Introduction

Abundant evidence now supports a role for vertebrate regulation of the structure and function of foodwebs [1]–[4]. While the majority of trophic cascade research has been conducted along plant-based pathways [5]–[7], comparatively little is known about cascade dynamics in along detritus pathways [7]. In particular, the fecal detritus pathway makes a major contribution to terrestrial nutrient cycles [8] and is expected to be sensitive to top-down regulation of the availability or diversity of fecal detritus inputs [6], [9]. Top-down regulation of the fecal detritus web may arise from tri-trophic indirect interactions, with implications for plants that are either negative (e.g. via predator-mediated reductions in detritivore densities) [5], or positive (e.g. via predator-mediated changes in detritivore behavior) [10].

Alternatively, predator-mediated reduction in herbivore fecal resource availability may instigate four-level trophic cascades along the fecal detritus web. For example, mammal overhunting in tropical forests is predicted to negatively impact fecal detritivore communities by reducing the diversity and availability of fecal detritus inputs from the game mammals targeted by rural hunters [11], [12]. These indirect impacts should further cascade to influence plant growth and demography by reducing rates of detrivore-mediated, plant-facilitating processes including nutrient cycling and secondary seed dispersal [10], [12], [13]. A range of cascading influences of human activity on tropical forest function has been explored along plant-based pathways [14], [15], but these effects have never been examined along fecal detritus-based pathways. Resolving these uncertainties is critical to a more complete understanding of the ecological impacts of human activity in tropical forests.

Along a 380-km gradient of human impact along the Juruá River in the western Brazilian Amazon (Fig. 1), we quantified the influence of human activity on a four-level fecal detritus-based pathway, composed of game mammals, fecal detritivores (i.e. Scarabaeine dung beetles), and fecal detritus process rates (i.e. dung beetle-mediated secondary burial of excreted seeds) [16]. We relied on these data to address two related questions.

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Figure 1. Map of study region.

Panels show location of: (top left) the state of Amazonas within Brazil, (top right) the two focal reserves within the state of Amazonas, and (bottom) the distribution of sampled communities (white circles) and settlement size (scaled to size of circle) within and immediately adjacent to the two focal reserves (the Médio Juruá Extractive Reserve and the Uacarí Sustainable Development Reserve). Shaded and white areas indicate terra firme and várzea forest, respectively.

https://doi.org/10.1371/journal.pone.0075819.g001

First, does human activity in tropical forest influence the community structure of fecal detritivores by decreasing the availability and diversity of mammal fecal inputs? The ability of trophic cascades to substantially alter the biomass or diversity of entire trophic levels (i.e. community-level cascades) remains controversial [17]. Community-wide cascades are considered unlikely in tropical terrestrial habitats [17], [18], as high spatial heterogeneity and high species and trait diversity [19]–[21] may lead to compensatory responses that mask the detection of community-level change [19]. However, top-down regulation of the fecal detritus web may result in community-level responses by fecal detritivores, given their strong dependence on game mammal feces [11], [12] and the lack of density or biomass compensation in perturbed dung beetle communities, particularly within the Neotropics [33].

Alternatively, the strength of trophic cascades may be driven by variation in values of species' trait important for trophic interaction [22]–[25]. Human activity-mediated reductions in the availability and diversity of game mammal feces are hypothesized to disproportionately penalize larger-bodied species whose reproductive output is most closely associated with the large fecal deposits of large-bodied game vertebrates [12]. Fecal resource decline may also differentially influence dung beetle species with different morphologies associated with feces handling and relocation (nesting). Species with ‘tunneler’ and ‘dweller’ strategies appear to be morphologically equipped to manipulate the soft fecal masses produced by those large-bodied primates that are targeted by rural hunters [26]. In contrast, ‘roller’ species commonly manipulate small, pelleted feces, and may more easily handle the feces of non-hunted, smaller-bodied mammals.

Second, can human impact-mediated trophic cascades influence a key detrital process - the secondary dispersal by dung beetles of seeds excreted in mammal feces? We used a field experiment to quantify the proportion of seeds buried by detrivores across a gradient of human impact. We expected that (i) heavier human impact would be correlated with reduced seed burial rates due to the indirect influence of hunting on community-level dung beetle biomass and diversity, (ii) the negative effects of human impact would be disproportionately strong for the largest sized seeds [27], and that (iii) the biomass of large-bodied beetle species would be most strongly correlated with seed dispersal rates across all seed sizes [36].

To better understand the generality of top-down trophic processes in fecal detritus webs, we explored these questions across two common Amazonian forest types. Upland forests (terra firme) represent the dominant forest type across the Amazon, and are associated with heavily leached and oligotrophic soils. Seasonally flooded forests (várzea) along white-water rivers account cover roughly 180,000 km² of the 7 million km² (2.6%) of the Amazon basin [28]. These forests differ dramatically in several factors that may influence cascade strength, including edaphic productivity [29], [30], vertebrate diversity [29], [31] and the seasonality and intensity of human resource use and access [32], including patterns of hunting and fishing [33].

Methods

Data Analysis

We examined the evidence for three distinct cascade structures, represented as either community-level (Fig. 2a, d) or trait-defined cascades (Fig. 2b, c, e, f). Each hypothesis was examined with two dung beetle metrics (i.e. species richness and total biomass) and analyzed separately for the two forest types (terra firme and várzea). We explored all models with both multiple generalized linear mixed models (GLMM) and generalized multilevel path analysis (GMPA) to examine the causal support for overall cascade structure with statistical controls [60].

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Figure 2. Three alternative trophic cascade structures along the detritus pathway in terra firme and várzea forest.

Cascade structures are represented as either community-level (A, D) or trait-defined (B–F). Mammal abbreviations include: primate (P), rodent (R) and ungulate (U). Dung beetle size classes include: small (S) and large (L). Dung beetle nesting strategies include: tunneler (T), roller (R) and dweller (D).

https://doi.org/10.1371/journal.pone.0075819.g002

To examine community-level cascades with generalized multiple linear mixed models, we modeled (i) game mammal abundance as a function of human impact (i.e. settlement size), (ii) dung beetle community species richness or biomass as a function of human impact and game mammal abundance, and (iii) the probability of seed burial as a function of human impact, game mammal abundance and dung beetle species richness or biomass. To discern which dung beetle community attribute (i.e. species richness or biomass) best explained seed burial probability, we compared two separate models including either beetle species richness or biomass with AIC-based model comparison.

To examine trait-defined cascades with a GLMM approach, we re-ran these same models after separating both the dependent and independent variables into groups defined by species traits relevant to trophic interactions. We separated game mammals into broad taxonomic groups (i.e. primate, ungulate and rodent) that both encounter differential selective hunting pressure (e.g. Jerozolimski and Peres 2003) and present distinct feces morphologies and deposition locations (i.e. arboreal vs. terrestrial) [9], [61] for dung beetles. We separated dung beetles into two distinct trait groups based on body mass (i.e. small: <0.1 g and large: ≥0.1 g) and nesting strategies (i.e. roller, tunneler or dweller). For terra firme models that included seed burial, we separated seeds into size classes (i.e. small: 2 mm <0.1 g, medium 5 mm: and large: 10 mm). To discern which property of dung beetle community structure (i.e. species richness or biomass) and trait-defined pathway (i.e. body size or nesting strategy) best explained seed burial probability, we compared four separate models for each seed size class with AIC-based model comparison. All analyses used beetle data taken from the 10 traps farthest (≥300 m) from the nearest mesocosm used to measure function to avoid potential bias in beetle capture rates. Ungulates and rodents were excluded from várzea forest models due to their rarity in this dataset. All predictors were centered on their means to facilitate interpretation. For all models, we used appropriate error structures (i.e. Poisson or Binomial) and incorporated both season (i.e. wet or dry) and transect identity as random effects in an unreplicated, crossed design [62].

To additionally assess the causal influence of human impact on cascade structure, we used generalized multilevel path models (GMPA) to examine the support for overall cascade structure [60]. GMPA is a generalization of Shipley's d-sep test, wherein a generalized linear mixed model (GLMM) can be used to test a series of related claims of independence in a path diagram. The hypothetical causal structure defined by a DAG can be tested with directional separation tests (d-sep) that quantify if the proposed model corresponds to the patterns of dependence or independence in the data [63]. This d-sep approach involves first finding the ‘basis set’ B_U of independence claims implied by a DAG that express the full set of dependence and independence claims implied by the causal graph, when taken as a set (e.g. Table S6). B_U is obtained by listing each of the k pairs of variables (X_i, X_j) in a causal graph that lack an arrow between them and then conditioning each of those k pairs by the set of variables Z that are either a direct cause of X_i or of X_j (Table S6). The probability p_i associated with each of the k independence claims in B_U is obtained using appropriate statistical tests (in our case, GLMMs). The overall hypothesized causal structure implied by the path diagram can then be tested by combining values of p_i using Fisher's test statistic C as:(1)The proposed causal model is rejected if the P value associated with the C statistic is smaller than the specified α-level (here, α = 0.05) after comparison to a chi-square (χ²) distribution with 2k degrees of freedom. A significant P value supports a rejection of the proposed DAG, as it implies that the data depart significantly from what would be expected under such a causal model [60].

We represented each of our three overall hypotheses about community and trait-defined trophic cascade structure with a DAG (Fig. 2) and tested the k independence claims implied by each proposed causal path models (see TS6). These GMPAs used identical model structures as the GLMMs described above. Values of p_i were taken from the P value associated with the t statistic for the regression coefficient of the composite variable. All analyses were conducted using the ‘nlme’ [64] package in the R environment [65].

Results

Across the 26 forest transects sampled for both mammals and dung beetles, we conducted a total of 8,430 km of mammal census walks (324±344 km, mean ±1 SD, range 80–1,260 km). These transects were associated with 15 neighboring human settlements, varying in size from five to 500 households (78±25.9 households, median ±1 SD). Human communities adjacent to terra firme or várzea forest sites were similar in both size (terra firme 22.5±29.5 households, várzea 19.3±23.3 households, mean ± SD, t₂₃ = 0.3, p = 0.76) and distance to censused transects (terra firme 0.78±0.39 km, várzea 0.84±0.35 km, mean ± SD, t₂₃ = −0.38, p = 0.78).

Mammal surveys resulted in observations of 38 species (see Table S1). Primates accounted for 38% of all individuals detected, followed by rodents (18%) and ungulates (16%). Of all species encountered, 58% are considered hunted game species in the region (unpublished data). The mean number of mammal individuals encountered was similar between terra firme and várzea sites (terra firme 1.27±1.4, várzea 0.90±0.78 individuals/km, mean ± SD, t₂₃ = 0.8, p>0.1), while terra firme sites supported significantly higher mammal species richness (terra firme 0.015±1.4, várzea 0.009±0.78 species/km, mean ± SD, t₂₂ = 3.2, p = 0.004).

A total of 10,819 dung beetle individuals in 90 species were captured (terra firme: N = 5,887, S = 83; várzea: N = 5,513, S = 57; see Table S2). Total beetle abundance per trap was higher in várzea forest (várzea: 19.5±29.3, terra firme: 15.4±15.0 individuals, mean ± SD, t₄₄₅ = −2.26, p = 0.001), while biomass and species richness were higher in terra firme (biomass: várzea 0.5±0.41, terra firme 0.73±0.53 g, mean ± SD, t₇₂₇ = 509, p<0.001; species richness: várzea 5.2±3.3, terra firme 6.3±3.9 species, mean ± SD, t₇₂₁ = 4.21, p = 0.001). There were no significant differences in mean individual beetle body mass between forest types (várzea: 0.10±0.08 g, terra firme: 0.11±0.07 g, mean ± SD, t₆₆₄ = 1.83, p = 0.10). Dung beetle biomass and species richness per trap were significantly higher in the dry season (biomass: dry 2.05±1.87 g, wet 0.89±856 g, mean ± SD, t₅₆₀ = 9.4, p<0.0001; richness: dry 7.0±3.9, wet 3.9±2.4 species, mean ± SD, t₅₆₀ = 11.0, p<0.0001).

Most dung beetle species were diurnal (67%) and used a tunneling nesting strategy (58%). For our analyses, a total of 68 species were classified as ‘small’ (i.e. <0.1 g; 0.022±0.02 g; mean ±1 SD, range 0.0001–0.092 g) and 31 species as ‘large’ (i.e. ≥0.1 g; 0.256±0.187 g; range 0.103–0.79 g). The distribution of nesting strategies across small and large species was similar, with the majority classified as ‘tunnelers’ (small: 64%; large: 68%), while ‘rollers’ represented 30% of small species and 20% of large species. The proportion of seed mimics (hereafter, seeds) removed by detritivores per forest site was greatest for large seeds, lowest for medium seeds and intermediate for small seeds (large 0.22±0.27; medium 0.19±0.18; small 0.20, ±0.13, mean ± SD; n = 15 for each).

Trait-defined cascade structures

Across trait-defined mammal groups, only hunted primates in terra firme forest showed a significant negative relationship with human impact (t₁₃ = −1.18, p = 0.026; all other p>0.05, see Table S3). Across beetle body-mass defined models in terra firme forests, rodent and ungulate abundances were unrelated to beetle body mass (all p>0.05, see Table S3A). In terra firme forests, both the biomass and species richness of small beetle species were negatively correlated with human impact (biomass z₂₄₄ = −2.76, p = 0.006; richness z₂₄₄ = −2.50, p = 0.013; Fig. 3A, C), yet remained independent of the abundance of all three mammal groups (all p>0.05, Table S4A). In contrast, the biomass and species richness of large beetle species were independent of human impact (all p>0.05, Fig. 3b,d see Table S4B), yet positively correlated with hunted primate abundance (biomass z₂₄₄ = 3.65, p = 0.013; richness z₂₄₄ = 1.86, p = 0.063; Fig. 3). Both small and large beetles were unrelated to the abundance of hunted rodents and ungulates abundances (all p>0.05, see Table S3A). Neither biomass nor species richness of small beetles in várzea forests were associated with human impact or primate abundance (all p>0.05, see Table S4B). Finally, we found strongly positive relationships in terra firme forests between both beetle species richness and abundance (r₁₃ = 0.95, p<0.0001) and biomass (r₁₃ = 0.86, p<0.0001), suggesting the absence of density or biomass compensation.

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Figure 3. Standardized regression coefficients (β) for GLM models of terra firme dung beetle biomass and species richness.

Models conducted separately for (A, C) small-bodied and (D, E) large-bodied beetle species; model terms include human impact and game mammal abundance.

https://doi.org/10.1371/journal.pone.0075819.g003

Across beetle nesting strategy-defined models, the biomass and species richness of all three strategies were independent of human impact in both terra firme and várzea forest (all p>0.05, see Table S4). In terra firme forest, the biomass of beetles with a ‘dwelling’ strategy was positively correlated with hunted primate abundance (z₂₄₄ = 2.03, p = 0.042). The biomass of species with a ‘roller’ strategy was negatively associated with game rodent abundance (z₂₄₄ = −1.98, p = 0.048), while the species richness of rollers was negatively correlated with ungulate abundance in terra firme forest (z₂₄₄ = −2.17, p = 0.03). In várzea forest, the abundance of hunted primates was unrelated to all measures of nesting strategy (all p>0.05, see Table S4B).

Trait-defined detritivore-mediated process rates

For all three seed size classes, the top AIC model included the biomass of body-mass-defined trait groups (Table S5). Human impact was unrelated to the probability of seed burial, irrespective of seed size (all p>0.05, Table S5). All classes of seed size showed a strong positive relationship between seed burial probability and the biomass of small-bodied beetles (large: z₁₅ = 2.87, p = 0.0041; medium: z₁₅ = 2.21, p = 0.027; small: z₁₅ = 2.05, p = 0.041), as well as ungulate abundance (large: z₁₅ = 4.29, p<0.0001; medium: z₁₅ = 2.87, p = 0.004; small: z₁₅ = 3.62, p<0.0001). The likelihood of small seed burial was negatively associated with primate abundance (z₅₉ = −2.51, p = 0.012, Fig. 4). Rodent abundance was unrelated to seed burial for all size classes (all p> 0.05, see Table S5B).

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Figure 4. Standardized regression coefficients (β) for GLM models of the probability of secondary seed burial.

Model terms include human impact, game mammal abundance and dung beetle biomass.

https://doi.org/10.1371/journal.pone.0075819.g004

Generalized multilevel path analysis approach

We found support for community-level (Fig. 2a, d), but not trait-defined (Fig. 2b, c, e, f) cascade structure in both terra firme and várzea forest and for both dung beetle community attributes (terra firme: biomass C₆ = 4.17, p = 0.65, species richness C₆ = 5.12, p = 0.53; várzea: biomass C₂ = 1.96, p = 0.37, species richness C₂ = 0.75, p = 0.69). Despite this strong overall model support, individual path coefficients from both forest types were weak (Fig. 5), and there was no evidence of significant relationships between any trophic level in either forest type.

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Figure 5. Model structure and standardized path coefficients from generalized multilevel path analysis.

Path coefficients (i.e. standardized regression coefficients) above each DAG of the detrital pathway in (A) terra firme and (D) várzea forests represent values for models based on dung beetle biomass; path coefficients below represent models based on dung beetle species richness. No path coefficients were significant at the α = 0.05 level.

https://doi.org/10.1371/journal.pone.0075819.g005

Discussion

To our knowledge, this represents the first landscape-scale study on the influence of human activity on the structure and function of the fecal detrital pathway. We show that human presence in tropical forests can influence the fecal detritus food web structure via body-size-dependent responses by detritivores. These indirect impacts on fecal detritivores occurred even in the absence of strong community-level responses by game mammals to human activities. Human presence in tropical forest was most strongly associated with declining abundance of large-bodied primate game species, as commonly observed elsewhere in tropical forests [26], [66]. We found no evidence that human activity indirectly influence rates of detritivore-mediated secondary seed dispersal rates. We also found few consistent relationships between beetle-mediated seed dispersal and game mammal abundance. Seed dispersal rates were positively associated with the biomass of small, but not large-bodied beetles – an unexpected finding given the previous empirical support for a dominant role of larger-bodied beetle species in the secondary dispersal of large seeds [16], [58], [67], [68]. Finally, we found stronger associations between dung beetles and both human presence and game mammal abundance in upland terra firme forests, compared to seasonally flooded várzea forests. Similar to other Neotropical studies, we detected no evidence of density or biomass compensation across the fecal detrivore community [69].

We found no consistent patterns of association between dung beetle nesting strategy and responses to human presence or game mammal abundance. Beetle species with a ‘dwelling’ strategy were positively associated with primate abundance in terra firme forest. In the Neotropics, all dwellers are strictly coprophagous members of a single genus (Eurysternus). In contrast, species with a ‘rolling’ nesting strategy were negatively associated with the abundance of both caviomorph rodents (i.e. Dasyprocta fuliginosa, Agouti paca) and ungulates (i.e. Mazama spp., Tapirus terrestris, Tayassu pecari, Pecari tajacu). While the predation of adult dung beetles by caviomorph rodents and ungulates is a possible explanation for these results [70], future manipulative studies will be required to understand the mechanisms behind these observed beetle-mammal associations.

We found stronger support for trophic effects defined by dung beetle body-size than those defined by nesting strategy. Contrary to our initial expectations [9], small-bodied beetle species were disproportionately sensitive to human presence in (upland) tropical forests. A similarly negative effect on small-bodied beetles was reported by Andresen and Laurance (2007) in Barro Colorado Island, Panama, even 15 years after hunting activity had ceased [11]. Culot et al. (2013) also reported that negative trends between mammal abundance and dung beetle species richness were stronger for smaller-bodied beetles [71]. In contrast, human impact was unrelated to the diversity and biomass larger-bodied beetles in either forest type. The combination of hunting pressure, and mammal avoidance near permanent human settlement may translate into ‘sinks’ of lower feces availability that disproportionately impact smaller beetle species with reduced dispersal abilities that are incapable of subsidizing their diet in neighboring patches with greater fecal resources. In contrast, the neutral response by large beetles to human activity may be a result of three potentially interacting phenomena: (1) dispersal-mediated buffering, (2) resource scarcity effects, and/or (3) the human subsidy effect.

First, the high vagility of large dung beetles may enable the detection and pursuit of fecal resources across wider spatial extents [72], which can buffer the fitness effects of local resource scarcity, relative to smaller beetles. Such effects may be more likely at early stages of defaunation, when local resource depletion operates in patches of higher and lower resources, rather than across an entire region.

Alternatively, the neutral abundance response of larger-bodied beetles in areas of human settled areas may arise from a positive relationship between local resource scarcity and capture rates [73], [74]. Such resource scarcity effects are a common practical issue for field studies that use attractive baits [75], are more likely to influence capture rates of larger individuals with elevated dispersal abilities, responding to food resources detected over wider spatial scales. Future work should attempt to determine the role of such scarcity effects on observational studies that report perplexingly strong and negative relationships between beetle abundance and mammal biomass [71]. Third and finally, local subsidies of human fecal resources may positively influence either the population density or observed capture rates of larger-bodied beetles, given the ready attraction of dung beetles to primate (including human) feces, and the frequent occurrence of open-air defecation in this study system (Nichols, pers. obs.). We consider this final alternative hypothesis to be relatively unlikely, both because a human fecal subsidy should positively influence small and large-bodied beetles, and because the positive impact of this subsidy should be tempered by the strongly negative abundance responses to the agricultural land-use that surround human settlements [76].

For large-bodied dung beetles in terra firme forest, we observed a decoupled response to human activity (neutral) and the abundance of large-bodied ateline primates (positive) that were themselves strongly impacted by human activity. This decoupled response may reflect the high demographic consequences of dispersal through the faunal depletion zone for large-bodied primates [38], [77], [78]; effects that may be relatively neutral for large-bodied beetles.

Any of these three of these size-biased processes may translate into a degree of functional ‘spatial insurance’ [72] across the heterogeneous fecal resource landscape of hunted tropical forests. The persistence of such spatial insurance is likely to be sensitive to activities that reduce connectivity between fecal resource patches, including increased mammal offtake around permanent human settlements and localized land-use changes following agricultural expansion. Taken together, these results suggest that the lasting human footprint on dung beetle persistence may accrue through two distinct pathways: early declines of small-bodied beetle species, compounded by subsequent declines of large-bodied specialists.

We found no relationship between human activity in tropical forest and detritivore-mediated rates of secondary seed dispersal. Strong attenuation between top-down forces and processes related to plant growth and demography are not uncommon in trophic cascade studies, particularly those that focus on density-mediated indirect interactions between predators and plants [79], [80]. We also found a strong, unexpected relationship between the biomass of small-bodied beetle species and the probability of burial for large seeds. These results differ from those reported from an identical experimental design in another western Amazonian site, where both the biomass and richness of larger-bodied beetles and richness (though not biomass) of small beetles were positively associated with large seed burial rate [81]. These contradictory results echo a lack of clear, consistent associations between dung beetle community attributes and beetle-mediated ecological function in observational studies [67], [74], [82].

We posit that part of this variability may arise from a widespread sampling artifact. In studies that collect data on ecological process rates and biodiversity in separate steps (i.e. through mesocosms and pitfall traps, as used here), differences in the size of the baits used to measure function (150 g) or attract beetle diversity in pitfalls (20 g) may introduce a large-beetle bias in ecological process measurements, as larger-bodied beetles can respond from greater distances to the larger scent plumes emitted by functional mesocosms. Horgan (2005) reported marked differences in observed beetle-function relationships when mesocosm data were compared with biodiversity data collected either directly within the mesocosms, or in neighboring pitfall traps (as used here). This suggests that size-biased sampling artifacts can indeed influence the observed correlations between dung beetle community attributes and function. This artifact can be overcome with simple modifications to the collection of either paired functional or biodiversity data.

We also found that forest type strongly mediated trophic cascade strength, with clearer evidence for human impact-induced cascade effects in terra firme, rather than várzea forests. These differences were strong, and are likely associated with the biological and socio-economic features unique to each forest types, despite their naturally close spatial proximity. Biomass of all vertebrates [83] and large-bodied primates in particular [84] can be orders of magnitude lower in upland, oligotrophic forests than in neighboring seasonally flooded forests [30], potentially leaving stronger signatures of co-decline in areas where hunting pressure was recently or historically high. In addition, as opportunistic hunting typically accompanies extractive and agricultural activities [45], [85], the year-round accessibility of terra firme forests, and location of manioc fields within terra firme sites may support the exploitation of large-bodied primates in upland forest, beyond the threshold at which active pursuit is predicted on the basis of hunting effort alone [86]. These general differences between terra firme and várzea forests were specifically present across our study region, where the two forest types differed in mean basal area [34], vertebrate community structure (this study; Endo unpublished) and patterns of human forest access and use [87], [88].

Finally, we found that our use of two analytical approaches (i.e. GLMM and GMPA) resulted in strikingly different assessments of both cascade structure and strength. Path analysis suggested that a community-level model of cascade structure was most appropriate for both forest types, a result potentially linked to the higher number of parameters in trait-defined models (see Table S6). Despite the support for these community models, the individual path coefficients linking trophic levels were weak, reflecting similar results to those reported from generalized linear mixed models. Taken together, these results highlight the complementarity of these analytical approaches, and suggest that further examination of the structure of trophic cascades along the fecal detritus pathway is warranted.

Our study also raises an interesting and currently underexplored issue, related to the net effects on ecological function of cascade dynamics in donor-controlled systems. When the indirect interactions that lead to detritivore decline are mediated by a reduction in the availability of detrital resources, and the ecological processes of interest result from the consumption of those detrital resources, does biodiversity loss beget a true net loss of ecological functioning? This question stems from the donor-controlled nature of the detritus pathway, and is generalizable to any detritus based system. While feedbacks between plants and plant consumers in green-world pathways largely determine overall cascade structure and strength [17], [89], the absence of interactions between detritus and detritus consumers has been alternatively proposed to weaken detrital cascades [90] or alternatively strengthen them relative to plant cascades, by tightly coupling consumption to resource depletion. A quantitative exploration of these questions will demand new information on the topology of ecological interaction networks formed by fecal detritus producers and consumers, as well as an improved understanding of the spatial dynamics of feces producer and consumer co-decline.

Our landscape-level study allowed us to detect evidence for a cascading impact of human activity on detritivores, but not detritivore-mediated processes [91]. Future manipulated experiments will be necessary to determine the mechanisms by which human activity influences cascade structure and strength in the fecal detritus web. In particularly, disentangling the potential influence of dung beetle mobility on cascade dynamics observed here will require additional attention to the spatial dimensions of trophic cascades [92], including spatial patterns of mammal defaunation [93], the interaction of beetle dispersal ability and fecal resource availability [94], and how spatial exchanges across areas exposed to variable levels of hunting pressure may affect dung beetle-mediated ecological process rates. Recent evidence also suggests that future inclusion of trait-mediated indirect interactions in cascade studies will be critical to understanding cascade dynamics in the fecal detritus systems [10]. Such mechanisms may include predator-mediated changes in detritivore behavior, physiology or even stoichiometry [95], [96], and importantly may strongly influence the observed functional and spatial relationships [97] between detritivores and plant-facilitating processes, even in the absence of obvious density-mediated effects [10]. Our findings provide the first landscape-scale evidence that human presence in tropical forests can influence the structure of fecal detritus pathways and support the ongoing prioritization of research that explores the impacts of human use of tropical forest on food web structure and function.

Supporting Information

Acknowledgments

We gratefully thank the communities of ResEx Médio Juruá and RDS Uacarí for their patience, insights and support, with particular thanks to field assistants Seu Antonio Jurití and Bola. Additional line-transect survey data was provided in partnership with the ProBUC program of the Centro Estadual de Unidades de Conservação, a division of the Amazonas State Secretariat for Environment and Development. This is publication No. 8 of the Projeto Médio Juruá series on resource management in Amazonian reserves.