Nation-wide indicators of ecological integrity in Mexico: The status of mammalian apex-predators and their habitat

Ecological indicators that evaluate the status and trends of mammalian apex predators are necessary for monitoring the ecological integrity of landscapes. Several nation-wide spatial indicators that describe the status of apex predators after habitat transformation have been developed for México. These spatial indicators show the condition of the remnant natural landscape for maintaining the complexity of predator-prey interactions and habitat selection and use. The indicators were obtained using the concept of ecological integrity, that characterize the landscape based upon manifest and latent variables of naturalness, stability and self-organization, according with the measures of spatial distribution of species and natural habitat. When the current status is evaluated for individual species of apex predators, all species showed less than 50% of their distribution areas with a high degree of ecological integrity. Neotropical predators (such as jaguars and ocelots) are more threatened by the transformation of natural habitat, than their counterparts in Nearctic regions (e.g., bears, cougars, bobcats, and coyotes), which showed nonetheless, a high amount of their distribution areas with a high proportion of degraded habitat. The indicators allowed evaluating the status of still extant top predators in the landscape and their habitat condition within major ecoregions in the country.     

Non-linear relationship between body size of terrestrial carnivores and their trophic niche breadth and overlap

Studying food partitioning of mammalian predators is important for understanding trophic structures and interactions between coexisting carnivore species. This is particularly pertinent in the light of expanding ranges of populations of generalist species whose habitat and diet overlap with more specialized species. Here, we tested the resource partitioning hypothesis in terrestrial carnivores, predicting that trophic niche breadth and overlap relate positively to body mass. We used dietary data from 18 terrestrial carnivore taxa in four families (Canidae, Mustelidae, Felidae and Ursidae; body mass 0.1–173.6 kg) in three regions in Central and Eastern Europe, i.e. deciduous forest and forest-steppe region (DFR), temperate deciduous and mixed forest region (MFR) and transitory mixed forest regions (TFR). We ranked carnivores along an axis of trophic niche (breadth and overlap), and analysed the relationship between trophic niche and body mass (or pair-wise difference in body mass). A hierarchical cluster analysis of diet composition divided carnivores into four ecological groups: wild ungulate predators; small-mammal predators; amphibians and small mammal predators and omnivores. The relationship between body mass of predators and both trophic niche breadth and trophic niche overlap were hump-shaped. The trophic niche breadth to body mass ratio was significantly lower in DFR than in TFR and trophic niche overlap was significantly higher in DFR than in MFR and TFR. The predominant food resource is small mammals whose abundance is related to local agricultural and forestry management practices. Modifications of management techniques can affect population dynamics and community composition of carnivore species, especially in the case of small-mammal predators.     

Environmental change and predator diversity drive alpha and beta diversity in freshwater macro and microorganisms

Global biodiversity is eroding due to anthropogenic causes, such as climate change, habitat loss, and trophic simplification of biological communities. Most studies address only isolated causes within a single group of organisms; however, biological groups of different trophic levels may respond in particular ways to different environmental impacts. Our study used natural microcosms to investigate the predicted individual and interactive effects of warming, changes in top predator diversity, and habitat size on the alpha and beta diversity of macrofauna, microfauna, and bacteria. Alpha diversity (i.e., richness within each bromeliad) generally explained a larger proportion of the gamma diversity (partitioned in alpha and beta diversity). Overall, dissimilarity between communities occurred due to species turnover and not species loss (nestedness). Nevertheless, the three biological groups responded differently to each environmental stressor. Microfauna were the most sensitive group, with alpha and beta diversity being affected by environmental changes (warming and habitat size) and trophic structure (diversity of top predators). Macrofauna alpha and beta diversity was sensitive to changes in predator diversity and habitat size, but not warming. In contrast, the bacterial community was not influenced by the treatments. The community of each biological group was not mutually concordant with the environmental and trophic changes. Our results demonstrate that distinct anthropogenic impacts differentially affect the components of macro and microorganism diversity through direct and indirect effects (i.e., bottom‐up and top‐down effects). Therefore, a multitrophic and multispecies approach is necessary to assess the effects of different anthropogenic impacts on biodiversity.     

Biochemical tracers reveal intra-specific differences in the food webs utilized by individual seabirds

Food web structure regulates the pathways and flow rates of energy, nutrients, and contaminants to top predators. Ecologically and physiologically meaningful biochemical tracers provide a means to characterize and quantify these transfers within food webs. In this study, changes in the ratios of stable N isotopes (e.g., δ¹⁵N), fatty acids (FA), and persistent contaminants were used to trace food web pathways utilized by herring gulls (Larus argentatus) breeding along the shores of the St Lawrence River, Canada. Egg δ¹⁵N values varied significantly among years and were used as an indicator of gull trophic position. Temporal trends in egg δ¹⁵N values were related to egg FA profiles. In years when egg δ¹⁵N values were greater, egg FA patterns reflected the consumption of more aquatic prey. Egg δ¹⁵N values were also correlated with annual estimates of prey fish abundance. These results indicated that temporal changes in aquatic prey availability were reflected in the gull diet (as inferred from ecological tracer profiles in gull eggs). Analysis of individual eggs within years confirmed that birds consuming more aquatic prey occupied higher trophic positions. Furthermore, increases in trophic position were associated with increased concentrations of most persistent organic contaminants in eggs. However, levels of highly brominated polybrominated diphenyl ether congeners, e.g, 2,2′,3,3′,4,4′,5,5′,6,6′-decabromoDE (BDE-209), showed a negative relationship with trophic position. These contrasting findings reflected differences among contaminant groups/homologs in terms of their predominant routes of transfer, i.e., aquatic versus terrestrial food webs. High trophic level omnivores, e.g., herring gulls, are common in food webs. By characterizing ecological tracer profiles in such species we can better understand spatial, temporal, and individual differences in pathways of contaminant, energy, and nutrient flow.     

Evaluating the effects of large marine predators on mobile prey behavior across subtropical reef ecosystems

The indirect effect of predators on prey behavior, recruitment, and spatial relationships continues to attract considerable attention. However, top predators like sharks or large, mobile teleosts, which can have substantial top–down effects in ecosystems, are often difficult to study due to their large size and mobility. This has created a knowledge gap in understanding how they affect their prey through nonconsumptive effects. Here, we investigated how different functional groups of predators affected potential prey fish populations across various habitats within Biscayne Bay, FL. Using baited remote underwater videos (BRUVs), we quantified predator abundance and activity as a rough proxy for predation risk and analyzed key prey behaviors across coral reef, sea fan, seagrass, and sandy habitats. Both predator abundance and prey arrival times to the bait were strongly influenced by habitat type, with open homogenous habitats receiving faster arrival times by prey. Other prey behaviors, such as residency and risk‐associated behaviors, were potentially driven by predator interaction. Our data suggest that small predators across functional groups do not have large controlling effects on prey behavior or stress responses over short temporal scales; however, habitats where predators are more unpredictable in their occurrence (i.e., open areas) may trigger risk‐associated behaviors such as avoidance and vigilance. Our data shed new light on the importance of habitat and context for understanding how marine predators may influence prey behaviors in marine ecosystems.     

Superpredation patterns in four large European raptors

Predatory interactions among top predators, like superpredation or intraguild predation (IGP), can influence community structure. Diurnal raptors occupy high trophic levels in terrestrial food webs, and thus can regulate the presence of mesopredators. We studied superpredation (the killing and eating of another predator) in four large European raptors. We gathered 121 dietary studies, totalling 161,456 prey for the Goshawk Accipiter gentilis L., Golden Eagle Aquila chrysaetos L., Bonelli’s Eagle Aquila fasciata Vieillot, and Eagle Owl Bubo bubo L. Results showed that superpredation: (1) is a widespread interaction in large raptors, but it can vary according to the top predator species; (2) is not an important energetic resource for large raptors, but rather seems mostly related to diet diversification when the main prey decreases; (3) is spatially clustered reflecting habitat heterogeneity, but shows no temporal or large-scale spatial trends; and (4) it is associated with lower breeding success of the top predator species. These findings support the food stress hypothesis as the main driving force behind increases in superpredation and IGP in raptors, with the decrease in breeding performance as a side effect. Superpredation by large raptors deserves future research to understand its effects on mesopredators, because on one hand it might contribute to promote biodiversity, while on the other hand, it can sometimes represent an additional risk for small populations of endangered mesopredators.     

Stable isotopes, ecological integration and environmental change: wolves record atmospheric carbon isotope trend better than tree rings

Large-scale patterns of isotope ratios are detectable in the tissues of organisms, but the variability in these patterns often obscures detection of environmental trends. We show that plants and animals at lower trophic levels are relatively poor indicators of the temporal trend in atmospheric carbon isotope ratios (delta13C) when compared with animals at higher trophic levels. First, we tested how differences in atmospheric delta13C values were transferred across three trophic levels. Second, we compared contemporary delta13C trends (1961-2004) in atmospheric CO2 to delta13C patterns in a tree species (jack pine, Pinus banksiana), large herbivore (moose, Alces alces) and large carnivore (grey wolf, Canis lupus) from North America. Third, we compared palaeontological (approx. 30000 to 12000 14C years before present) atmospheric CO2 trends to delta13C patterns in a tree species (Pinus flexilis, Juniperus sp.), a megaherbivore (bison, Bison antiquus) and a large carnivore (dire wolf, Canis dirus) from the La Brea tar pits (southern California, USA) and Great Basin (western USA). Contrary to previous expectations, we found that the environmental isotope pattern is better represented with increasing trophic level. Our results indicate that museum specimens of large carnivores would best reflect large-scale spatial and temporal patterns of carbon isotopes in the palaeontological record because top predators can act as ecological integrators of environmental change.     

Inside‐container effects drive mosquito community structure in Brazilian Atlantic forest

Metacommunity theory is a convenient framework in which to investigate how local communities linked by dispersal influence patterns of species distribution and abundance across large spatial scales. For organisms with complex life cycles, such as mosquitoes, different pressures are expected to act on communities due to behavioral and ecological partitioning of life stages. Adult females select habitats for oviposition, and resulting offspring are confined to that habitat until reaching adult stages capable of flight; outside‐container effects (OCE) (i.e., spatial factors) are thus expected to act more strongly on species distributions as a function of adult dispersal capability, which should be limited by geographic distances between sites. However, larval community dynamics within a habitat are influenced by inside‐container effects (ICE), mainly interactions with conspecifics and heterospecifics (e.g., through effects of competition and predation). We used a field experiment in a mainland‐island scenario to assess whether environmental, spatial, and temporal factors influence mosquito prey and predator distributions and abundances across spatial scales: within‐site, between‐site, and mainland‐island. We also evaluated whether predator abundances inside containers play a stronger role in shaping mosquito prey community structure than do OCE (e.g., spatial and environmental factors). Temporal influence was more important for predators than for prey mosquito community structure, and the changes in prey mosquito species composition over time appear to be driven by changes in predator abundances. There was a negligible effect of spatial and environmental factors on mosquito community structure, and temporal effects on mosquito abundances and distributions appear to be driven by changes in abundance of the dominant predator, perhaps because ICE are stronger than OCE due to larval habitat restriction, or because adult dispersal is not limited at the chosen spatial scales.     

Scale issues in the study of primate foraging: red colobus of Kibale National Park

Diet data have been used to address a number of theoretical issues. We often calculate the proportion of time spent eating different foods (e.g., fruits, leaves) to place species into dietary categories and contrast morphological or behavioral traits among categories. Yet we have little understanding of how flexible species can be in terms of the plant parts and species consumed. To address this issue, we analyzed data on the diets of red colobus monkeys (Procolobus badius) from Kibale National Park, Uganda, to evaluate temporal and spatial variability in the plant parts and species eaten. After considering observer differences and sampling issues, we evaluated how different a group's diet could be if samples were taken in different years. We found that the diet of the same groups showed significant, consistent changes over a 4-year period. For example, the time spent feeding on leaves increased from 56% in 1994 to 76% in 1998. The plant parts and species eaten by eight groups inhabiting different types of forest (e.g., pristine, logged, riverine) varied among groups. The largest interdemic difference was seen in the use of young leaves (38%). Dietary differences were also found between groups with overlapping home ranges (41-49% overlap). Different subspecies of Procolobus badius also varied in diet; however, this variation was often not of the magnitude documented within Kibale for the same population. The fact that diet can vary considerably over small spatial and short temporal scales within the same species raises the intriguing question as to what level of interspecific difference is biologically significant for addressing particular questions. We conclude that behavioral flexibility blurs our traditional stereotypic assessment of primates; a study of one group that occupies a specific habitat at one point in time may not adequately represent the species.     

Spatial patterns and dynamic responses of arctic food webs corroborate the exploitation ecosystems hypothesis (EEH)

According to the exploitation ecosystems hypothesis (EEH), productive terrestrial ecosystems are characterized by community-level trophic cascades, whereas unproductive ecosystems harbor food-limited grazers, which regulate community-level plant biomass. We tested this hypothesis along arctic-alpine productivity gradients at the Joatka field base, Finnmark, Norway. In unproductive habitats, mammalian predators were absent and plant biomass was constant, whereas herbivore biomass varied, reflecting the productivity of the habitat. In productive habitats, predatory mammals were persistently present and plant biomass varied in space, but herbivore biomass did not. Plant biomass of productive tundra scrublands declined by 40% when vegetation blocks were transferred to predation-free islands. Corresponding transfer to herbivore-free islands triggered an increase in plant biomass. Fertilization of an unproductive tundra heath resulted in a fourfold increase in rodent density and a corresponding increase in winter grazing activity, whereas the total aboveground plant biomass remained unchanged. These results corroborate the predictions of the EEH, implying that the endotherm community and the vegetation of the North European tundra behaves dynamically as if each trophic level consisted of a single population, in spite of local co-occurrence of >20 plant species representing different major taxonomic groups, growth forms, and defensive strategies.     

Spatial and seasonal patterns of fish assemblages in mountain streams of the Ren River,southwest China

The spatial–temporal patterns of fish assemblages in lotic systems can provide useful information in developing effective conservation measures. This study aimed to explore the spatial and seasonal changes in fish assemblages and their association with environmental factors in mountain streams of the Ren River, southwest China. Field investigations were conducted at 18 sites during the rainy and dry seasons in 2017. A total of 1,330 individuals, belonging to three orders, eight families, 19 genera, and 21 species, were collected. Analysis of similarities (ANOSIM) showed that the structure of fish assemblages varied significantly at the spatial scale, but not at the seasonal scale. In low‐order sites, fish assemblages were mainly dominated by cold‐water and rheophilic species (e.g., Rhynchocypris oxycephalus, Scaphesthes macrolepis, Metahomaloptera omeiensis, and Gnathopogon herzensteini), while those in high‐order sites were predominated by warm‐water and eurytopic or stagnophilic species (e.g., Squalidus argentatus, Hemiculter leucisculus, and Zacco platypus). Canonical correspondence analysis (CCA) showed that the fish assemblages were structured by a combination of large‐scale landscape factors (e.g., altitude and C‐link) and small‐scale habitat features (e.g., channel width, water temperature, and depth). Among these factors, landscape had the greatest influence on fish assemblages, while local habitat variables were less important or were only significant in certain seasons.     

Invasive species cause large-scale loss of native California oyster habitat by disrupting trophic cascades

Although invasive species often resemble their native counterparts, differences in their foraging and anti-predator strategies may disrupt native food webs. In a California estuary, we showed that regions dominated by native crabs and native whelks have low mortality of native oysters (the basal prey), while regions dominated by invasive crabs and invasive whelks have high oyster mortality and are consequently losing a biologically diverse habitat. Using field experiments, we demonstrated that the invasive whelk’s distribution is causally related to a large-scale pattern of oyster mortality. To determine whether predator–prey interactions between crabs (top predators) and whelks (intermediate consumers) indirectly control the pattern of oyster mortality, we manipulated the presence and invasion status of the intermediate and top trophic levels in laboratory mesocosms. Our results show that native crabs indirectly maintain a portion of the estuary’s oyster habitat by both consuming native whelks (density-mediated trophic cascade) and altering their foraging behavior (trait-mediated trophic cascade). In contrast, invasive whelks are naive to crab predators and fail to avoid them, thereby inhibiting trait-mediated cascades and their invasion into areas with native crabs. Similarly, when native crabs are replaced with invasive crabs, the naive foraging strategy and smaller size of invasive crabs prevents them from efficiently consuming adult whelks, thereby inhibiting strong density-mediated cascades. Thus, while trophic cascades allow native crabs, whelks, and oysters to locally co-exist, the replacement of native crabs and whelks by functionally similar invasive species results in severe depletion of native oysters. As coastal systems become increasingly invaded, the mismatch of evolutionarily based strategies among predators and prey may lead to further losses of critical habitat that support marine biodiversity and ecosystem function. Electronic supplementary material  The online version of this article (doi:) contains supplementary material, which is available to authorized users.     

Spatial and temporal patterns of seed predation on three tree species in an oak-pine forest

We experimentally examined spatial and temporal patterns of seed predation on three tree species in an oak-pine forest in southern Maine. USA, Rodents were the principal seed predators. Rates of seed loss varied with tree species and exposure to three different suites of potential seed predators (all vertebrate seed predators, medium-sized rodents [primarily squirrels] and small rodents [primarily mice and voles]), Acer rubrum seeds were removed more slowly (mean of 17.7% within 2 d across all habitats and treatments in 1991) than seeds of either Quereus rubra or Pinus strobus (e,g., > 99% removed within 2 d across all habitats and treatments for each species in 1991), Levels of final removal (cumulative removal at final census) varied with year but not with microhabitat; i.e., seed predation in four types of forest gap was not significantly different than in intact forest. Both field data and experimental feeding trials with captive Peromyscus leucopus and Clethrionomys gapperi suggest that a significant proportion of while pine seeds is eaten at time of detection, while red oak acorns are more likely to be cached. Captive Peromyscus leueopus cached and ate significantly more red oak acorns than Clethrionomys gapperi. These results suggest that red oak mast may be more important in overwintering success in Feromyscus than in Clethrionomys. Nevertheless, both species did consume red oak acorns, suggesting that in southern Maine these species are not substantially inhibited by high tannin levels in red oak acorns, as has been suggested by researchers elsewhere.     

Novel tri‐isotope ellipsoid approach reveals dietary variation in sympatric predators

Sympatric species may partition resources to reduce competition and facilitate co‐existence. While spatial variation and specialization in feeding strategies may be prevalent among large marine predators, studies have focussed on sharks, birds, and marine mammals. We consider for the first time the isotopic niche partitioning of co‐occurring, teleost reef predators spanning multiple families. Using a novel tri‐isotope ellipsoid approach, we investigate the feeding strategies of seven of these species across an atoll seascape in the Maldives. We demonstrate substantial spatial variation in resource use of all predator populations. Furthermore, within each area, there was evidence of intraspecific variation in feeding behaviors that could not wholly be attributed to individual body size. Assessing species at the population level will mask these intraspecific differences in resource use. Knowledge of resource use is important for predicting how species will respond to environmental change and spatial variation should be considered when investigating trophic diversity.     

Predation risk and habitat complexity modify intermediate predator feeding rates and energetic efficiencies in a tri‐trophic system

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Above and below ground impacts of terrestrial mammals and birds in a tropical forest

Understanding the impact of losing trophic diversity has global significance for managing ecosystems as well as important theoretical implications for community and ecosystem ecology. In several tropical forest ecosystems, habitat fragmentation has resulted in declines and local extinctions of mammalian and avian terrestrial insectivores. To assess the ability of a tropical rainforest community in Ivory Coast to resist perturbation from such loss of trophic diversity, I traced feedbacks in above and below ground communities and measured changes in nutrient levels and herbivory rates in response to an experimental exclosure of avian and mammalian terrestrial insectivores. I present evidence that loss of this functional group may result in increased tree seedling herbivory and altered nutrient regimes through changes in the abundance and guild structure of invertebrates. Exclusion of top predators of the forest floor resulted in increased seedling herbivory rates and macro-invertebrate (>5 mm) densities with strongest effects on herbivorous taxa, spiders and earthworms. Densities of microbivores including Collembola, Acarina and Sciaridae showed the opposite trend as did levels of inorganic phosphorus in the soil. Results were evaluated using path analysis which supported the presence of a top down trophic cascade in the detrital web which ultimately affected turnover of phosphorus, a limiting nutrient in tropical soils. Results illustrate the potential importance of vertebrate predators in both above and belowground food webs despite the biotic diversity and structural heterogeneity of the rainforest floor.     

Habitat overlap of enemies: temporal patterns and the role of spatial complexity

Environmental heterogeneity can promote coexistence of conflicting species by providing spatial or temporal refuges from strong interactions (e.g., intraguild predation, competition). However, in many systems, refuge availability and effectiveness may change through time and space because of variability in habitat use by either species. Here I consider how the intensity of intraguild predation risk varies from day to night for aquatic insects that use both vegetated and open water habitats. Large (1,265 l) and small (42 l) mesocosms were used to test the hypothesis that Buenoa would choose an open-water habitat that minimized predation by the ambush predator Notonecta during the day, but that at night Buenoa would safely use both vegetated and open water. Regardless of container size, Notonecta remained in vegetated water during the day and exploited both habitats at night, despite exhibiting greatest instantaneous predation rates in open water during the day. In contrast, Buenoa maintained an even distribution throughout the mesocosms during day and night, even though habitat-specific predation risks were fivefold lower in open waters than in vegetation during the day and habitat-specific predation risk would have been reduced threefold by fully exploiting open waters. Thus, temporal heterogeneity was both beneficial and detrimental to Buenoa; darkness of night reduced predation, but spatial refuges also disappeared. Together, these patterns suggest that while environmental heterogeneity can dampen intense biotic interactions, enemies do not select habitats solely on the basis of conflict avoidance. Instead, it appears that habitat-specific variation in other biotic (e.g., visual predators) or physical factors (e.g., UV radiation) may also mediate species interactions by influencing habitat selection.     

Why are predators more sensitive to habitat size than their prey? Insights from bromeliad insect food webs

Ecologists have hypothesized that the exponent of species-area power functions (z value) should increase with trophic level. The main explanation for this pattern has been that specialist predators require prior colonization of a patch by their prey, resulting in a compounding of the effects of area up trophic levels. We propose two novel explanations, neither of which assumes trophic coupling between species. First, sampling effects can result in different z values if the abundances of species differ (in mean or evenness) between trophic levels. Second, when body size increases between trophic levels, effects of body size on z values may appear as differences between trophic levels. We test these alternative explanations using invertebrate food webs in 280 bromeliads from three countries. The z value of predators was higher than that of prey. Much of the difference in z values could be explained by sampling effects but not by body size effects. When damselflies occurred in the species pool, predator z values were even higher than predicted, as damselflies avoid small, drought-prone bromeliads. In one habitat, dwarf forests, detrital biomass became decoupled from bromeliad size, which also caused large trophic differences in z values. We argue that there are often simpler explanations than trophic coupling to explain differences in z values between trophic levels.     

Variations in prey consumption of centipede predators in forest soils as indicated by molecular gut content analysis

Predation is an important ecological factor driving animal population structures, community assemblages and consequently ecosystem stability and biodiversity. Many environmental factors influence direction and intensity of predation, suggesting that trophic linkages between animals vary between different habitats. This in consequence has particular relevance in anthropogenically altered habitats such as managed forests, where disturbance regime, tree composition and stand age may change the natural food web structure. We investigated how prey consumption of three common centipede predators (Lithobius spp., Chilopoda), representing two body sizes varies between four differently managed forest types in two regions across Germany. We hypothesized that prey preference of these generalist predators is independent of forest type but rather driven by habitat structure, prey abundance and predator body size. Applying specific PCR assays to test for DNA of three abundant prey groups, i.e. Collembola, Diptera and Lumbricidae, in the predators’ guts, we tracked trophic interactions. The results showed that management type indeed has no influence on centipede prey consumption but depth of litter layer and soil pH. Trophic interactions varied between the two sampled forests regions mainly due to changes in the detection of Lumbricidae and Diptera. Also, effect of litter layer and prey abundance significantly differed between the smaller L. crassipes and the larger L. mutabilis, indicating a body size effect. The results complement food web analyses using fatty acids and stable isotopes by elucidating trophic interactions in soil in unprecedented detail.