Ecological niche differences are necessary for stable species coexistence but are often difficult to discern. Models of dietary niche differentiation in large mammalian herbivores invoke the quality, quantity, and spatiotemporal distribution of plant tissues and growth forms but are agnostic toward food plant species identity. Empirical support for these models is variable, suggesting that additional mechanisms of resource partitioning may be important in sustaining large-herbivore diversity in African savannas. We used DNA metabarcoding to conduct a taxonomically explicit analysis of large-herbivore diets across southeastern Africa, analyzing ∼4,000 fecal samples of 30 species from 10 sites in seven countries over 6 y. We detected 893 food plant taxa from 124 families, but just two families—grasses and legumes—accounted for the majority of herbivore diets. Nonetheless, herbivore species almost invariably partitioned food plant taxa; diet composition differed significantly in 97% of pairwise comparisons between sympatric species, and dissimilarity was pronounced even between the strictest grazers (grass eaters), strictest browsers (nongrass eaters), and closest relatives at each site. Niche differentiation was weakest in an ecosystem recovering from catastrophic defaunation, indicating that food plant partitioning is driven by species interactions, and was stronger at low rainfall, as expected if interspecific competition is a predominant driver. Diets differed more between browsers than grazers, which predictably shaped community organization: Grazer-dominated trophic networks had higher nestedness and lower modularity. That dietary differentiation is structured along taxonomic lines complements prior work on how herbivores partition plant parts and patches and suggests that common mechanisms govern herbivore coexistence and community assembly in savannas.
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Mechanisms of dietary resource partitioning in large‐herbivore assemblages: a plant‐trait‐based approach
Sympatric large mammalian herbivore species differ in diet composition, both by eating different parts of the same plant and by eating different plant species. Various theories proposed to explain these differences are not mutually exclusive, but are difficult to reconcile and confront with data. Moreover, whereas several of these ideas were originally developed with reference to within-plant partitioning (i.e., consumption of different tissues), they may analogously apply to partitioning of plant species; this possibility has received little attention.
Plant functional traits provide a novel window into herbivore diets and a means of testing multiple hypotheses in a unified framework. We used DNA metabarcoding to characterize the diets of 14 sympatric large-herbivore species in an African savanna and analyzed diet composition in light of 27 functional traits that we measured locally for 204 plant species.
Plant traits associated with the deep phylogenetic split between grasses and eudicots formed the primary axis of resource partitioning, affirming the generality and importance of the grazer-browser spectrum. A secondary axis comprised plant traits relevant to herbivore body size. Plant taxa in the diets of large-bodied species were lower on average in digestible energy and protein, taller on average (especially among grazers), and tended to be higher in tensile strength, zinc, stem-specific density, and potassium (and lower in sodium, stem dry matter content, and copper). These results are consistent with longstanding hypotheses linking body size with forage quality and height, yet they also suggest the existence of undiscovered links between herbivore body size and a set of rarely considered food-plant traits. We also tested the novel hypothesis that the leaf economic spectrum (LES), a major focus in plant ecology, is an axis of resource partitioning in large-herbivore assemblages; we found that the LES was a minor axis of individual variation within a few species, but had little effect on interspecific dietary differentiation.
Synthesis. These results identify key plant traits that underpin the partitioning of food-plant species in large-herbivore communities and suggest that accounting for multiple plant traits (and tradeoffs among them) will enable a deeper understanding of herbivore-plant interaction networks.
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- NSF-PAR ID:
- 10314523
- Editor(s):
- Austin, A
- Date Published:
- Journal Name:
- Journal of Ecology
- ISSN:
- 0022-0477
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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Abstract Megafauna assemblages have declined or disappeared throughout much of the world, and many efforts are underway to restore them. Understanding the trophic ecology of such reassembling systems is necessary for predicting recovery dynamics, guiding management, and testing general theory. Yet, there are few studies of recovering large‐mammal communities, and fewer still that have characterized food‐web structure with high taxonomic resolution.
In Gorongosa National Park, large herbivores have rebounded from near‐extirpation following the Mozambican Civil War (1977–1992). However, contemporary community structure differs radically from the prewar baseline: medium‐sized ungulates now outnumber larger bodied species, and several apex carnivores remain locally extinct.
We used DNA metabarcoding to quantify diet composition of Gorongosa’s 14 most abundant large‐mammal populations. We tested five hypotheses: (i) the most abundant populations exhibit greatest individual‐level dietary variability; (ii) these populations also have the greatest total niche width (dietary diversity); (iii) interspecific niche overlap is high, with the diets of less‐abundant species nested within those of more‐abundant species; (iv) partitioning of forage species is stronger in more structurally heterogeneous habitats; and (v) selectivity for plant taxa converges within guilds and digestive types, but diverges across them.
Abundant (and narrow‐mouthed) populations exhibited higher among‐individual dietary variation, but not necessarily the greatest dietary diversity. Interspecific dietary overlap was high, especially among grazers and in structurally homogenous habitat, whereas niche separation was more pronounced among browsers and in heterogeneous habitat. Patterns of selectivity were similar for ruminants—grazers and browsers alike—but differed between ruminants and non‐ruminants.
Synthesis . The structure of this recovering food web was consistent with several hypotheses predicated on competition, habitat complexity, and herbivore traits, but it differed from patterns observed in more intact assemblages. We propose that intraspecific competition in the fastest‐recovering populations has promoted individual variation and a more nested food web, wherein rare species use subsets of foods eaten by abundant species, and that this scenario is reinforced by weak predation pressure. Future work should test these conjectures and analyse how the taxonomic dietary niche axis studied here interacts with other mechanisms of diet partitioning to affect community reassembly following wildlife declines. -
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Abstract Theory predicts that trophic specialization (i.e. low dietary diversity) should make consumer populations sensitive to environmental disturbances. Yet diagnosing specialization is complicated both by the difficulty of precisely quantifying diet composition and by definitional ambiguity: what makes a diet ‘diverse’?
We sought to characterize the relationship between taxonomic dietary diversity (TDD) and phylogenetic dietary diversity (PDD) in a species‐rich community of large mammalian herbivores in a semi‐arid East African savanna. We hypothesized that TDD and PDD would be positively correlated within and among species, because taxonomically diverse diets are likely to include plants from many lineages.
By using DNA metabarcoding to analyse 1,281 faecal samples collected across multiple seasons, we compiled high‐resolution diet profiles for 25 sympatric large‐herbivore species. For each of these populations, we calculated TDD and PDD with reference to a DNA reference library for local plants.
Contrary to our hypothesis, measures of TDD and PDD were either uncorrelated or negatively correlated with each other. Thus, these metrics reflect distinct dimensions of dietary specialization both within and among species. In general, grazers and ruminants exhibited greater TDD, but lower PDD, than did browsers and non‐ruminants. We found significant seasonal variation in TDD and/or PDD for all but four species (Grevy's zebra, buffalo, elephant, Grant's gazelle); however, the relationship between TDD and PDD was consistent across seasons for all but one of the 12 best‐sampled species (plains zebra).
Our results show that taxonomic generalists can be phylogenetic specialists, and vice versa. These two dimensions of dietary diversity suggest contrasting implications for efforts to predict how consumers will respond to climate change and other environmental perturbations. For example, populations with low TDD may be sensitive to phylogenetically ‘random’ losses of food species, whereas populations with low PDD may be comparatively more sensitive to environmental changes that disadvantage entire plant lineages—and populations with low dietary diversity in both taxonomic and phylogenetic dimensions may be most vulnerable of all.
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A major challenge in biology is to understand how phylogeny, diet, and environment shape the mammalian gut microbiome. Yet most studies of nonhuman microbiomes have relied on relatively coarse dietary categorizations and have focused either on individual wild populations or on captive animals that are sheltered from environmental pressures, which may obscure the effects of dietary and environmental variation on microbiome composition in diverse natural communities. We analyzed plant and bacterial DNA in fecal samples from an assemblage of 33 sympatric large-herbivore species (27 native, 6 domesticated) in a semiarid East African savanna, which enabled high-resolution assessment of seasonal variation in both diet and microbiome composition. Phylogenetic relatedness strongly predicted microbiome composition ( r = 0.91) and was weakly but significantly correlated with diet composition ( r = 0.20). Dietary diversity did not significantly predict microbiome diversity across species or within any species except kudu; however, diet composition was significantly correlated with microbiome composition both across and within most species. We found a spectrum of seasonal sensitivity at the diet−microbiome nexus: Seasonal changes in diet composition explained 25% of seasonal variation in microbiome composition across species. Species’ positions on (and deviations from) this spectrum were not obviously driven by phylogeny, body size, digestive strategy, or diet composition; however, domesticated species tended to exhibit greater diet−microbiome turnover than wildlife. Our results reveal marked differences in the influence of environment on the degree of diet−microbiome covariation in free-ranging African megafauna, and this variation is not well explained by canonical predictors of nutritional ecology.more » « less
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Abstract Despite the shared prediction that the width of a population's dietary niche expands as food becomes limiting, the Niche Variation Hypothesis (NVH) and Optimal Foraging Theory (OFT) offer contrasting views about how individuals alter diet selection when food is limited.
Classical OFT predicts that dietary preferences do not change as food becomes limiting, so individuals expand their diets as they compensate for a lack of preferred foods. In contrast, the NVH predicts that among‐individual variation in cognition, physiology or morphology create functional trade‐offs in foraging efficiency, thereby causing individuals to specialize on different subsets of food as food becomes limiting.
To evaluate (a) the predictions of the NVH and OFT and (b) evidence for physiological and cognitive‐based functional trade‐offs, we used DNA microsatellites and metabarcoding to quantify the diet, microbiome and genetic relatedness (a proxy for social learning) of 218 moose
Alces alces across six populations that varied in their degree of food limitation.Consistent with both the NVH and OFT, dietary niche breadth increased with food limitation. Increased diet breadth of individuals—rather than increased diet specialization—was strongly correlated with both food limitation and dietary niche breadth of populations, indicating that moose foraged in accordance with OFT. Diets were not constrained by inheritance of the microbiome or inheritance of diet selection, offering support for the little‐tested hypothesis that functional trade‐offs in food use (or lack thereof) determine whether populations adhere to the predictions of the NVH or OFT.
Our results indicate that both the absence of strong functional trade‐offs and the digestive physiology of ruminants provide contexts under which populations should forage in accordance with OFT rather than the NVH. Also, because dietary niche width increased with increased food limitation, OFT and the NVH provide theoretical support for the notion that plant–herbivore interaction networks are plastic rather than static, which has important implications for understanding interspecific niche partitioning. Lastly, because population‐level dietary niche breadth and calf recruitment are correlated, and because calf recruitment can be a proxy for food limitation, our work demonstrates how diet data can be employed to understand a populations' proximity to carrying capacity.
- Free Publicly Accessible Full Text
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Accepted Manuscript1.0
- Journal Article:
- https://doi.org/10.1111/1365-2745.13843
