Multi-level responses of coral reef fishes to habitat degradation: An investigation with spatial, molecular and functional tools

Clever, Friederike Katharina (2021) Multi-level responses of coral reef fishes to habitat degradation: An investigation with spatial, molecular and functional tools. Doctoral thesis (DPhil), Manchester Metropolitan University.

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Abstract

Coral reef fishes are increasingly subjected to anthropogenic benthic change, habitat degradation and loss. This alters fish communities that rely in many di˙erent ways on coral reef habitat for resources and, in consequence, perils ecosystem functioning and human livelihoods. It is therefore vital to explore the underlying ecological interactions by which fish communities may shift, and to gain a detailed understanding of their functional properties in relation to spatial-environmental context. Yet, this requires a suÿcient fine-scale resolution of empirical data, which has been diÿcult to achieve. This thesis investigates e˙ects of spatial variation and habitat degradation on coral reef fish communities, diets, and gut microbiomes using spatial, functional, and molecular tools (DNA metabarcoding). Chapter 2 investigates fish taxonomic and functional diversity patterns in relation to specific reef structures across three atolls within a high biodiversity system, the Mesoamerican Barrier Reef, Belize, and develops a visual analysis of relative functional trait-space occupancy. The results show a diversity gradient with highest levels at the largest and least isolated atoll contrasting relative protection levels among the three atolls at the time of sampling. This suggests that e˙ects of biogeography and geomorphology may override protection status and highlight the need to integrate these factors into marine spatial planning for e˙ective conservation. Furthermore, di˙erent levels of functional trait space occupancy among atolls may reflect variation in the dominant functional processes at play within each atoll ecosystem. Overall, the atoll fish communities featured low levels of redundancy suggesting a potential for functional vulnerability. Chapter 3 investigates two benthic fish feeding strategies (browsing and active predation) with largely unknown levels of specialisation across a habitat gradient at Bocas del Toro, Panama. The results show that di˙erent feeding strategies exhibit variable responses in terms of resource use across reefs with varying levels of coral cover. DNA-based stomach and gut content analysis (metabarcoding) revealed that the diets of a facultative corallivore (Chaetodon capistratus) and a benthic crustaceans feeder (Hypoplectrus puella) were predicted by coral cover but to di˙erent degrees. Both species coped with low habitat quality at degraded reefs, but dietary adjustments appeared associated with subtle declines in physical condition. H. puella broadened its diet where coral cover was low and increasingly consumed planktonic prey. C. capistratus switched its dominant diet item from cnidarians to annelids. These findings suggest that fish trophic roles may spatially vary and that such variation might be exacerbated with increasing coral decline. Building on Chapter 3, Chapter 4 examines how the gut microbiome of a coral reef fish changes across Caribbean reefs that vary in coral cover. Using 16S high-throughput sequencing of the gut microbiome of C. capistratus, the results show an increase in gut microbiome variability for some components of the microbial assemblage at the most degraded reefs. This microbial pattern extended to closely host-associated, and presumably beneficial bacteria (i.e., the core microbiome) that were expected to remain stable. Altered fish-microbe associations in response to habitat degradation entail potential for acclimatisation, but on the other hand may bear consequences for fish health if stressors continue to intensify. This thesis provides a detailed spatial description of fish taxonomic and functional diversity patterns and contributes to understanding how coral reef habitat degradation a˙ects fish trophic and microbial interactions via fish interrelations with the benthos. Using extensive visual surveys, DNA-Metabarcoding and spatial analysis, this thesis gives insight into spatial determinants of fish functional diversity and little explored processes of intraspecific variation and feeding strategy responses, influencing fish communities and ecosystem functioning.