Theories involving niche diversification to explain high levels of tropical diversity propose that species are more likely to co-occur if they partition at least one dimension of their ecological niche space. Yet, numerous species appear to have widely overlapping niches based upon broad categorizations of resource use or functional traits. In particular, the extent to which food partitioning contributes to species coexistence in hyperdiverse tropical ecosystems remains unresolved. Here, we use a molecular approach to investigate inter- and intraspecific dietary partitioning between two species of damselfish (Dascyllus flavicaudus, Chromis viridis) that commonly co-occur in branching corals. Species-level identification of their diverse zooplankton prey revealed significant differences in diet composition between species despite their seemingly similar feeding strategies. Dascyllus exhibited a more diverse diet than Chromis, whereas Chromis tended to select larger prey items. A large calanoid copepod, Labidocera sp., found in low density and higher in the water column during the day, explained more than 19% of the variation in dietary composition between Dascyllus and Chromis. Dascyllus did not significantly shift its diet in the presence of Chromis, which suggests intrinsic differences in feeding behaviour. Finally, prey composition significantly shifted during the ontogeny of both fish species. Our findings show that levels of dietary specialization among coral reef associated species have likely been underestimated, and they underscore the importance of characterizing trophic webs in tropical ecosystems at higher levels of taxonomic resolution. They also suggest that niche redundancy may not be as common as previously thought.
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Reconstructing hyperdiverse food webs: Gut content metabarcoding as a tool to disentangle trophic interactions on coral reefs
Anthropogenic stressors have strong impacts on ecosystems. To understand their influence, detailed knowledge about trophic relationships among species is critical. However, this requires both exceptional resolution in dietary assessments and sampling breadth within communities, especially for highly diverse, tropical ecosystems. We used gut content metabarcoding across a broad range of coral reef fishes (8 families, 22 species) in Mo'orea, French Polynesia, to test whether this technique has the potential to capture the structure of a hyperdiverse marine food web. Moreover, we explored whether taxonomic groups (families) and traditional, broad‐scale trophic assignments explained fish diet across four different metrics of quantifying predator–prey interactions. Metabarcoding yielded a large number (4,341) of unique operational taxonomic units (i.e. prey) with high‐resolution taxonomic assignments (i.e. often to the level of genus or species). We demonstrate that across multiple metrics, taxonomic group at the family level is a consistently better, albeit still weak, predictor of empirical trophic relationships than frequently used, broad‐scale functional assignments. Our method also reveals a complex trophic network with fine‐scale partitioning among species, further emphasizing the importance of examining fish diets beyond broad trophic categories. We demonstrate the capacity of metabarcoding to reconstruct diverse and complex food webs with exceptional resolution, a significant advancement from traditional food web reconstruction. Furthermore, this method allows us to pinpoint the trophic niche of species with niche‐based modelling, even across hyperdiverse species assemblages such as coral reefs. In conjunction with complementary techniques such as stable isotope analysis, applying metabarcoding to whole communities will provide unparalleled information about energy and nutrient fluxes and inform their susceptibility to disturbances even in the world's most diverse ecosystems.
- NSF-PAR ID:
- 10457378
- Publisher / Repository:
- Wiley-Blackwell
- Date Published:
- Journal Name:
- Methods in Ecology and Evolution
- Volume:
- 10
- Issue:
- 8
- ISSN:
- 2041-210X
- Page Range / eLocation ID:
- p. 1157-1170
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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Abstract Providing taxonomically precise dietary characterisations for freshwater fish species is critical for gaining a deeper understanding of the trophic dynamics present in freshwater ecosystems. However, our current understanding of freshwater trophic ecology has relied almost entirely upon direct observation of foraging attempts or morphological identification of partially digested prey. Due to the limitations of morphological dietary characterisations of soft‐bodied arthropod prey, these techniques offer dietary descriptions that can lack satisfactory taxonomic resolution and may bias our interpretations of freshwater food webs.
Recent advancements in DNA‐based prey identification have allowed for species‐level prey characterisations for many terrestrial insectivores, although these techniques have seldom been applied to understand the diets of freshwater fish. This study used DNA metabarcoding with high‐throughput, next‐generation sequencing to provide species‐level descriptions of prey composition for three naturally reproducing, syntopic freshwater trout species.
Our study supports previous findings that suggested that brook trout (
Salvelinus fontinalis ), brown trout (Salmo trutta ), and rainbow trout (Oncorhynchus mykiss ) are generalist predators that display a high degree of seasonal dietary flexibility. Prey composition varied significantly across sampling periods, with detection frequency of terrestrial prey greater in thespring/summer period compared to theautumn period.Pollution‐sensitive aquatic macroinvertebrates were detected frequently across both sampling periods, highlighting the importance of high‐quality streams that support such arthropod prey. DNA metabarcoding also detected a high richness of soft‐bodied, Lepidoptera prey species, a taxonomic group that has been largely underrepresented in previous trout dietary studies that used traditional morphological techniques.
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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. -
Dam, Hans G. (Ed.)Siphonophores (Cnidaria: Hydrozoa) are abundant and diverse gelatinous predators in open-ocean ecosystems. Due to limited access to the midwater, little is known about the diets of most deep-dwelling gelatinous species, which constrains our understanding of food-web structure and nutrient flow in these vast ecosystems. Visual gut-content methods can rarely identify soft-bodied rapidly-digested prey, while observations from submersibles often overlook small prey items. These methods have been differentially applied to shallow and deep siphonophore taxa, confounding habitat and methodological biases. DNA metabarcoding can be used to assess both shallow and deep species’ diets under a common methodological framework, since it can detect both small and gelatinous prey. We (1) further characterized the diets of open-ocean siphonophores using DNA metabarcoding, (2) compared the prey detected by visual and molecular methods to evaluate their technical biases, and (3) evaluated tentacle-based predictions of diet. To do this, we performed DNA metabarcoding analyses on the gut contents of 39 siphonophore species across depths to describe their diets, using six barcode regions along the 18S gene. Taxonomic identifications were assigned using public databases combined with local zooplankton sequences. We identified 55 unique prey items, including crustaceans, gelatinous animals, and fish across 47 siphonophore specimens in 24 species. We reported 29 novel predator-prey interactions, among them the first insights into the diets of nine siphonophore species, many of which were congruent with the dietary predictions based on tentilla morphology. Our analyses detected both small and gelatinous prey taxa underrepresented by visual methods in species from both shallow and deep habitats, indicating that siphonophores play similar trophic roles across depth habitats. We also reveal hidden links between siphonophores and filter-feeders near the base of the food web. This study expands our understanding of the ecological roles of siphonophores in the open ocean, their trophic roles within the ‘jelly-web’, and the importance of their diversity for nutrient flow and ecosystem functioning. Understanding these inconspicuous yet ubiquitous predator-prey interactions is critical to predict the impacts of climate change, overfishing, and conservation policies on oceanic ecosystems.more » « less
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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.
