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.
Oligotrophic tropical coral reefs are built on efficient internal energy and nutrient cycling, facilitated by tight trophic interactions. In the competition for available prey, some small fishes have evolved to feed on apparently barren sand patches that connect hard‐substratum patches in many reef habitats. One strategy for obtaining prey from a particulate matrix is to sift out small prey items from the sediment (often called ‘winnowing’). Yet, the trophic link between small winnowing consumers and their prey are poorly resolved, let alone the morphological specialisations that enable this foraging behaviour. We used aquarium‐based feeding experiments to quantify the impact of winnowing by two sand‐dwelling goby species ( After 4 days of sifting through the sand matrix, the two species significantly reduced meiobenthic prey abundance by 30.7% ± 9.2 Our results provide important background on the trophic link between the meiobenthos and winnowing gobies on coral reefs. The revealed specialisations of the goby feeding apparatus facilitate sand‐sifting foraging behaviour and access to an otherwise inaccessible trophic niche of microscopic prey. By having evolved a specialised strategy to obtain nutritious and highly abundant prey from seemingly barren sand, we suggest that winnowing gobies act as an important conduit for sand‐derived energy to higher trophic levels.
Read the free
- Award ID(s):
- 1701665
- NSF-PAR ID:
- 10369702
- Publisher / Repository:
- Wiley-Blackwell
- Date Published:
- Journal Name:
- Functional Ecology
- Volume:
- 36
- Issue:
- 8
- ISSN:
- 0269-8463
- Page Range / eLocation ID:
- p. 1936-1948
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
More Like this
-
more » « less
Abstract -
more » « less
Abstract Cleaning symbioses on coral reefs are mutually beneficial interactions between two individuals, in which a ‘cleaner’ removes and eats parasites from the surface of a ‘client’ fish. A suite of behavioural and morphological traits of cleaners signal cooperation with co‐evolved species, thus protecting the cleaner from being eaten by otherwise predatory clients. However, it is unclear whether cooperation between cleaners and predatory clients is innate or learned, and therefore whether an introduced predator might consume, cooperate with or alter the behaviour of cleaners.
We explored the role of learning in cleaning symbioses by comparing the interactions of native cleaner fishes with both naïve and experienced, non‐native and native fish predators. In so doing, we tested the vulnerability of the predominant cleaners on Atlantic coral reefs, cleaning gobies (
Elacatinus spp.), to the recent introduction of a generalist predator, the Indo‐Pacific red lionfish (Pterois volitans ).Naïve juveniles of both invasive (
P. volitans ) and native predators (Cephalopholis spp. groupers) initially attacked cleaning gobies and hyperventilated from a putative toxin on the gobies' skin during laboratory experiments. After one to five such encounters, invasive lionfish often approached the cleaner closely, then turned away without striking. Consistent with learned avoidance, invasive lionfish rarely interacted with cleaning gobies in the wild, either antagonistically or cooperatively, and did not affect gobies' abundance. Native predators showed little evidence of learning during early encounters; they repeatedly attacked the cleaner during laboratory experiments and hyperventilated less violently than did lionfish. However, consistent with learned cooperation, native predators rarely antagonised and were frequently cleaned by gobies in the wild.We demonstrated that rapid, learned avoidance protects a distasteful cleaning mutualist from an invasive predator. The behavioural plasticity of this invader likely contributes to its success across its invaded range. Additionally, our results suggest that the cleaner's chemical defence most likely evolved as a way to deter predation and reinforce cooperation with naïve individuals of native species.
-
Fish-associated microorganisms are known to be affected by the environment and other external factors, such as microbial transfer between interacting partners. One of the most iconic mutualistic interactions on coral reefs is the cleaning interactions between cleaner fishes and their clients, during which direct physical contact occurs. Here, we characterized the skin bacteria of the Caribbean cleaner sharknose goby, Elacatinus evelynae, in four coral reefs of the US Virgin Islands using sequencing of the V4 region of the 16S rRNA gene. We specifically tested the relationship between gobies’ level of interaction with clients and skin microbiota diversity and composition. Our results showed differences in microbial alpha- and beta-diversity in the skin of gobies from different reef habitats and high inter-individual variation in microbiota diversity and structure. Overall, the results showed that fish-to-fish direct contact and specifically, access to a diverse clientele, influences the bacterial diversity and structure of cleaner gobies’ skin. Because of their frequent contact with clients, and therefore, high potential for microbial exchange, cleaner fish may serve as models in future studies aiming to understand the role of social microbial transfer in reef fish communities.more » « less
-
more » « less
Abstract Sponges are a diverse phylum of sessile filter‐feeding invertebrates that are abundant on Caribbean reefs and provide essential ecological services, including nutrient cycling, reef stabilization, habitat, and food for a variety of fishes and invertebrates. As prominent members of the benthic community, and thus potential food resources, factors determining the biochemical and energetic content of sponges will affect their trophic contributions to coral reef ecosystems. In order to evaluate the influence of geographic variation on biochemical composition and energetic content in the tissue of sponges, we collected several common and widespread species (
Agelas conifera ,Agelas tubulata ,Amphimedon compressa ,Aplysina cauliformis ,Niphates amorpha ,Niphates erecta , andXestospongia muta ) from multiple shallow reefs in four countries across the Caribbean Basin, including Belize, Curaçao, Grand Cayman, and St. Croix, U.S. Virgin Islands. In addition, we correlated inherent species‐level traits, including the production of antipredator chemical defenses and the relative abundance of microbial symbionts, with biochemical and energetic content. We found that energetic content was higher in sponges with antipredator chemical defenses, and was significantly correlated with the concentration of chemical extracts from these sponges. We also noted that sponges with high microbial abundance contained significantly more soluble protein than sponges with low microbial abundance. Finally, both biochemical and energetic content varied significantly among sponges from different locations; sponges from Grand Cayman had the highest lipid and energetic content, whereas sponges from Belize had the highest carbohydrate content but lowest energetic content. Despite similar environmental conditions at these sites, our results demonstrate that biochemical and energetic content of sponges exhibits geographic variability, with potential implications for the trophic ecology of sponges throughout the Caribbean Basin. -
more » « less
Abstract Mesopredator release following top predator loss may reduce biodiversity and harm foundation species. We investigated the potential for moderate environmental changes to trigger mesopredator release by disrupting the foraging ability of top predators without affecting their abundance by performing an in situ experiment designed to isolate the magnitude of mesopredator effects on oyster reefs (
Crassostrea virginica ). In estuaries, fishes occupy upper trophic levels. Most are visual foragers and become less effective predators in high turbidity. Communities were 10% more diverse, fish predation was 20% higher, and oyster recruitment four times higher in low turbidity. Crab mesopredators were 10% larger and 260% more abundant in high turbidity. Caging treatments to exclude mesopredators significantly affected communities in high but not low turbidity. Oysters had 150% stronger shells in turbid areas, a known response to crabs that was indicative of higher crab abundance. These findings indicated that increased turbidity attenuated fish foraging ability without disrupting the foraging ability of mesopredators (e.g., crabs) that forage by chemoreception. Larger and more numerous crab mesopredators significantly affected oyster reef community structure as well as the survival and growth of oysters in turbid environments. In environments where apex predators and mesopredators utilize different sensory mechanisms, sensory‐mediated mesopredator release may occur when conditions affect the foraging ability of higher order predators but not their prey.
