g. proximity to villages and roads, fragment size) to categorize sites as ‘‘defaunated’’ or ‘‘non-defaunated.’’ As a result, animal communities within and between defaunated and non-defaunated study sites are highly variable. This is illustrated by examining the occurrence of 10 widely dis- tributed genera in Neotropical sites. Great heterogeneity in animal richness (Fig. 1A) and community composition (Fig. 1B) exists within defaunated and non-defaunated sites. In some cases, sites with similar species compositions would be considered ‘‘non-def- B aunated’’ in one study, and ‘‘defaunated’’ in another (Fig. 1). Research on indirect effects of defaunation has predominantly focused on Neotropical mammals. Only 17% of studies reviewed here investigated effects of avian defaunation; 93% examined effects of mammalian defaunation. Most of the latter studies focused on rodents and/or primates, rather than ungulates or elephants. Sixty-nine percent of studies were conducted in the Neotropics; fewer were conducted in Africa (19%), Asia (10%) and Polynesia (2%). Forest comparison studies generally had low site replication, reflecting the logistical challenges of working at the large spatial scales upon which defaunation occurs. Approximately a quarter of studies compared just one non-defaunated or control site with one defaunated site; an additional quarter compared one non-defaunated site with two to three defaunated sites. Fig. 1. Animal community composition for 19 Neotropical studies. (A) Mean percentage of 10 focal animal species occurring in the defaunated sites vs. non- defaunated of each study. (B) Non-metric multidimensional scaling (NMDS) 3.2. Plant–animal interactions ordination based on 10 focal animal species for the defaunated sites and non- defaunated sites. 3.2.1. Seed dispersal Approximately three quarters of woody species in tropical forests rely exclusively on biotic dispersal agents for seed dispersal ical non-effects, because they also could be caused by the hetero- (Almeida-Neto et al., 2008; Muller-Landau and Hardesty, 2005). geneity among studies. Some of the largest, most threatened vertebrate species, like elephants, tapir, and large primates, are known to disperse large 2.3. Index of defaunation intensity quantities of seeds comprising tens to hundreds of species (Blake et al., 2009; Campos-Arceiz and Blake, 2011; O’Farrill et al., in Quantification of defaunation intensity was restricted to Neo- press; Stevenson and Aldana, 2008). Some of these plant species tropical sites because more extensive and comparative data on ver- may have no alternative disperser, either because no other animal tebrate communities were reported for this region. I selected 10 species in the community is large enough to ingest and move the genera of mammalian frugivores, granivores, and browsers that seed (Babweteera and Brown, 2009; Nunez-Iturri et al., 2008; Peres differ in body mass and sensitivity to defaunation pressures: Tapir, and van Roosmalen, 2002; Stevenson, 2011), or because those that Tayassu, Pecari, Odocoileus, Mazama, Ateles, Alouatta, Cebus, Agouti, can are seed predators, not dispersers (Campos-Arceiz et al., 2012). and Dasyprocta. These genera are wide-ranging in the Neotropics, Small-bodied dispersal agents, e.g. bats, squirrels, and small birds, though the specific species may vary, and range from highly vul- are expected to be less negatively affected by forest fragmentation nerable to defaunation (e.g. Tapir, Tayassu, Ateles) to more resistant and hunting than large-bodied dispersal agents, in some cases even to defaunation (e.g. Dasyprocta, Cebus)(Peres and Palacios, 2007). increasing in abundance (Appendix A). Defaunation intensity was calculated as the percent of focal genera Seed dispersal is thought to promote plant recruitment in trop- that appeared to be locally extirpated in that site from occurrence ical forests by facilitating escape from natural enemies (Muller- data, though present historically (Appendix D). Landau, 2007), helping species with particular environmental requirements for germination and survival (e.g. light-demanding 2.4. Seed size data species) reach favorable microhabitats (Brodie et al., 2009; Mul- ler-Landau, 2007), and promoting seed survival and germination To assess predictions that are seed size dependent, I assembled via pulp removal (De Barros Leite et al., 2012; Heer et al., 2010) seed mass and length data from studies reviewed, other published and gut passage (Traveset and Verdú, 2002). Via these mecha- literature and the Royal Botanic Gardens Kew Seed Information nisms, any reduction in seed dispersal for a particular species is Database (SID) (2008). These were used to rank species by size. hypothesized to have negative effects on its later overall recruitment (Muller-Landau, 2007). 3. Results and discussion 3.2.1.1. Primary seed dispersal. Here, primary seed dispersal is de- 3.1. What is defaunation? fined as physical removal of the seed from the parent tree and deposition on the ground. Seed dispersal has been directly mea- There is a general consensus that defaunation refers conceptu- sured, either as the quantity of seeds removed by primary dispers- ally to declines in abundance and occurrence of animals in a com- ers such as birds or primates (44%), or as the number of seeds E.L. Kurten / Biological Conservation 163 (2013) 22–32 25 arriving in a new location (56%). Consistent with expectation, seed either by terrestrial vertebrates ingesting the seeds and defecating dispersal was lower in defaunated forests in almost all nine cases them elsewhere, or by rodents scatter-hoarding, or caching, seeds examined (Fig. 2A). Declines ranged from 25% to 93%. The magni- in the ground. Secondary seed dispersal by terrestrial vertebrates tude of the decrease appears to be weakly correlated with seed is expected to vary with defaunation in accordance with the abun- size, but was not significant (Spearman-Rank correlation À0.36, dance of the particular seed disperser. Only seed caching has been p = 0.195). measured in the context of defaunation. While individual cached The species reported here represent only the very upper range seeds may be predated at a later time, seeds that are not subse- of tropical seed mass distributions (Wright et al., 2007a) and were quently recovered are afforded protection from vertebrate and generally studied because they were most likely to show declines invertebrate seed predators. For some species, such as large-seeded in dispersal. How dispersal declines affect the plant community palms with specialist bruchid beetle seed predators, seed survival as a whole is less clear. Changes in the abundances of species in is heavily dependent upon seed caching by rodents (Smythe, 1989). the seedling layer suggest that the broader community of species All studies of seed caching were conducted in the Neotropics. In may experience dispersal declines in a seed size-dependent man- eight of the 19 cases, seed caching was higher (15–400%) in defau- ner (Terborgh et al., 2008), however this evidence is indirect. Only nated sites relative to non-defaunated sites (Fig. 2B). In nine cases, two studies directly measured how defaunation affects the dis- seed caching was lower (7–100%). In these cases, the defaunated persal of smaller-seeded species (<1 cm fruit diameter), with con- sites were usually small fragments, islands, or heavily hunted sites trasting results. Dispersal of Bocageopsis multiflora in defaunated in which agoutis, an important Neotropical scatter-hoarding seed sites was more than 2-fold higher than in non-defaunated sites disperser, were extirpated or rare. Squirrels did not fully compen- (Fig. 2A), possibly due to more abundant generalist, frugivorous sate for the loss of agoutis (Donatti et al., 2009). This suggests that birds in highly fragmented sites (Cramer et al., 2007). In contrast, agoutis are primarily responsible for the higher rates of seed a decrease in avian forest specialists that was not compensated caching. for by forest generalists appears to be responsible for a net de- These results are consistent with the hypothesis that the ro- crease in seed dispersal in Celtis durandii (Kirika et al., 2008). dents primarily responsible for seed caching in these forests, specifically agoutis, may actually benefit from a reduction in the abundance of predators and larger-bodied competitors at low to 3.2.1.2. Vertebrate seed caching. Secondary seed dispersal, occurring medium levels of defaunation (Dirzo et al., 2007; Peres and Pala- after the seed has been deposited on the ground, can be performed cios, 2007; Wright, 2003). Therefore, while defaunation may have a negative effect on primary dispersal, this negative effect does not always extend to secondary seed dispersal by terrestrial ro- A dents. The effects of defaunation on invertebrate seed dispersal have received less study. However, there is some evidence that defaunation has negative effects on dung beetle abundance, species richness, average size, and seed caching activity (Culot et al., 2013; Andresen, 2003; Larsen et al., 2005; Andresen and Laurance, 2007). To my knowledge, no functional equivalent to the agouti has yet been discovered in Paleotropical forests. The musky rat kangaroo (Hypsiprymnodon moschatus) in the Australian tropics is a scatter- hoarding marsupial that is slightly smaller than a Neotropical acouchi (Myoprocta spp.) (Dennis, 2003; Forget and Vander Wall, 2001). Scatter-hoarding rodents such as squirrels and murid rodents exist in Africa and Asia (Corlett, 2009; Forget and Vander B Wall, 2001), however they are smaller-bodied (generally <1 kg) and likely incapable of handling the full range of seed sizes (Dirzo et al., 2007; Mendoza and Dirzo, 2007). The larger Paleotropical rodents, e.g. Cricetomys species, are reported to larder-hoard seeds in burrows where they will not survive (Guedje et al., 2003), though recent work on Carapa grandiflora in Rwanda, suggests that they do scatter-hoard at least a limited proportion of seeds (2–3%), possibly more (Nyiramana et al., 2011). Future studies of Carapa dispersal should provide a more accurate picture of Cricetomys as an agouti functional equivalent (P.-M. Forget, pers. comm.). Nevertheless, the compensatory seed dispersal that agoutis may provide some plant species in the Neotropics seems less likely to be present in Asian, if not African, tropical forests. Even within the Neotropics, compensation may be restricted to plant species with seeds one gram in size or larger (Galetti et al., 2010).

3.2.1.3. Spatial distribution of seeds and seedlings. The altered 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 non-defaunated forests, and fewer seeds or seed- Fig. 2. Differences in (A) primary seed dispersal and (B) seed caching rates in defaunated sites relative to non-defaunated sites. Species ranked by seed size. No lings at distances away from parent trees. Indeed for many species, bar indicates no difference. (#) = study number (Appendix C). seed numbers under parent trees were 1.4–24-fold higher in def- 26 E.L. Kurten / Biological Conservation 163 (2013) 22–32

plants, compensation is likely to be limited. There are two types of evidence for this: studies of animal diets and studies of seed dispersal. Recent work demonstrates that tropical dispersal networks are modular and nested, such that subgroups of dispersers are linked only to subsets of species in their module (Donatti et al., 2011)(Donatti et al., 2011), limiting the potential number of species able to compensate for the loss of another disperser in the module. Many larger arboreal seed dispersers diverge in their diet preferences, presumably partitioning resources to limit competition (e.g. Dew, 2005; Guix et al., 2001; Martins, 2008; Savini and Kanwatanakid-Savini, 2011). Within dispersal networks, smaller primates only disperse a nested subset of the plant species dispersed by larger primates (Peres and Van Roosmalen, 2002; Ste- venson and Aldana, 2008). Even when co-occurring dispersers 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 fully compensate for one another. What Poulsen and colleagues observed, however, was a realized niche (sensu Ackerly, 2003), i.e. the diet of a species with a competitor present, rather than the fundamen- tal niche, i.e. what the diet could be in the absence of competition. A study of Virola in Ecuador, however, addressed this issue, observ- Fig. 3. The number or proportion of seeds or seedlings under and away from parent ing that when the principal dispersers were absent, alternative dis- trees, in defaunated sites relative to non-defaunated sites. Species ranked by seed size. (#) = study number (Appendix C). persers did not shift their diet preferences enough to fully compensate for that loss (Holbrook and Loiselle, 2009). In other cases, species having dietary overlap with principal dis- aunated sites relative to non-defaunated sites (Fig. 3). Increases in persers fail to disperse seeds. Whereas larger primates would swal- seedling numbers were more modest, 1.5–13-fold higher (Fig. 3). low and disperse some larger seeds, smaller primates might spit Away from parent trees, seed and seedling numbers were 25– them out as they feed at the parent tree (Babweteera and Brown, 96% and 61–93% lower, respectively, in defaunated forests relative 2009; Lambert, 1999; Stevenson, 2011). Even tapirs, which in Neo- to non-defaunated forests, excepting Attalea butyraceae (Fig. 3). tropical forests are the largest extant vertebrates and are consid- These patterns are consistent with the loss of biotic dispersal ered to be key seed dispersers (O’Farrill et al., in press), have agents. been shown to be seed predators of some elephant-dispersed spe- There are two notable exceptions to these trends. Hymenaea on cies in Southeast Asia (Campos-Arceiz et al., 2012). Squirrels may land-bridge islands in Venezuela showed the highest increases in partially compensate for losses of seed-caching agoutis, however seed pods remaining under parent trees in sites without agoutis many small rodents do not scatter-hoard, and those that do are un- relative to sites with agoutis. However, it is one of the few cases likely to handle the full range of seed sizes (Dirzo et al., 2007). in which seedling densities are actually lower under parent trees Empirical studies of seed dispersal also inform the discussion of in defaunated forests (Fig. 3). This is due to the natural history of dispersal compensation. Decreases in seed dispersal (Fig. 2) dem- Hymenaea, which relies on agoutis to open its seed pods so that onstrate, at the very least, that for larger-seeded species, alterna- seeds may germinate (Asquith et al., 1999). The other exception tive primary dispersers do not fully compensate for the loss of a is A. butyraceae in Panama. Despite an 81% reduction in seeds dis- principal primary disperser. It is possible that terrestrial secondary persed away from parent trees in defaunated sites, seedling num- dispersers may also compensate for the loss of an arboreal primary bers were 3-fold higher, due to reduced seed predation in disperser, as the former experience asymmetric competition from defaunated sites (Wright and Duber, 2001; Section 3.2.2). arboreal dispersers, increasing the likelihood that they exhibit a Cramer et al. (2007) estimated changes in dispersal distances compensatory response to competitive release. Alternatively, ter- with defaunation. Mean and maximum dispersal distances were restrial dispersers themselves could be declining with defaunation 60% and 80% lower respectively for the large-seeded Duckeoden- in some cases, compounding the effect of losing a principal dis- dron cestroides in defaunated fragments, relative to continuous for- perser. In cases where species have lost their primary dispersal est. In the same study, mean and maximum dispersal distances agent, the number of seeds and seedlings remaining under adult were not significantly different for the smaller-seeded B. multiflora. trees in defaunated sites is often higher than in non-defaunated These results, together with the patterns of altered seed and seed- sites (Fig. 3). It is clear that terrestrial seed dispersers are not fully ling distribution (Fig. 3), suggest that seedlings of large-seeded compensating for loss of principal avian and primate dispersers in species may become more spatially aggregated in defaunated for- these cases. It is unclear from seed and seedling data alone the ex- ests. Whether this shift in the spatial template of the seedling com- tent to which partial compensation may be occurring in these munity will translate into increased aggregation of adult trees will cases. depend on the net effects of seedling predation, herbivory, density- dependent mortality, and the spatial distribution of favorable sites for recruitment (Muller-Landau, 2007). 3.2.2. Seed predation Effects of defaunation on seed predation have received less 3.2.1.4. Compensation among dispersal agents. A key question attention than effects on seed dispersal, and yet, understanding regarding seed dispersal in tropical forests is whether the loss of them is critical for understanding how defaunation may alter plant a principal dispersal agent may be compensated for by alternative recruitment and forest composition. Dirzo et al. (2007) proposed dispersers. Evidence is accumulating that, for many species of that seed predation rates depend upon (1) the plant species and E.L. Kurten / Biological Conservation 163 (2013) 22–32 27 its traits (specifically seed size), (2) the seed predator and its re- 3.2.2.3. Invertebrate seed predation. A reduction in vertebrate seed sponse to defaunation, and (3) the intensity of defaunation. predation may benefit invertebrate seed predators in two ways. More specifically, larger-seeded species were predicted to ini- First, invertebrates experience a release from competition for seed tially experience higher seed predation rates in response to defau- resources (Muller-Landau, 2007). Second, larvae developing in nation, as their seed predators increased in abundance (Dirzo et al., seeds may experience decreased mortality due to the reduction 2007). As defaunation intensified, however, predation rates of of seed predation by vertebrates (Silvius, 2002). Through these large-seeded species were predicted to decline as their seed preda- mechanisms, defaunation may lead to higher abundances of these tors declined. Predation rates of smaller-seeded species were pre- invertebrates, and thereby higher rates of invertebrate seed dicted to increase monotonically with increasing defaunation predation. intensity, as small rodents experienced release from competition Consistent with expectation, invertebrate seed predation of and predation (Dirzo et al., 2007). palms was higher in defaunated sites for most species investigated (Fig. E1). However, in general, the absolute increase in invertebrate seed predation rates only partially compensated for the co-occur- 3.2.2.1. Pre-dispersal seed predation. Beckman and Muller-Landau ring decreases in vertebrate seed predation (Wright et al., 2000; (2007) investigated effects of defaunation on pre-dispersal seed Wright and Duber, 2001, but see Galetti et al., 2006). In O. mapora predation for two plant species of contrasting seed size in central and C. bicolor, pre-dispersal seed predation by insects between Panama. They hypothesized that predation rates from small mam- sites was not significantly different for either species (Beckman mals would be higher in defaunated forests. However, they found and Muller-Landau, 2007), suggesting that higher rates of inverte- that pre-dispersal seed predation by mammals was significantly brate seed predation in response to defaunation are not universal. lower in the defaunated sites for the larger-seeded Oneocarpus mapora, and did not occur for small-seeded Cordia bicolor. Small mam- 3.2.3. Herbivory and trampling mal abundances were not measured, so the discrepancy between As with seed predators, ungulates are expected to decline with hypothesis and result is unexplained. defaunation, resulting in decreased herbivory and trampling. Few observational studies have evaluated differences in herbivory or trampling as a consequence of defaunation. However, these have 3.2.2.2. Post-dispersal seed predation. After primary dispersal, seeds generally shown large declines in vertebrate damage to plants. Dir- may be preyed upon by terrestrial vertebrates such as rodents, zo and Miranda (1991) reported a complete absence of vertebrate ungulates, birds, and reptiles. The majority of studies comparing herbivory in defaunated Los Tuxtlas, Mexico. Alves-Costa (2004) seed predation rates between defaunated and non-defaunated found that the frequency of Syagrus romanzoffiana individuals sites have performed manipulative experiments, setting out arrays experiencing little to no herbivory was 66% higher in defaunated of seeds and monitoring the fates of those seeds. A few studies of sites in Brazil. In addition, ‘‘trampling’’ of seedling models by ver- species with slowly decomposing endocarps have looked at tebrates was 75% lower in defaunated forests in Bolivia (Roldán ‘‘standing’’ rates of seed predation in the field (Galetti et al., and Simonetti, 2001). 2006; Wright and Duber, 2001; Wright et al., 2000). In 22 of the In extreme cases of defaunation, competitive release of small 31 cases, seed predation rates were lower in defaunated sites, rodents can actually increase rates of herbivory, in the form of while in nine cases, seed predation rates were higher (Fig. 4). seedling predation (Asquith et al., 1997)(Fig. E2). However, spiny This suggests that defaunation may provide a demographic ben- rat (Proechimys semispinosus) densities in this study were among efit to some species in the form of reduced seed predation. How do highest ever recorded (Adler, 1996), and unlikely to be representa- these differences vary with seed size and defaunation intensity? tive of most defaunation scenarios. This analysis does not generally support the hypothesis that seed predation of larger-seeded species initially increases and then de- 3.3. Plant population demography creases as defaunation intensifies, or that predation of smaller seeds increases with defaunation intensity (Fig. 4) (but see Fleury One might expect decreases in seed dispersal in defaunated for- and Galetti, 2006; Mendoza and Dirzo, 2007; Stoner et al., 2007). ests (Fig. 2) to translate to lower observed recruitment rates and Given the variation in faunal composition among sites and species seedling densities of affected plant species in defaunated sites. traits compared, it would be premature to conclude that seed pre- However, lower net rates of seed predation (Section 3.2.2) and her- dation does not vary as predicted. A study of seed predation over a bivory (Section 3.2.3) should promote higher seedling recruitment range of seed sizes and defaunation intensities is needed to com- rates and densities. These benefits may be attenuated by density- prehensively test these hypotheses. dependent mortality, the availability of favorable recruitment sites, and plant–plant competition (Muller-Landau, 2007). Depending on how these effects integrate, one might expect net species recruitment rates in defaunated forests to be higher, lower, or similar to those in non-defaunated forests.

3.3.1. Recruitment Empirically, plant recruitment was reported either as new seedlings entering the population in a deﬁned length of time, as the ratio of seedlings to adults, or as the ratio of saplings to seedlings (Appendix C). In about half of cases, recruitment was 2–5-fold higher in defaunated forests than in non-defaunated forests, both for seedlings and saplings (Fig. 5). In the other half of cases, recruitment was 19–98% lower in defaunated forests. The variation in changes in recruitment does not seem to be consistently related to the degree of defaunation across studies, Fig. 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 loss of particular dispersers or seed predators, or particular plant plant species. traits. In the absence of information about agents of seedling mor- 28 E.L. Kurten / Biological Conservation 163 (2013) 22–32

Fig. 5. Variation in seedling and sapling recruitment in defaunated sites relative to non-defaunated sites. (#) = study number (Appendix C). Fig. 6. Differences in plant densities in defaunated sites relative to non-defaunated sites. (#) = study number (Appendix C). tality, it is difﬁcult to further interpret the variation in the context predation in the defaunated site (Babweteera et al., 2007). Mean- of defaunation. while, bird-dispersed species are less abundant in defaunated sites. Due to the low site replication of some studies, it is also possible All studies involving rodent-dispersed species were conducted that some differences in recruitment, seedling survival (Sec- on palm species or Dipteryx, most of which are preferred food spe- tion 3.3.2) and seedling densities (Section 3.3.3) are due to other cies for agoutis and peccaries, important Neotropical seed preda- environmental factors that vary across the landscape, such as pre- tors (Beck, 2006). For these species, reductions in vertebrate seed cipitation or edaphic conditions. This is particularly true in studies and seedling predation appear to more than compensate for any where fragmentation was a driver of defaunation, as fragmentation increases in mortality by other natural enemies, resulting in a alters many aspects of the microclimate that affect seedling net increase in survival. More studies in Neotropical forests are re- dynamics independently of defaunation. quired to determine if other species preyed upon by agoutis also increase in abundance in defaunated sites. At least two of the three 3.3.2. Seedling survival studies of bird-dispersed species were conducted in Paleotropical As with recruitment, responses of seedling survival to defauna- forests with different assemblages of seed predators, which per- tion are quite variable (Fig. E2). Asquith et al. (1997) found that dif- haps do not provide the same opportunities for seed predation es- ferences in seedling survival varied among species within the same cape as those observed in Neotropical forests. study system. Survival was lowest on highly defaunated islands in Lake Gatun, Panama for two of the three species tested. Exclosure 3.4. Plant community diversity experiments veriﬁed that spiny rats, free of competition and predation from larger mammals and were responsible for the increased Seed dispersers carry seeds to favorable recruitment sites, be mortality (Asquith et al., 1997), reaching population sizes 10-fold they sites free from natural enemies, or sites with favorable envi- greater on these islands relative to the non-defaunated sites (Adler, ronmental conditions (e.g. gaps for light-demanding species (Bro- 1996). The third species, Virola surinamensis, suffered 100% mortal- die et al., 2009)). Seed predators and herbivores limit the ity at both defaunated and non-defaunated sites (Asquith et al., abundances of fast growing, competitively dominant species, pre- 1997). venting better defended, but slower growing species from being Differences in survival rates can also be variable within a spe- outcompeted (Coley and Barone, 1996). If any of these interactions cies in the same region, likely due to differences in the defaunation is disrupted, one would expect diversity at the community level to intensities being compared. In the Lake Gatun region of central decrease as a consequence (Muller-Landau, 2007). Panama, the survival of Gustavia superba was higher where the animal community of the hunted site was not so impoverished as to 3.4.1. Community seedling density lead to a competitive release of small rodents (Sork, 1987). How- Seedling or herb density at the community level is consistently ever, on islands with only high populations of spiny rats present, higher where exclosure experiments eliminate most vertebrate survival of G. superba was lower in the defaunated site (Asquith herbivory and seed predation (Beck et al., 2013; Ickes et al., et al., 1997). 2001; Royo and Carson, 2005). In forest comparisons, however, whole community seedling densities are generally lower in defau- 3.3.3. Standing abundance nated sites, relative to non-defaunated sites (Fig. 7A) (but see Dirzo Exclosure experiments generally demonstrate that, when pro- and Miranda, 1991). This discrepancy may be due to the fact that tected from vertebrate granivores and herbivores, seedling densi- exclosures do not typically manipulate primary dispersal. They ties increase (Beck et al., 2013; Ickes et al., 2001; Royo and also may not mimic increases in small mammal seed and seedling Carson, 2005). However, because defaunation also reduces seed predators caused by defaunation (Appendix A). dispersal, it is possible that seedling densities in defaunated forests will not show similar increases. Indeed, species do not respond 3.4.2. Diversity uniformly to defaunation. Species that are facultatively dispersed Over time, defaunated communities converge on composition and predated upon by scatter-hoarding rodents tend to be more with fewer species and lower evenness. Several short-term exclo- abundant in defaunated sites (Fig. 6). Likewise, the higher seedling sure studies have shown that species richness initially increases abundance of the elephant-dispersed Balanites wilsoniana, despite with herbivore removal (Fig. 7B), in contrast to expectations. How- reduced seed dispersal, was attributed to low seed and seedling ever, exclosure studies do not disrupt primary seed dispersal, and E.L. Kurten / Biological Conservation 163 (2013) 22–32 29

A B

Fig. 7. Community-level responses of (A) species richness, (B) seedling and herb densities and (C) species diversity indices to defaunation. Groups with different dispersal agents are denoted in parentheses. Richness and diversity for the Columbian field study is for different size classes. (#) = study number (Appendix C). rarefaction analyses suggest this may simply be an effect of stem was lower in defaunated sites (Nunez-Iturri et al., 2008; Stevenson densities initially increasing upon exclosure, with a corresponding and Aldana, 2008; Terborgh et al., 2008), while in Panama, the increase in rare species inside the exclosures (Theimer et al., 2011). community mean seed mass was higher in defaunated sites In forest comparisons, species richness was generally lower (1– (Wright et al., 2007b). The discrepancy may be due to differences 65%) as expected (Fig. 7B). Unlike short-term exclosure experi- in faunal communities. In Peru and Columbia, defaunation reduced ments, defaunated forests have generally experienced decades of populations of ateline dispersers (Nunez-Iturri et al., 2008; Steven- defaunation, likely allowing competitively dominant plant species son and Aldana, 2008), while not greatly affecting the relatively to outcompete rarer and less dominant species over time, reducing low populations of seed predators such as agoutis. In contrast, def- diversity. Consistent with this hypothesis, species dominance was aunation in Panama greatly reduced agouti populations (Wright higher in the cases that reported it (Alves-Costa, 2004; Dirzo and and Duber, 2001), but did not greatly affect seed dispersal by spi- Miranda, 1991; Royo and Carson, 2005). In forest comparisons, der monkeys, as these animals are absent even in several of the diversity indices in defaunated sites were generally lower (9– non-defaunated sites. 71%) than in non-defaunated sites (Fig. 7C). In exclosures, diversity Studies of indirect effects of defaunation on other functional indices appear to obscure changes in community composition, be- traits are rare. Leaf mass per area and leaf laminar toughness in cause the effects of increased species richness and increased dom- the seedling community did not change in response to defaunation inance tend to cancel each other out. or exclosure (Kurten, 2010). However, community mean leaf toughness and leaf nitrogen were lower and higher respectively in the saplings of an exclosure (Kurten, 2010), demonstrating that 3.4.3. Plant functional groups loss of terrestrial vertebrates favors less defended, higher leaf Plant traits vary along a number of functional trait axes, reflect- nutrient species. Community mean wood density was lower in ing trade-offs in life history strategies (Wright et al., 2007a). Where the forest comparison but unchanged in an exclosure study. This defaunation alters the relative favorability of various life-history is likely due to the fact that primary dispersal is altered in the for- strategies, changes in functional trait composition may occur est comparison, but not in the exclosure study; dispersal by game (Wright, 2003; Wright et al., 2007b). Specifically, defaunation species and higher wood densities are associated traits in that par- would disfavor species with hunted dispersal agents. Large-seeded ticular forest (Kurten, 2010). species may be disfavored or favored, depending upon whether the effect of reduced dispersal or escape from seed predation is larger. Species which are more or less palatable to herbivores will be fa- 3.5. Improving how we study defaunation vored by a reduction or increase in herbivory, respectively. As expected, species dispersed by game animals consistently Synthesizing responses to defaunation among studies is chal- show decreased abundances in defaunated sites, while species lenged by three limitations. The first is a lack of information on with abiotic or unhunted, biotic dispersal agents show higher the animal communities effecting the change. Few studies measure abundances (Nunez-Iturri et al., 2008; Terborgh et al., 2008; the abundances of the animals in their study sites, and many rely Wright et al., 2007b). As a corollary, lianas, which tend to be abiot- on proxies to classify sites into treatments, making no empirical ically dispersed (Muller-Landau and Hardesty, 2005), also have measurements of the animal community. Unfortunately, terms higher relative abundances in defaunated sites (Terborgh et al., such as ‘‘hunted’’, ‘‘fragmented,’’ or ‘‘disturbed’’ are often used as 2001; Wright et al., 2007b). proxies to classify sites into treatments, but do not correspond to Community seed mass responses differed among sites. In Peru a specific change in a vertebrate community (Fig. 1). Control sites and Colombia, the relative abundance of large-seeded species experience the same issue. In cases where hypotheses depend 30 E.L. Kurten / Biological Conservation 163 (2013) 22–32 upon the intensities of defaunation compared, where results are the whole, the impact of altered species interactions on recruit- contrary to expectation, or where studies produce contradicting re- ment as a consequence of defaunation is more often negative than sults, the absence of animal abundance data is a barrier to develop- positive. Additional mechanistic studies like that of Wright and ing meaningful insights into the mechanisms underlying the Duber (2001) are needed to refine our understanding of which differences. types of plant species are most vulnerable to decline as a conse- Low site replication is the second limitation. Half of the studies quence of defaunation, with a greater focus on the plant traits reviewed here had only one non-defaunated site and only 1–3 non- and environmental factors that mediate post-dispersal mortality. defaunated sites. Such low replication makes it difficult to distin- guish between biologically meaningful departures from expectation and variation in responses caused by spurious 4. Conclusions and future directions environmental, edaphic, or other site differences. This is particularly true for studies focusing on recruitment, diversity, and func- Though the effects of defaunation on diversity are generally tional trait composition. A third limitation is that, while many of negative, species-specific demographic responses of plants to def- the interactions and patterns reviewed here are hypothesized to aunation are highly variable. In general, large-seeded tree species vary with defaunation intensity, few studies evaluate plant re- relying on hunted dispersal agents are likely to suffer the greatest sponses at several levels of defaunation simultaneously. negative effects as a consequence of tropical defaunation. How- In short, empirically measuring animal species composition and ever, species which (1) experience weaker natural enemy-medi- abundances, expanding studies to more sites, and increasing the ated, negative density-dependent mortality, (2) do not require variation and range of defaunation intensities studied would better dispersal to special microenvironments, such as gaps (3) attract a facilitate hypothesis testing and data synthesis. Implementing variety of dispersal agents, and (4) escape seed predation due to these improvements is resource-intensive and logistically chal- their seed size and associated faunal community, have traits which lenging, though some remedies exist (Galetti and Dirzo, 2013). likely attenuate potential negative effects. In addition, limited evi- Due to the time and expense associated with quantifying animal dence suggests that highly defended, slow-growing species may be communities, a good first goal for the research community would disadvantaged by a loss of herbivores. Future work should move be to agree upon regional protocols for objectively characterizing beyond the study of isolated stages of the seed dispersal cycle for the animal communities we study on the basis of species occur- a limited number of large-seeded species. Studies should integrate rence (e.g. the index used here). Occurrence-based defaunation effects of defaunation on all processes from seed dispersal through indices serve as a first step toward a longer-term goal of imple- plant recruitment and broaden the scope of plant phylogenetic and menting vertebrate abundance-based indices of defaunation (e.g. functional diversity studied. Ironically, the regions that are experi- Giacomini and Galetti, 2013). encing the most severe defaunation, namely tropical Asia and Afri- ca, and the vertebrate groups most vulnerable to defaunation, 3.6. Linking species interactions, plant species recruitment, and particularly large ungulates and elephants, are also the most biodiversity understudied to date.

As has been shown previously (Markl et al., 2012; McConkey Acknowledgements et al., 2012), dispersal of large-seeded species generally decreases as a consequence of defaunation (Figs. 2A and 3, but see Fig. 2B). M. Galetti provided valuable feedback at various stages of this Seed dispersal networks (Donatti et al., 2011), studies of animal work. Comments from R. Dirzo, D. Ackerly and four anonymous diets (Section 3.2.1.4), and more clustered spatial distributions of reviewers greatly improved the manuscript. A graduate assistant- seeds and seedlings in defaunated forests (Fig. 3) all suggest that ship from the Stanford University Department of Biology sup- the ability of remaining dispersers to compensate for one another ported this work. when a system losses its most vulnerable vertebrate species is limited. However, the studies reviewed here also suggest that some large-seeded species may experience a benefit from defaunation, Appendices. Supplementary material in the form of reduced seed predation (Fig. 6). Reduced herbivory (Section 3.2.3) may provide similar benefits to plant species on Supplementary data associated with this article can be found, in the basis of their leaf traits (Kurten, 2010). the online version, at http://dx.doi.org/10.1016/j.biocon.2013. Does decreased dispersal necessarily translate to lower plant 04.025. recruitment, when other species interactions are changing concur- rently? Though seedling densities at the community level are gen- References erally lower in defaunated forests (Fig. 7A), species-specific plant responses to defaunation are highly variable, even among large- Ackerly, D.D., 2003. Community assembly, niche conservatism, and adaptive seeded species (Section 3.3). Only one study to date has simulta- evolution in changing environments. Int. J. Plant Sci. 164, S165–S184. neously measured changes in dispersal, seed predation, and seed- Adler, G.H., 1996. The island syndrome in isolated populations of a tropical forest rodent. Oecologia 108, 694–700. ling recruitment to understand the integrated impacts of Almeida-Neto, M., Campassi, F., Galetti, M., Jordano, P., Oliveira-Filho, A., 2008. defaunation on a single species (Wright and Duber, 2001). In that Vertebrate dispersal syndromes along the Atlantic forest: broad-scale patterns case, the decrease in vertebrate seed predation associated with and macroecological correlates. Glob. Ecol. Biogeogr. 17, 503–513. the defaunation outweighed the negative effects of reduced seed Alves-Costa, C.P., 2004. Efeitos da defaunação de mamíferos herbívoros na comunidade vegetal. Ph.D. Dissertation. Universidade Estadual de Campinas. dispersal and increased invertebrate seed predation, resulting in Andresen, E., 2003. Effect of forest fragmentation on dung beetle communities and higher seedling densities in defaunated sites. functional consequences for plant regeneration. Ecography 26, 87–97. This example, as well as the higher recruitment rates and abun- Andresen, E., Laurance, S.G.W., 2007. Possible indirect effects of mammal hunting on dung beetle assemblages in Panama. Biotropica 39, 141–146. dances of other species in defaunated sites (Figs. 5 and 6, and E1), Asquith, N.M., Wright, S.J., Clauss, M.J., 1997. Does mammal community illustrate the danger in assuming that reduced dispersal alone is composition control recruitment in Neotropical forests? Evidence from sufficient for reducing recruitment and abundance. That being said, Panama. Ecology 78, 941–946. Asquith, N.M., Terborgh, J., Arnold, A.E., Riveros, N., Carolina, N., 1999. The fruits the decreases in diversity and changes in functional trait composition agouti ate: Hymenaea courbaril seed fate when its disperser is absent. J. Trop. at the community level (Sections 3.4.1 and 3.4.2) suggest that on Ecol. 15, 229–235. E.L. Kurten / Biological Conservation 163 (2013) 22–32 31

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