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Abstract Background Management actions that address local-scale stressors on coral reefs can rapidly improve water quality and reef ecosystem condition. In response to reef managers who need actionable thresholds for coastal runoff and dredging, we conducted a systematic review and meta-analysis of experimental studies that explore the effects of sediment on corals. We identified exposure levels that ‘adversely’ affect corals while accounting for sediment bearing (deposited vs. suspended), coral life-history stage, and species, thus providing empirically based estimates of stressor thresholds on vulnerable coral reefs. Methods We searched online databases and grey literature to obtain a list of potential studies, assess their eligibility, and critically appraise them for validity and risk of bias. Data were extracted from eligible studies and grouped by sediment bearing and coral response to identify thresholds in terms of the lowest exposure levels that induced an adverse physiological and/or lethal effect. Meta-regression estimated the dose–response relationship between exposure level and the magnitude of a coral’s response, with random-effects structures to estimate the proportion of variance explained by factors such as study and coral species. Review findings After critical appraisal of over 15,000 records, our systematic review of corals’ responses to sediment identified 86 studies to be included in meta-analyses (45 studies for deposited sediment and 42 studies for suspended sediment). The lowest sediment exposure levels that caused adverse effects in corals were well below the levels previously described as ‘normal’ on reefs: for deposited sediment, adverse effects occurred as low as 1 mg/cm 2 /day for larvae (limited settlement rates) and 4.9 mg/cm 2 /day for adults (tissue mortality); for suspended sediment, adverse effects occurred as low as 10 mg/L for juveniles (reduced growth rates) and 3.2 mg/L for adults (bleaching and tissue mortality). Corals take at least 10 times longer to experience tissue mortality from exposure to suspended sediment than to comparable concentrations of deposited sediment, though physiological changes manifest 10 times faster in response to suspended sediment than to deposited sediment. Threshold estimates derived from continuous response variables (magnitude of adverse effect) largely matched the lowest-observed adverse-effect levels from a summary of studies, or otherwise helped us to identify research gaps that should be addressed to better quantify the dose–response relationship between sediment exposure and coral health. Conclusions We compiled a global dataset that spans three oceans, over 140 coral species, decades of research, and a range of field- and lab-based approaches. Our review and meta-analysis inform the no-observed and lowest-observed adverse-effect levels (NOAEL, LOAEL) that are used in management consultations by U.S. federal agencies. In the absence of more location- or species-specific data to inform decisions, our results provide the best available information to protect vulnerable reef-building corals from sediment stress. Based on gaps and limitations identified by our review, we make recommendations to improve future studies and recommend future synthesis to disentangle the potentially synergistic effects of multiple coral-reef stressors.more » « less
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 (
Elacatinusspp.), 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 ( Cephalopholisspp. 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.