Biological Conservation 163 (2013) 90–98

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Biological Conservation

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Special Issue: Defaunation’s impact in tropical terrestrial ecosystems Effects of collared peccary (Pecari tajacu) exclusion on leaf litter and reptiles in a Neotropical wet forest, Costa Rica ⇑ Kelsey E. Reider a, , Walter P. Carson b, Maureen A. Donnelly c a Florida International University, Department of Biological Sciences, OE 167, 11200 SW 8th St., Miami, FL 33199, United States b Department of Biological Sciences, University of Pittsburgh, Pittsburgh, PA 15260, United States c Florida International University, College of Arts and Sciences, ECS 450, 11200 SW 8th St., Miami, FL 33199, United States article info abstract

Article history: Peccaries are known to shape vegetation structure and create important breeding habitat for some pond- Available online 4 February 2013 breeding amphibians in Neotropical forests. Because peccaries are also important agents of disturbance and microhabitat variation in the litter, peccary loss could have important consequences for litter Keywords: amphibians and reptiles that depend entirely upon the litter for shelter, foraging and reproduction sites, Anuran and thermoregulation. However, very little is known about the effects of peccaries or their loss on litter Defaunation amphibians and reptiles. We experimentally reduced peccary density in 20 50 m fenced exclusion plots Ecosystem engineer (n = 5). We compared standing litter structure and and reptile abundance where peccaries Indirect effects were excluded to paired, open-forest control plots that had natural peccary densities. We encountered Microhabitat quality 16% more amphibian and reptile individuals in open control plots, and we encountered more juveniles of the most common anuran species in control plots than on peccary exclusions. Control plots had more compacted litter than peccary exclusion plots, indicating that peccaries alter the physical structure of the standing leaf litter in a way that promotes greater recruitment of juvenile anurans. Our results demon- strate that peccaries should be viewed not just as seed predators or ecosystem engineers for palms and pond-breeding amphibians, but also as important agents that affect leaf litter structure and abundance of terrestrial amphibians and reptiles. Peccary extirpation from overhunting or habitat degradation could have unexpected negative consequences for litter amphibians and reptiles, a diverse group already severely threatened by habitat loss, climate change, disease, and other anthropogenic effects worldwide. Ó 2012 Elsevier Ltd. All rights reserved.

1. Introduction et al., 2001; Wright and Duber, 2001; Bodmer and Ward, 2006; Peres and Palacios, 2007; Terborgh et al., 2008; Estes et al., 2011; The world’s tropical forests are under unrelenting pressure from Farwig and Berens, 2012). human activities, resulting in the tragic loss of plant and Most research on mammal defaunation has focused on its ef- species (Bradshaw et al., 2009). The goal of considerable ecological fects on plant diversity and distributions. Tapirs and peccaries research has been to quantify how biodiversity loss affects ecosys- are important seed dispersers and predators (Galetti et al., 2001; tem structure and function (Hooper et al., 2005; Hector et al., 2007; Beck, 2005; Keuroghlian and Eaton, 2008) and structure plant Thebault and Loreau, 2006; Isbell et al., 2011; Wardle et al., 2011). communities through seed dispersal, seed predation, and seedling Many Neotropical rainforest mammals affect plant diversity and trampling (Beck, 2006, 2007; Clark and Clark, 1989; Fragoso, 1997; structure, yet habitat loss, diseases, pollution, and overhunting Wright et al., 2000; Guariguata et al., 2000; Roldán and Simonetti, threaten mammal populations with extirpation (Bodmer et al., 2001; Silman et al., 2003; Paine and Beck, 2007; Keuroghlian and 1997; Peres, 2001; Grelle, 2005; Wilkie et al., 2011). Worldwide, Eaton, 2009). Defaunated and partially-defaunated forests may many otherwise intact tropical forests are at least partially defau- undergo shifts in plant diversity and density that, over time, could nated (Peres and Palacios, 2007; Michel and Sherry, 2012). The lead to changes in forest structure, ecosystem function, and elimination or reduction of large mammals, especially frugivores regeneration (Dirzo and Miranda, 1990; Redford, 1992; Terborgh and seed predators, poses a serious threat to biodiversity and com- et al., 2001; Wright et al., 2007). Because partial defaunation plicates forest conservation (Wright et al., 2000, 2007; Terborgh may result in mesoherbivore release with increased consumption of seeds and seedlings, mammal loss might have positive or negative effects on seed fate and seedling recruitment (Dirzo and ⇑ Corresponding author. Tel.: +1 305 348 6513; fax: +1 305 348 1986. Miranda, 1990; Asquith et al., 1997; Wright et al., 2007). The E-mail addresses: [email protected] (K.E. Reider), [email protected] (W.P. effects of large mammals likely go beyond impacts on tropical Carson), [email protected] (M.A. Donnelly).

0006-3207/$ - see front matter Ó 2012 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.biocon.2012.12.015 K.E. Reider et al. / Biological Conservation 163 (2013) 90–98 91 forest vegetation to the entire ecosystem and we expect mam- 2. Methods mal defaunation to have strong direct and indirect effects on other in tropical forests as well (see Wardle and Bardgett, 2.1. Study site 2004). Peccaries (collared, Pecari tajacu, and white-lipped, Tayassu Our research was conducted at the La Selva Biological Station pecari) are model systems to study the impact of large mammal (hereafter La Selva), located in the Caribbean lowlands of north- loss from Neotropical forests. Peccaries are large, often abundant eastern Costa Rica in Heredia Province (10°260N, 84°000W). The pri- mammals that contribute substantially to the mammalian biomass mary forest is described as lowland wet forest, located between in Neotropical forests, and have large home ranges (McCoy et al., 35 m and 137 m asl, and receives 4 m of precipitation annually 1990; Judas and Henry, 1999; Keuroghlian et al., 2004). Given with a mild dry season from January to April. See McDade and the rapid rates of deforestation and the potential for overhunting Hartshorn (1994) for a complete description of the site. La Selva by humans, the extirpation of collared and white-lipped peccaries is home to a robust collared peccary population. Collared peccaries is a possibility throughout the Neotropics (Beck, 2005; Beck et al., weigh 17–35 kg (Emmons, 1997; Desbiez et al., 2009) and at La 2008; Gongora et al., 2011; Altrichter et al., 2012). The cascading Selva can form groups of up to 30 individuals (K. Reider, pers. effects of peccary extirpation on Neotropical forests would likely obs.). Collared peccary density estimates for La Selva are 13–15 be substantial but only a handful of studies have investigated the individuals/km2 derived from radio-telemetry of a few peccary effects of peccaries on other animals. For example, peccaries re- groups (Torrealba-Suárez and Rau, 1993). Estimates from long- duce bruchid beetle populations through consumption of palm term camera trapping show that collared peccary relative abun- fruits (Beck, 2005; Wright et al., 2007). White-lipped peccaries in dance is 3–4 times higher at La Selva than the more seasonal and the Amazon are considered to be ecosystem engineers because isolated forests at Barro Colorado Island and Gigante, Panamá (N. they create wallows that hold water longer into the dry season Michel, personal communication). White-lipped peccaries (T. than do natural depressions. For many amphibians, wallows sup- pecari) were extirpated from the region by the mid-1900s (Timm, port reproductive activities and increase the anuran biodiversity 1994). of forests with peccaries (Gascon, 1991; Beck et al., 2010). Peccary loss would leave wallow-breeding anurans without access to crit- 2.2. Experimental design ical reproductive habitat (‘‘habitat split’’, Becker et al., 2009), and could result in population declines if pools are limited reproductive We used five mammal exclusion plots established in June 2000 in resources for forest . primary forest (Appendix I in Supplementary Material). Since March Peccaries alter soil and leaf litter through their foraging activ- 2009, the exclusion fences have been maintained to prevent access ities which include rooting, redistributing leaf litter, and tram- to plots by peccaries. The plots are 20 m 50 m and are surrounded pling of soil and litter (Beck, 2005; Keuroghlian and Eaton, by a 2 m high chain-link fence which is expected to exclude large, 2009). If ecosystem engineering by peccaries alters litter dynam- non-arboreal and non-volant mammals (e.g., deer, tapir, peccaries). ics and the detrital food web, peccary loss could affect the organ- Deer and tapir density at La Selva is very low (Timm, 1994) and we isms that depend on the leaf litter as primary habitat. The diverse did not observe deer or tapir sign near the plot locations during leaf litter amphibians and reptiles of moist tropical forest use leaf the 10 months of our study. Small terrestrial mammals like agoutis litter for foraging, reproduction, and retreat (Scott, 1976; Lieber- and armadillos have access to all exclusion plots through openings at man, 1986; Heinen, 1992). Litter amphibians are dominated by the soil surface that extend under the fences. To compare the effects direct-developing species in the families Eleutherodactylidae, of collared peccary presence and absence, we paired exclusion plots Strabomantidae, and that lack an aquatic tadpole with five control plots, which are completely open. All control and stage; adults and juveniles co-occur in the leaf litter covering exclusion plots were located 15–25 m from each other on the same the forest floor. Litter amphibians and lizards are prominent soil type to avoid confounding effects of soil on the litter amphibians among the top predators of invertebrates involved in the detrital and reptiles (Watling, 2005), on level ground, and at least 50 m from food web (Whitfield and Donnelly, 2006) and litter-dwelling pit streams. All data were collected from randomly determined points. vipers are among the top predators in tropical forests. Litter Measurements on controls and exclusions were collected by the amphibians and reptiles contribute substantially to the biomass same observer on the same day. No data were collected within 1 m of the detrital food web and represent important trophic links of the fences inside the exclusion plots to avoid fence effects. All plot among the detrital, aquatic, and arboreal food webs (Donnelly, locations will hereafter be referred to by their La Selva trail acro- 1991; Whitfield and Donnelly, 2006). Litter amphibians and rep- nyms (LOC2300, LOC2650, LS, SHO, and SSO). tiles are sensitive to changes in microhabitat structure because the leaf litter ameliorates the effects of desiccation and daily ther- mal fluctuations (Scott, 1976; Heinen, 1992). If peccary foraging 2.3. Mammal activity activities create sites for reproduction or thermoregulation, or promote the availability of arthropod prey, we would expect pec- To ensure that peccary activity and use of area inside exclusion cary loss to have a negative effect on amphibian and reptile pop- plots was lower than control plots, we deployed a pair of motion- ulations. Over time, defaunation or partial defaunation of activated cameras (Bushnell Trophy Camera Model 119405) in the peccaries could affect the abundance and demography of litter LOC2300, LOC2650, SHO, and LS control and exclusion plots in amphibian and reptile populations. July–August 2010, and June–July 2011. The cameras failed when To determine if collared peccary loss can affect litter amphibian they were placed in the SSO control and exclusion, and we were and reptile populations, we compared the relative abundance and not able to redeploy cameras there because of time constraints. community assembly of litter reptiles and amphibians in plots We placed the camera traps simultaneously inside peccary exclu- where peccaries were experimentally excluded and open control sion plots at tunnels under fences, and outside the fences on con- plots that allowed access by peccaries. Because litter amphibian trol plots. Cameras were attached to trunks of trees at a height of and reptile populations depend on litter for habitat and food, we approximately 50 cm. The cameras were set to take three photo- also examined correlates of litter quality (standing litter mass, graphs after each trigger event, with a 1 min. delay between trigger complexity, depth, and moisture), and understory vegetation events. When individuals appeared in multiple photos of the three density. taken, they were only counted once. Individuals may have been 92 K.E. Reider et al. / Biological Conservation 163 (2013) 90–98 counted more than once (e.g., as they entered and exited the plot, length (SUL) ranges given in Savage (2002). The leaf litter and or if they re-entered through the same hole later) and so we used understory up to 2 m were thoroughly but gently disturbed with our mammal monitoring data as an index of mammal activity in a 1 m long PVC probe to find litter amphibians and reptiles. Plot control plots and exclusions. We only made statistical comparisons sampling order, starting point, and direction of travel in each plot of mammal activity for periods where cameras were fully func- were randomized for each sampling session. We attempted to cap- tional in each pair of plots (SHO, LOC2300, LOC2650). ture, identify, and weigh all amphibians and reptiles (except ven- omous snakes). Captured animals were marked with a unique 2.4. Litter dynamics toe-clip code for identification of recaptures (except snakes, and juvenile anurans <10 mm SUL; Donnelly et al., 1994). Amphibians We compared litter fall in control and peccary exclusion plots and reptiles were identified in the field using Savage (2002) and using five 50 50 cm mesh litter traps that were placed at random Guyer and Donnelly (2005). locations within each plot, and moved to a new location every 2– 3 months. We determined the monthly average for each trap by 2.7. Statistical analyses pooling bi-weekly collections. Leaves, flowers, fruits, and leaf pet- ioles, but not logs or sticks, were collected from the traps. Litter fall We compared the number of all mammals and peccaries cap- samples were dried in an oven at 60 °C for 48 h and then weighed. tured in photos in control and exclusion plots using Wilcoxon Rank We estimated the standing litter mass by collecting litter from Sum tests using wilcox.test of the package stats in the statistical inside 25 25 cm quadrats (n = 6 in September, n = 9 in October– package R (R Development Core Team, 2011). November, and n = 15 from December–March) from random loca- We utilized generalized linear mixed models for most of our tions within control and peccary exclusion plots. We collected or- hypothesis testing because they can accommodate hierarchical ganic material within the quadrats (leaves, parts of leaves, and very experimental designs and handle non-normal data distributions small seed pods and fruits). Large seed pods and fruits, and coarse (Bolker et al., 2009). We analyzed the hypotheses that litter woody debris were not collected. We transported the litter sam- dynamics on control and exclusion plots were the same using lin- ples to the laboratory in sealed plastic bags to retain moisture. ear mixed effects models with the lme procedure of package nlme We determined moisture content by weighing the wet litter, oven in R (R Development Core Team, 2011). Dry litter-fall mass (g) and drying it (60 °C for 48 h), and weighing the dry litter. Dial calipers log-transformed standing litter mass (g) were used as response (±0.1 mm) were used to measure litter depth by piercing litter with variables, with peccary treatment as a fixed factor, and plot loca- the depth bar. The depth bar was extended and direct downward tion within sampling month as nested random factors. For litter force was exerted until the soil was contacted. Some litter com- depth and complexity we used monthly averages of litter depth pression was expected by the action but we expected it to have and the number of leaves as the response variables, with peccary no overall effect on relative depth as the same person took mea- treatment as a fixed effect, and sampling month and plot location surements in the same way in both exclusion and control plots. as crossed random effects. We used crossed random effects in anal- The number of leaves pierced by the depth bar was recorded as a yses where plot-wide measurements were averaged because spa- measure of litter complexity. Monthly rainfall averages were deter- tial pseudoreplication was not an issue. We compared canopy mined from open-source La Selva meteorological station data (OTS, density and understory density using a generalized linear mixed http://www.ots.ac.cr/meteoro/). effects models with the lmer procedure in the lme4 package in R. We included peccary treatment as the fixed effect, plot location 2.5. Vegetation density within sampling month as nested random effects. We specified binomial error distributions for the canopy density and visual In November 2009 and February 2011, we estimated understory obstruction proportions and Poisson errors for stem density vegetation density using a modified Robel pole for visual obstruc- counts. tion measurements (Vermeire et al., 2002). We fixed alternating We tested the hypothesis that peccaries affected the density of color bands (pink and black) to a 2.5 cm diameter PVC tube that amphibians and reptiles in peccary exclusion and control plots was 1 m in length. To measure vegetation density, an assistant held using a generalized linear mixed effects model with Poisson errors the tube horizontally 1 m above the ground. An observer standing using the lmer procedure described above. We used number of 5 m away from the tube reported the number of pink bands 25% or encounters per sample session (n = 3) each month (n = 4–8) as more visible on the tube. We counted understory stem density as the response variable. Peccary treatment was a fixed factor, and the number of stems within a 50 50 cm quadrats placed at 10 plot location and sample month were nested random factors. random locations in each plot in November 2009. We estimated Encounters include all new, recaptured, and escaped individuals. canopy cover over peccary exclusions and controls using a spheri- We repeated the lmer analysis for all amphibians, all reptiles, each cal densiometer to be sure that our plots were similar with respect of the four most common species encountered, and using only new to canopy openness. The densiometer was read in each cardinal captures during each sampling session. We calculated the recap- direction at 20 random points on each plot in November 2009 ture probability for each plot as: ((number of animals recaptured and December 2010. each sample session)/(the number of marked animals known to be alive during each sample session))/100. We compared recapture 2.6. Reptile and amphibian relative abundance probability in controls and exclusions using a t-test on the average recapture probability for each plot. Modified Visual Encounter Surveys (VES; Crump and Scott, We used permutational MANOVA with the Bray–Curtis dissim- 1994) were conducted in 20 20 m mark-recapture plots inside ilarity metric using call adonis in the package vegan (R Develop- each exclusion and control plot (n = 5). Surveys were conducted ment Core Team, 2011) to test for significant differences between in each pair of plots for three consecutive days every month (Octo- the amphibian and reptile communities encountered in control ber 2009–May 2010) by 1–2 observers walking at a set pace in a and exclusion plots. We identified potential indicator species in standardized pattern for 48 min/plot (2.5 m/min). We paused the the control and exclusion plots using the indval procedure in the sampling clock to identify, record, weigh, and measure each cap- labdsv package in R. The indval procedure evaluates indicator tured animal. We assigned individuals to age or size classes (juve- species by considering abundance and fidelity of the species in nile and adult) using the snout-vent length (SVL) or snout–urostyle different treatments. Indicator species for a treatment are both K.E. Reider et al. / Biological Conservation 163 (2013) 90–98 93 abundant and consistently found in that type of site, e.g. control different between treatments (t = 0.794, P = 0.43). There was no plots. We created rank-abundance curves and individual-based difference in leaf litter moisture content between peccary exclu- rarefaction curves for the controls and exclusions in the package sions and controls (t = 0.007, P = 0.995). Biodiversity R (R Development Core Team, 2011). 3.3. Understory vegetation density 3. Results There was no difference in understory vegetation density mea- 3.1. Mammal activity sured as stem density (t = 0.381, P = 0.70), or using the visual obstruction method (t = 1.079, P = 0.28) in control and exclusion Cameras were deployed for 97 trap days in control plots and plots. 152 trap days in exclusion plots. We recorded 286 mammal encounters in control plots and 117 encounters in exclusions. Pec- 3.4. Reptile and amphibian abundance and community composition caries accounted for only 1.7% of all mammal encounters in exclu- sion plots, compared to 27.0% of all mammal encounters in control We encountered 1907 reptiles and amphibians of 27 species plots. We conducted statistical analyses on 67 trap days when (Table 1). We encountered significantly fewer reptile and amphib- cameras were paired on control and exclusion plots (Appendix ian individuals in peccary exclusion plots compared to controls II). The total number of mammal encounters in control and exclu- (value = 0.158, SE = 0.046, z = 3.437, P < 0.001). We encountered sion plots was not significantly different (W = 18, P = 0.26). The significantly fewer amphibians in peccary exclusion plots com- number of peccary encounters in control plots was significantly pared to controls (value = 0.184, SE = 0.058, z = 3.19, P = 0.001; higher than it was in exclusion plots (W = 23.5, P = 0.01). Fig. 1). Peccary exclusions and controls were not different when we compared encounters of lizards alone (value = 0.139, 3.2. Litter dynamics SE = 0.0786, z = 1.762, P = 0.08), or all reptiles (value = 0.113, SE = 0.076, z = 1.480, P = 0.14). Encounters of most common Canopy density (t = 0.596, P = 0.55) and litter-fall mass did not species peaked in the dry season (Fig. 2). Encounters of juveniles differ between experimental treatments (t = 0.589, P = 0.56). Lit- of the most common species peaked in February and March ter mass did not differ between experimental treatments (Appendix III). There was no difference in encounter rates between (t = 0.153, P > 0.80). Peccary exclusion plots had approximately control and peccary exclusion plots for total encounters or new 20% deeper litter than controls (t=3.525, P = 0.001; Fig. 1). Litter individuals of the two most common amphibian species complexity was also greater in exclusion plots than control plots ( bransfordii and Oophaga pumilio) and lizards (Norops (t = 2.502, P = 0.01). Litter ground cover was not significantly quaggulus and N. limifrons). Of these four common species, C. bran- sfordii was significantly larger (snout–urostyle length) in exclusion plots than on controls (W = 7422, P = 0.01) and the probability of finding juvenile C. bransfordii was significantly higher in control plots than exclusion plots (v2 = 4.14, df =1,P (two-tailed) = 0.04). We found no difference in recapture probability of marked individuals between peccary exclusions and controls (t = 0.233, P = 0.82). The community analysis indicated that the assemblage of anu- rans in control and exclusion plots were significantly different (df = 1.66; F = 2.77; R2 = 0.04; P = 0.03). There was no difference in community composition of lizards (df = 1.66; F = 0.68, R2 = 0.1, P = 0.62) or when anurans and lizards were combined (df = 1.66; F = 1.62; R2 = 0.02; P = 0.10). The rank-abundance curves demon- strate that common species occurred in control and exclusion plots, while the rarefaction curves indicate that our sampling effort was sufficient (Appendix IV, V). The anuran species most responsi- ble for compositional differences between control and exclusion plots were Pristimantis cerasinus (indicator value = 0.497, P = 0.01) and Craugastor megacephalus (indicator value = 0.391, P = 0.005), which had high indicator species values in control plots.

4. Discussion

Although peccaries are found throughout Neotropical ecosys- tems (Altrichter et al., 2012), our study is the first to examine the effects of peccary exclusion on the abundance and diversity of other animals. We encountered 16% more amphibian and reptile individuals in control plots than on peccary exclusions, and 18% more anuran individuals in control plots than in exclusions. Fig. 1. Average litter depth and average amphibian and reptile encounters in Encounters of C. bransfordii, C. megacephalus, C. talamancae, Pristi- control and peccary exclusion plots. (a) Leaf-litter depth (mean ± 1 SE) in peccary mantis cerasinus, O. pumilio, N. quaggulus, and N. limifrons (which exclusion and open control plots. Litter was significantly deeper in peccary made up 90% of identified individuals) peaked in the dry season, exclusions compared to control plots. (b) Average monthly encounters (mean ± 1 and for most sampling months there was no difference in overall SE) in peccary exclusions and controls for all amphibians and reptiles. We encountered more amphibians and reptiles in control plots compared to peccary amphibian and reptile relative abundance as a result of peccary exclusions. exclusion. Overall densities of amphibians and reptiles differed 94 K.E. Reider et al. / Biological Conservation 163 (2013) 90–98

Table 1 Amphibians and reptiles encountered during 205 Visual Encounter Surveys from October 2009 to May 2010.

Taxon Exclosure Treatment Control (n = 5) Exclusion (n = 5) Total Amphibians Bufonidae Rhaebo haematiticus 2 2 Craugastoridae Craugastor bransfordii 179 174 353 C. fitzingeri 71 8 C. megacephalus 48 5 53 C. mimus 12 10 22 C. noblei 61016 C. talamancae 26 15 41 Strabomantidae Pristimantis cerasinus 66 36 102 P. ridens 56 11 Eleutherodactylidae Diaspora diastema 79 16 Microhylidae Gastrophryne pictiventris 1 1 Ranidae Lithobates warsczewitchii 22 4 Dendrobatidae Oophaga pumilio 241 230 471 Phyllobates lugubris 11 Unidentified 59 51 110 Lizards Teiidae Ameiva festiva 31 27 58 Corytophanidae Corytophanes cristatus 33 Polychrotidae Norops biporcatus 1 1 N. capito 86 14 N. carpenteri 13 4 N. quaggulus 201 178 379 N. lemurinus 1 1 N. limifrons 87 75 162 Scincidae Sphenomorphus cherriei 10 10 20 Unidentified lizard 18 11 29 Snakes Viperidae Bothrops asper 37 10 Bothriechis schlegelii 33 Porthidium nasutum 24 6 Dipsadidae Imantodes cenchoa 1 1 Unidentified snake 2 2 Unidentified amphibian/reptile 1 2 3 Total 1028 879 1907

between control and peccary exclusion plots most clearly in Febru- litter-fall between treatments, implying that decomposition rates ary, which coincides with peak reproductive activity of most litter were slowed in peccary exclusions. Decomposition of litter and frogs and reptiles (Guyer, 1986; Watling and Donnelly, 2002). other detritus fuels the diverse litter invertebrate community (Kas- We attribute the significantly higher litter reptile and amphib- pari and Yanoviak, 2009), which in turn comprise the majority of ian abundance in controls than exclusions to the emergence of prey items for most litter amphibians and reptiles (Whitfield and juveniles in February. We encountered higher relative abundances Donnelly, 2006). of the four common litter amphibians and two litter anoles in con- Peccary presence in control plots was associated with structural trol plots compared to peccary exclusions in February (Fig. 2). For differences in litter depth and complexity which implies microhab- these litter amphibians and reptiles, we observed an increase in the itat engineering by peccaries occurred there in addition to trophic abundance of juveniles that peaked higher in control plots than effects. Ecosystem engineering by peccaries has positive indirect exclusions (Appendix III). We encountered new individuals of Cra- effects on palm seedlings (Keuroghlian and Eaton, 2009), but our ugastor megacephalus and Pristimantis cerasinus, the control plot study provides the first evidence for effects of peccaries on other indicator species, nine times more frequently, and twice as fre- animals. Peccary exclusions had 20% overall deeper and signifi- quently in control plots compared to exclusions. If peccary distur- cantly more complex litter than control sites. Litter depth was bances, like trampling, had a negative effect on litter amphibian greater on exclusion plots for most of the year, except following and reptile clutch success or hatchling survival, we would have ex- the driest months when we observed a flush of new litter. The litter pected to find fewer juveniles in control plots compared to exclu- depth differences we detected at some times of the year (e.g., sions. Instead, peccary presence positively affected the abundance December) imply that peccary disturbances alter microhabitat of juveniles in control plots for the most common litter amphibians characteristics that are important for litter amphibians and reptiles and reptiles at La Selva. at other times of the year. Peccary trampling and mixing likely The positive effects of peccary presence on litter amphibians compacted litter in control plots. Litter arthropod communities and reptiles that we observed could occur via indirect trophic may be sensitive to variations in litter complexity and depth (Bult- and structural mechanisms. Peccary exclusion likely had cascading man and Uetz, 1984), and although deep litter has been correlated trophic effects on the detrital food web. By mixing litter and soil, with high abundance of terrestrial amphibians and reptiles (Scott, and through the addition of nutrients in urine and dung, peccaries 1976; Inger, 1980; Lieberman, 1986; Heinen, 1992; Whitfield and could influence litter decomposition and nutrient availability. Dee- Pierce, 2005), deep litter does not necessarily always make the best per litter in peccary exclusions compared to controls suggests habitat for amphibians and reptiles (Whitfield, 2011). There is either litter input is greater in exclusions or that decomposition some evidence that deep litter harbors more predatory spiders is slow compared to control plots. We detected no differences in (Bultman and Uetz, 1982) and deep litter in peccary exclusion plots K.E. Reider et al. / Biological Conservation 163 (2013) 90–98 95

Fig. 2. Monthly average encounters (mean ± 1 SE) for the most common litter amphibian and reptile species on control and peccary exclusion plots. (a) Craugastor bransfordii, (b) C. megacephalus, (c) C. talamancae, (d) Pristimantis cerasinus, (e) Oophaga pumilio, (f) Norops quaggulus, (g) N. limifrons. Species a–d are direct-developing litter anurans, e is a phytotelm-breeding litter anuran, f–g are litter-breeding anoline lizards.

could reduce amphibian and reptile abundance if predators are amphibians and reptiles. For most litter species, reproduction has more common there. never been described or is known from a single observation of a We know very little about the microclimate conditions suitable clutch (e.g., Whitfield and Pierce, 2003; Whitfield and Reider, to or preferred by litter frogs for foraging, refuges, and egg clutch 2009). Although litter depth was clearly equal in controls and pec- deposition and success, but these could be major avenues by which cary exclusions during the February peak juvenile abundance, litter litter-disturbing animals like peccaries interact with litter-dwelling conditions as far back as December could have affected clutch 96 K.E. Reider et al. / Biological Conservation 163 (2013) 90–98 success of species with longer development times. N. quaggulus (=N. white-lipped peccary extirpation. Experimental peccary exclusion humilis) clutches can take 2 months to hatch (Guyer and Donnelly, in sites that still have both peccary species would be extremely 2005). Perhaps deeper, less-disturbed litter inside the exclusion informative. plots provided fewer suitable locations for clutch deposition, or af- Because peccaries also create habitats like wallows that are fected clutch success by making eggs more susceptible to fungal exploited by other organisms (Beck et al., 2010), Zimmerman and infection or predation than the more compacted litter in controls. Bierregaard (1986) recommended that the minimum size of pre- The moist litter also provides a relatively stable thermal and humid serves for aquatic-breeding amphibians in the Amazon should be microclimate. Litter amphibians in Neotropical lowland forests may determined on the basis of the size of reserve required to sustain be living at or near their physiological thermal maxima, and may white-lipped peccary populations. If the results of our study can have a low capacity for physiological acclimation to warming (Huey be scaled up to the forest level, they suggest that collared peccary et al., 2010, 2012; Duarte et al., 2011). Peccary disturbances may loss could also have negative effects on terrestrial amphibians. One create more diverse thermal and humidity conditions in the leaf lit- of the most interesting results of our study is that the presence of ter that facilitate behavioral mechanisms which allow poikilo- peccaries had positive indirect effects on litter-dwelling amphibian therms to thermoregulate in a warming world. and reptile species with a diverse range of life-history strategies Indirect trophic and microhabitat effects of mammals on other (e.g., direct-developing anurans, litter-breeding anurans with phy- animals have been documented in other systems (e.g., large herbi- totelm-developing tadpoles, litter-breeding anoline lizards). vores on snakes in an African savanna, McCauley et al., 2006). Understanding the mechanisms driving patterns of terrestrial White-tailed deer (Odocoileus virginianus) exclusions in temperate amphibian abundance is especially important because amphibian systems have produced marked direct and indirect trophic effects populations are declining at La Selva (Whitfield et al., 2007) and on the detrital food web and litter amphibians and reptiles. Bres- worldwide (Stuart et al., 2004; Sodhi et al., 2008). High biodiversity sette et al. (2012) reported that deer exclusion reduced soil nutri- in tropical forests ensures that biotic interactions characterize the ents, led to deeper litter, and increased litter arthropod diversity, ecosystem, and as tropical forests lose species we can expect to see biomass, and density. Similar to our findings, Greenwald et al. the alteration of unexpected species interactions that may further (2008) reported that deer presence had a positive effect on litter compromise biodiversity and ecosystem function. We recommend arthropod, red-backed salamander, and eastern garter snake abun- that future studies and management decisions consider that the dance, likely via a combination of indirect trophic and structural loss of Neotropical forest peccary species is likely to have strong, mechanisms. In our system, additional data are required to deter- unexpected effects on both plants and other animals. mine how trophic and structural mechanisms contribute to in- creased amphibian and reptile abundance in sites with collared Acknowledgments peccaries. Future research could test explicitly for a trophic effect of peccary exclusion on the detrital food web by comparing soil This research was supported by the Organization for Tropical and foliar nutrient concentrations, litter decomposition, microbial Studies, Idea Wild, a Tinker Field Grant, the American Society of and fungal biomass, and litter and understory invertebrate and Ichthyologists and Herpetologists Gaige Award, and the Chicago predator abundance in the presence and absence of peccaries. Herpetological Society. Four anonymous reviewers and M. Galetti We found adults and juveniles of the common amphibians and improved the manuscript. The authors thank Saras Yerlig, Pamela reptiles in all control and exclusion plots, indicating that reproduc- Valle, Ryan Kindermann, Katie Heyer, Benjamin Shapiro, Orlando tion occurred inside all plots. Exclusion fence permeability is unli- Vargas, Danilo Brenes, and Bernal Matarrita for exceptional assis- kely to have been a confounding factor for all but the largest litter tance at La Selva. We thank Steven Oberbauer, Deron Burkepile, reptiles and amphibians, which were never (e.g., turtles) or only Kellie Kuhn, and the FIU Herpetology Lab for valuable suggestions. very rarely (e.g., large adult vipers) encountered in control plots. This is contribution number 243 to the FIU Tropical Biology Pro- The fence mesh size (3–5 cm) was larger than most litter-dwelling gram. Appropriate ethics (FIU IACUC 09-016 to MAD) and research frogs. We observed several adult frogs (1.9–5 cm SVL) and large liz- approvals (MINAET Resolución 145-2009-SINAC to KER) were ob- ards (10 cm SVL) pass through the fence. Fences also had wider tained for this research. openings (30–40 cm) and larger animals would have been guided by the fence to these access points. Measuring the abundance of cryptically-colored organisms can be problematic as a result of dif- Appendix A. Supplementary material ferences in detectability under different environmental conditions. Because we found no difference in the recapture probability of Supplementary data associated with this article can be found, in individual animals in control plots compared to exclusions, it is un- the online version, at http://dx.doi.org/10.1016/j.biocon.2012.12. likely our results can be explained by differences in detectability. 015. We found the same common species in control and exclusion plots, and although a few rare species were only found in controls or exclusion plots, peccary exclusion was not a strong driver of spe- References cies richness. Altrichter, M., Taber, A., Beck, H., Reyna-Hurtado, R., Lizarraga, L., Keuroghlian, A., Humans are the primary threat to large mammal populations in Sanderson, E., 2012. Range-wide declines of a key Neotropical ecosystem tropical forests (Peres, 2001; Schipper et al., 2008). Although La architect, the Near Threatened white-lipped peccary Tayassu pecari. Oryx 46, Selva lost its white-lipped peccaries, the site is not unusual in 87–98. the tropics. Many tropical forest sites have already lost a portion Asquith, N., Wright, S., Clauss, M., 1997. Does mammal community composition control recruitment in neotropical forests? Evidence from Panama. Ecology 78, of their large mammal fauna or experienced declines as a result 941–946. of anthropogenic activities, and at such sites, vegetation structure, Beck, H., 2005. Seed predation and dispersal by peccaries throughout the Neotropics biogeochemical cycling, and population dynamics of other animals and its consequences: a review and synthesis. In: Forget, P.M., Lambert, J.E., Hulme, P.E., Vander Wall, S.B. (Eds.), Seed Fate: Predation, Dispersal, and might be significantly altered. Researchers have long acknowl- Seedling Establishment. University Press, Cambridge, United Kingdom, pp. 77– edged how important seed predators like peccaries are in deter- 115. mining forest structure, and how detrimental altering the Beck, H., 2006. A review of peccary-palm interactions and their ecological ramifications across the Neotropics. J. Mammal. 87, 519–530. densities of seed predators could be for forests. Much of Central Beck, H., 2007. Synergistic impacts of ungulates and falling palm fronds on saplings America is a case study in what happens to tropical forests after in the Amazon. J. Trop. Ecol. 23, 599–602. K.E. Reider et al. / Biological Conservation 163 (2013) 90–98 97

Beck, H., Taber, A., Altrichter, M., Keuroghlian, A., Reyna, R., 2008. Pecari tajacu. In: Heinen, J.T., 1992. Comparisons of the leaf litter herpetofauna in abandoned cacao IUCN 2011: IUCN Red List of Threatened Species. Version 2011.1. plantations and primary rain-forest in Costa Rica – some implications for faunal (downloaded on 03.08.11). restoration. Biotropica 24, 431–439. Beck, H., Thebpanya, P., Filiaggi, M., 2010. Do Neotropical peccary species Hooper, D.U., Chapin, F.S., Ewel, J.J., Hector, A., Inchausti, P., Lavorel, S., Lawton, J.H., (Tayassuidae) function as ecosystem engineers for anurans? J. Trop. Ecol. 26, Lodge, D.M., Loreau, M., Naeem, S., Schmid, B., Setala, H., Symstad, A.J., 407–414. Vandermeer, J., Wardle, D.A., 2005. Effects of biodiversity on ecosystem Becker, C.G., Fonseca, C., Haddad, C., Prado, P., 2009. Habitat split as a cause of local functioning: a consensus of current knowledge. Ecol. Monogr. 75, 3–35. population declines of amphibians with aquatic larvae. Conserv. Biol. 24, 287– Huey, R.B., Losos, J.B., Moritz, C., 2010. Are lizards toast? Science 328, 832–833. 294. Huey, R.B., Kearney, M.R., Krockenberger, A., Holtum, J.A.M., Jess, M., Williams, S.E., Bodmer, R., Ward, D., 2006. Frugivory in large mammalian herbivore. In: Danell, K., 2012. Predicting organismal vulnerability to climate warming: roles of Bergstroem, R., Duncan, P., Pastor, J. (Eds.), Seed Fate: Predation, Dispersal, and behaviour, physiology and adaptation. Philos. Trans. Roy. Soc. B-Biol. Sci. 367, Seedling Establishment. University Press, Cambridge, United Kingdom, pp. 232– 1665–1679. 260. Inger, R.F., 1980. Densities of floor-dwelling frogs and lizards in lowland forests of Bodmer, R.E., Eisenberg, J.F., Redford, K.H., 1997. Hunting and the likelihood of southeast-Asia and Central-America. Am. Nat. 115, 761–770. extinction of Amazonian mammals. Conserv Biol. 11, 460–466. Isbell, F., Calcagno, V., Hector, A., Connolly, J., Harpole, W.S., Reich, P.B., Scherer- Bolker, B.M., Brooks, M.E., Clark, C.J., Geange, S.W., Poulsen, J.R., Stevens, M.H., Lorenzen, M., Schmid, B., Tilman, D., van Ruijven, J., Weigelt, A., Wilsey, B.J., White, J.S., 2009. Generalized linear mixed models: a practical guide for ecology Zavaleta, E.S., Loreau, M., 2011. High plant diversity is needed to maintain and evolution. Trends Ecol. Evol. 24, 127–135. ecosystem services. Nature 477, 199–202. Bradshaw, C.J.A., Sodhi, N.S., Brook, B.W., 2009. Tropical turmoil: a biodiversity Judas, J., Henry, O., 1999. Seasonal variation of home range of collared peccary in tragedy in progress. Front. Ecol. Environ. 7, 79–87. tropical rain forests of French Guiana. J. Wildlife Manage. 63, 546–555. Bressette, J., Beck, H., Beauchamp, V., 2012. Beyond the browse line: complex Kaspari, M., Yanoviak, S., 2009. Biogeochemistry and the structure of tropical brown cascade effects mediated by white-tailed deer. Oikos 121, 1–14. food webs. Ecology 90, 3342–3351. Bultman, T.L., Uetz, G.W., 1982. Abundance and community structure of forest floor Keuroghlian, A., Eaton, D.P., 2008. Fruit availability and peccary frugivory in an spiders following litter manipulation. Oecologia 55, 34–41. isolated Atlantic Forest fragment: effects of peccary ranging behavior and Bultman, T.L., Uetz, G.W., 1984. Effect of structure and nutritional quality of litter on habitat use. Biotropica 40, 62–70. abundances of litter-dwelling arthropods. Am. Midl. Nat. 11, 165–172. Keuroghlian, A., Eaton, D.P., 2009. Removal of palm fruits and ecosystem Clark, D.B., Clark, D.A., 1989. The role of physical damage in the seedling mortality engineering in palm stands by white-lipped peccaries (Tayassu pecari) and regime of a Neotropical rain-forest. Oikos 55, 225–230. other frugivores in an isolated Atlantic Forest fragment. Biodivers. Conserv. 18, Crump, M.L., Scott Jr., N.J., 1994. Visual encounter surveys. In: Heyer, W.R., 1733–1750. Donnelly, M.A., McDiarmid, R.W., Hayek, L.C., Foster, M.S. (Eds.), Measuring and Keuroghlian, A., Eaton, D.P., Longland, W.S., 2004. Area use by white-lipped and Monitoring Biological Diversity: Standard Methods for Amphibians. collared peccaries (Tayassu pecari and Tayassu tajacu) in a tropical forest Smithsonian Institution Press, Washington, DC, pp. 84–92. fragment. Biol. Conserv. 120, 411–425. Desbiez, A.L.J., Santos, S.A., Keuroghlian, A., Bodmer, R.E., 2009. Niche partitioning Lieberman, S.S., 1986. Ecology of the leaf litter herpetofauna of a Neotropical rain among white-lipped peccaries (Tayassu pecari), collared peccaries (Pecari forest: La Selva, Costa Rica. Acta Zool. Mex. 15, 1–72. tajacu), and feral pigs (Sus scrofa). J. Mammal. 90, 119–128. McCauley, D.J., Keesing, F., Young, T.P., Allan, B.F., Pringle, R.M., 2006. Indirect effects Dirzo, R., Miranda, A., 1990. Contemporary neotropical defaunation and forest of large herbivores on snakes in an African savanna. Ecology 87, 2657–2663. structure, function, and diversity – a sequel. Conserv. Biol. 4, 444–447. McCoy, M.B., Vaughan, C.S., Rodrigues, M.A., 1990. Seasonal movement, home range, Donnelly, M.A., 1991. Feeding patterns of the strawberry poison frog, Dendrobates activity and diet of collared peccaries (Tayassu tajacu) in Costa Rican dry forest. pumilio (Anura: Dendrobatidae). Copeia 1991 (3), 723–730. Vida Silvestre Neotrop. 2, 6–20. Donnelly, M.A., Guyer, C., Juterbock, E.J., Alford, R.A., 1994. Techniques for marking McDade, L.A., Hartshorn, G.S., 1994. La Selva biological station. In: McDade, L.A., amphibians. In: Heyer, W.R., Donnelly, M.A., McDiarmid, R.W., Hayek, L.C., Bawa, K.S., Hespenheide, H.A., Hartshorn, G.S. (Eds.), La Selva: Ecology and Foster, M.S. (Eds.), Measuring and Monitoring Biological Diversity: Standard Natural History of a Neotropical Rain Forest. University of Chicago Press, Methods for Amphibians. Smithsonian Institution Press, Washington, DC. Chicago, pp. 6–14. Duarte, H., Tejedo, M., Katzenberger, M., Marangoni, F., Baldo, D., Beltran, J.F., Marti, Michel, N., Sherry, T., 2012. Human-altered mesoherbivore densities and cascading D.A., Richter-Boix, A., Gonzalez-Voyer, A., 2011. Can amphibians take the heat? effects on plant and animal communities in fragmented tropical forests. In: Vulnerability to climate warming in subtropical and temperate larval Sudarshana, P., Nageswara-Rao, M., Soneji, J. (Eds.), Tropical Forests. InTech amphibian communities. Glob. Change Biol. 18, 412–421. Open Access Publisher. Emmons, L.H., 1997. Neotropical Rainforest Mammals: a Field Guide. University of Paine, C.E.T., Beck, H., 2007. Seed predation by Neotropical rain forest mammals Chicago Press, Chicago, USA, 307p. increases diversity in seedling recruitment. Ecology 88, 3076–3087. Estes, J.A., Terborgh, J., Brashares, J.S., Power, M.E., Berger, J., Bond, W.J., Carpenter, Peres, C.A., 2001. Synergistic effects of subsistence hunting and habitat S.R., Essington, T.E., Holt, R.D., Jackson, J.B.C., Marquis, R.J., Oksanen, L., Oksanen, fragmentation on Amazonian forest vertebrates. Conserv. Biol. 15, 1490– T., Paine, R.T., Pikitch, E.K., Ripple, W.J., Sandin, S.A., Scheffer, M., Schoener, T.W., 1505. Shurin, J.B., Sinclair, A.R.E., Soule, M.E., Virtanen, R., Wardle, D.A., 2011. Trophic Peres, C.A., Palacios, E., 2007. Basin-wide effects of game harvest on vertebrate downgrading of planet Earth. Science 333, 301–306. population densities in Amazonian forests: implications for animal-mediated Farwig, N., Berens, D.G., 2012. Imagine a world without seed dispersers: a review of seed dispersal. Biotropica 39, 304–315. threats, consequences and future directions. Basic Appl. Ecol. 13, 109–115. R Development Core Team, 2011. R: A language and environment for statistical Fragoso, J.M.V., 1997. Tapir-generated seed shadows: scale-dependent patchiness in computing. R Foundation for Statistical Computing, Vienna, Austria. (ISBN 3-900051-07-0). Galetti, M., Keuroghlian, A., Hanada, L., Morato, M., 2001. Frugivory and seed Redford, K., 1992. The empty forest. Bioscience 42, 412–422. dispersal by the lowland tapir (Tapirus terrestris) in southeast Brazil. Biotropica Roldán, A.I., Simonetti, J.A., 2001. Plant-mammal interactions in tropical Bolivian 33, 723–726. forests with different hunting pressures. Conserv. Biol. 15, 617–623. Gascon, C., 1991. Population-level and community-level analyses of species Savage, J.M., 2002. The Amphibians and Reptiles of Costa Rica: A Herpetofauna occurrences of central amazonian rain-forest tadpoles. Ecology 72, 1731– between Two Continents, between Two Seas. University of Chicago Press, 1746. Chicago, 934p. Gongora, J., Reyna-Hurtado, R., Beck, H., Taber, A., Altrichter, M., Keuroghlian, A., Schipper, J., Chanson, J.S., Chiozza, F., Cox, N., Hoffmann, M., et al., 2008. The status 2011. Pecari tajacu. In: IUCN 2011. IUCN Red List of Threatened Species. Version of the world’s land and marine mammals: diversity, threat, and knowledge. 2011.2. (downloaded on 15..11.11). Science 322, 225–230. Greenwald, K.R., Petit, L.J., Waite, T.A., 2008. Indirect effects of a keystone herbivore Scott Jr., N.J., 1976. The abundance and diversity of the herpetofaunas of tropical elevate local animal diversity. J. Wildl. Manage. 72, 1318–1321. forest litter. Biotropica 8, 41–58. Grelle, C.E.V., 2005. Predicting extinction of mammals in the Brazilian Amazon. Silman, M.R., Terborgh, J.W., Kiltie, R.A., 2003. Population regulation of a dominant- Oryx 39, 347–350. rain forest tree by a major seed-predator. Ecology 84, 431–438. Guariguata, M.R., Adame, J.J.R., Finegan, B., 2000. Seed removal and fate in two Sodhi, N.J., Bickford, D., Diesmos, A., Lee, T.M., Koh, L.P., Brook, B.W., Sekercioglu, selectively logged lowland forests with constrasting protection levels. Conserv. C.H., Bradshaw, C.J.A., 2008. Measuring the meltdown: drivers of global Biol. 14, 1046–1054. amphibian extinction and decline. PLoS ONE 3, e1636. Guyer, C., 1986. Seasonal patterns of reproduction of Norops-Humilis (Sauria, Stuart, S.N., Chanson, J.S., Cox, N.A., Young, B.E., Rodrigues, A.S.L., Fischman, D.L., Iguanidae) in Costa-Rica. Rev. Biol. Trop. 34, 247–251. Waller, R.W., 2004. Status and trends of amphibian declines and extinctions Guyer, C., Donnelly, M.A., 2005. Amphibians and Reptiles of La Selva, Costa Rica, and worldwide. Science 306, 1783–1786. the Caribbean Slope. University of California Press, Berkeley. Terborgh, J., Lopez, L., Nunez, P., Rao, M., Shahabuddin, G., Orihuela, G., Riveros, M., Hector, A., Joshi, J., Scherer-Lorenzen, M., Schmid, B., Spehn, E.M., Wacker, L., Ascanio, R., Adler, G.H., Lambert, T.D., Balbas, L., 2001. Ecological meltdown in Weilenmann, M., Bazeley-White, E., Beierkuhnlein, C., Caldeira, M.C., predator-free forest fragments. Science 294, 1923–1926. Dimitrakopoulos, P.G., Finn, J.A., Huss-Danell, K., Jumpponen, A., Leadley, P.W., Terborgh, J., Nunez-Iturri, G., Pitman, N.C.A., Valverde, F.H.C., Alvarez, P., Swamy, V., Loreau, M., Mulder, C.P.H., Nesshoever, C., Palmborg, C., Read, D.J., Pringle, E.G., Paine, C.E.T., 2008. Tree recruitment in an empty forest. Ecology 89, Siamantziouras, A.S.D., Terry, A.C., Troumbis, A.Y., 2007. Biodiversity and 1757–1768. ecosystem functioning: reconciling the results of experimental and Thebault, E., Loreau, M., 2006. The relationship between biodiversity and ecosystem observational studies. Funct. Ecol. 21, 998–1002. functioning in food webs. Ecol. Res. 21, 17–25. 98 K.E. Reider et al. / Biological Conservation 163 (2013) 90–98

Timm, R.M., 1994. The mammal fauna. In: McDade, L.A., Bawa, K.S., Hespenheide, Whitfield, S.M., Pierce, M.S.F., 2003. Eleutherodactylus noblei (NCN). Reproduction H.A., Hartshorn, G.S. (Eds.), La Selva: Ecology and Natural History of a and parental care. Herpetol. Rev. 34 (4), 357–358. Neotropical Rain Forest. University of Chicago Press, Chicago, pp. 229–237. Whitfield, S.M., Pierce, M.S.F., 2005. Tree buttress microhabitat use by a Neotropical Torrealba-Suárez, I.M., Rau, J.M.,1993. Biology of collared peccary groups Tayassu leaf-litter herpetofauna. J. Herpetol. 39, 192–198. tajacu and their damage provocated in crops neighboring La Selva Biological Whitfield, S.M., Reider, K., 2009. Craugastor bransfordii reproduction and nest site. Station, Costa Rica: Final report 1993. (Unpubl.) Universidad Nacional de Costa Herpetol. Rev. 40 (1), 70–71. Rica, Programa Regional Manejo de Vida Silvestre. Whitfield, S.M., Bell, K.E., Philippi, T., Sasa, M., Bolaños, F., Chaves, G., Savage, J.M., Vermeire, L.T., Ganguli, A.C., Gillen, R.L., 2002. A robust model for estimating Donnelly, M.A., 2007. Amphibian and reptile declines over 35 years at La Selva, standing crop across vegetation types. J. Range Manage. 55, 494–497. Costa Rica. Proc. Natl. Acad. Sci. USA 104, 8352–8356. Wardle, D.A., Bardgett, R.D., 2004. Human-induced changes in large herbivorous Wilkie, D.S., Bennett, E.L., Peres, C.A., Cunningham, A.A., 2011. The empty forest mammal density: the consequences for decomposers. Front. Ecol. Environ. 2, revisited. Ann. N.Y. Acad. Sci., Year Ecol. Conserv. Biol. 1223, 120–128. 145–153. Wright, S.J., Duber, H.C., 2001. Poachers and forest fragmentation alter seed Wardle, D.A., Bardgett, R.D., Callaway, R.M., Van der Putten, W.H., 2011. Terrestrial dispersal, seed survival, and seedling recruitment in the palm Attalea ecosystem responses to species gains and losses. Science 332, 1273–1277. butyraceae, with implications for tropical tree diversity. Biotropica 33, 583– Watling, J.I., 2005. Edaphically-biased distributions of amphibians and reptiles in a 595. lowland tropical rainforest. Stud. Neotrop. Fauna Environ. 40, 15–21. Wright, S.J., Zeballos, H., Dominguez, I., Gallardo, M.M., Moreno, M.C., Ibanez, R., Watling, J.I., Donnelly, M.A., 2002. Seasonal patterns of reproduction and abundance 2000. Poachers alter mammal abundance, seed dispersal, and seed predation in of leaf litter frogs in a Central American rainforest. J. Zool. 258, 269–276. a Neotropical forest. Conserv. Biol. 14, 227–239. Whitfield, S.M., 2011. Litter dynamics regulate population densities of amphibians Wright, S.J., Stoner, K.E., Beckman, N., Corlett, R.T., Dirzo, R., Muller-Landau, H.C., and reptiles in a declining tropical herpetofauna. In: Whitfield, S.M. Enigmatic Nunez-Iturri, G., Peres, C.A., Wang, B.C., 2007. The plight of large animals in faunal declines at La Selva, Costa Rica: Patterns and processes in a collapsing tropical forests and the consequences for plant regeneration. Biotropica 39, Neotropical herpetofauna, FIU Electronic Theses and Dissertations, Paper 435, 289–291. pp. 153–182. Zimmerman, B., Bierregaard, R., 1986. Relevance of the equilibrium-theory of island Whitfield, S.M., Donnelly, M.A., 2006. Ontogenetic and seasonal variation in the biogeography and species area relations to conservation with a Case from diets of a Costa Rican leaf-litter herpetofauna. J. Trop. Ecol. 22, 409–417. Amazonia. J. Biogeogr. 13, 133–143.