Extreme Environmental Conditions Reduce Coral Reef Fish Biodiversity
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ARTICLE https://doi.org/10.1038/s41467-020-17731-2 OPEN Extreme environmental conditions reduce coral reef fish biodiversity and productivity ✉ ✉ Simon J. Brandl 1,2,3,4,10 , Jacob L. Johansen 5,6,10 , Jordan M. Casey3,4, Luke Tornabene7, Renato A. Morais 8,9 & John A. Burt 6 Tropical ectotherms are hypothesized to be vulnerable to environmental changes, but cascading effects of organismal tolerances on the assembly and functioning of reef fish 1234567890():,; communities are largely unknown. Here, we examine differences in organismal traits, assemblage structure, and productivity of cryptobenthic reef fishes between the world’s hottest, most extreme coral reefs in the southern Arabian Gulf and the nearby, but more environmentally benign, Gulf of Oman. We show that assemblages in the Arabian Gulf are half as diverse and less than 25% as abundant as in the Gulf of Oman, despite comparable benthic composition and live coral cover. This pattern appears to be driven by energetic deficiencies caused by responses to environmental extremes and distinct prey resource availability rather than absolute thermal tolerances. As a consequence, production, transfer, and replenishment of biomass through cryptobenthic fish assemblages is greatly reduced on Earth’s hottest coral reefs. Extreme environmental conditions, as predicted for the end of the 21st century, could thus disrupt the community structure and productivity of a critical functional group, independent of live coral loss. 1 Department of Biological Sciences, Simon Fraser University, Burnaby, BC, Canada. 2 CESAB—FRB, 5 Rue de l’École de Médecine, 34000 Montpellier, France. 3 PSL Université Paris: CNRS-EPHE-UPVD USR3278 CRIOBE, Université de Perpignan, Perpignan, France. 4 Laboratoire d’Excellence “CORAIL,”, Perpignan, France. 5 Hawai’i Institute of Marine Biology, University of Hawai’i at Manoa, Kane’ohe, HI, USA. 6 Marine Biology Laboratory, Centre for Genomics and Systems Biology, New York University Abu Dhabi, Abu Dhabi, United Arab Emirates. 7 School of Aquatic and Fishery Sciences and the Burke Museum of Natural History and Culture, University of Washington, Seattle, WA, USA. 8 ARC Centre of Excellence for Coral Reef Studies, James Cook University, Townsville, QLD, Australia. 9 College of Science and Engineering, James Cook University, Townsville, QLD, Australia. 10These authors contributed ✉ equally: Simon J. Brandl, Jacob L. Johansen. email: [email protected]; [email protected] NATURE COMMUNICATIONS | (2020) 11:3832 | https://doi.org/10.1038/s41467-020-17731-2 | www.nature.com/naturecommunications 1 ARTICLE NATURE COMMUNICATIONS | https://doi.org/10.1038/s41467-020-17731-2 hy do some species occur in a given location while epigenetic pathways36,46. This has been shown in a few model Wsimilar taxa are missing? And how do resulting species36,46,47, but demands increased energetic investments46,48. assemblages affect rates of ecological processes? As It is unclear whether this process can truly enhance the survival of escalating human impacts on the biosphere deplete and re-shuffle reef fishes in competitive, uncontrolled environments, and how biological communities across ecosystems1,2, answers to these species-specific temperature tolerance differences may mediate questions are key to our quest to preserve biodiversity and eco- coexistence in ecological communities. system services to humanity3. Cryptobenthic fishes are the smallest of all reef fishes, rarely A species’ presence at a given location is mediated by a hier- exceeding 50 mm in maximum body size49.Theyaccountfor archical interplay between organismal traits (e.g., temperature almost half of all reef fish species and are numerically abundant tolerance, trophic niche), environmental conditions (e.g., tem- and ubiquitous on reefs worldwide49–52. Due to their small body perature, salinity, dissolved oxygen), biotic interactions (e.g. size, these fishes have evolved a unique life-history strategy of habitat or food availability), biogeographic history, and stochastic rapid growth, high mortality, and continuous larval replenish- events (e.g., extinction, dispersal)4–6. Furthermore, the identity ment, and play an important role in coral reef trophody- and diversity of species impact rates of ecosystem functioning, namics53. Their small body size and associated life-history also including processes that are critical to human well-being, such as promise exceptional traceability concerning the effects of, and primary or consumer productivity7,8. However, by modifying responses to, changing environmental conditions49. Limited gill abiotic conditions, species’ niches, and biotic interactions, surface area, high mass-specific metabolism, and other physio- global stressors such as climate change can interfere with these logical challenges resulting from their minute size suggest that dynamics through numerous pathways9–11. At the organismal cryptobenthics are particularly susceptible to temperature level, changes in environmental factors, such as temperature, fluctuations40,49,54. Due to their limited mobility and close affect internal physiological processes in ectotherms (e.g., oxygen association with the benthos55, mitigation of temperature consumption)12, which, if not lethal, will alter organismal extremes through migration is also not viable and notable shifts energy expenditure13–15. Changes in organismal energy demands in cryptobenthic fish community composition have been subsequently drive resource acquisition (e.g. feeding rates, prey observed following small-scale changes in the benthic commu- species) and how resulting energy is allocated to life-supporting nity structure27,56. However, the extremely high generational processes (homeostasis), growth, and reproduction16–18. turnover (7.4 generations per year in the most extreme Dynamics of energy acquisition and investment, which are often species53,57) and prevalence of benthic clutch spawning and investigated through the lens of ecological niches and fitness, are parental care49 may make them ideally suited for transgenera- the basis of modern coexistence theory and critical for our tional adaptation to changing conditions34. In fact, an extremely understanding of community assembly dynamics19 and the rate fast evolutionary clock has been implicated as a driver for rapid of ecological processes that underpin energy and nutrient fluxes speciation in cryptobenthic fishes58, which may permit similarly through ecosystems20. Integration across levels of biological fast microevolutionary changes (i.e., rapid adaptation). Thus, organization is, therefore, crucial to understand the effects of cryptobenthic fishes may be well-suited to detect the impact of global environmental change on our planet’s ecosystems21. environmental change on organisms and populations, with Coralreefsarethemostdiversemarineecosystem,andtheir promising insights into whether transgenerational plasticity or productivity provides vital services for more than 500 million people adaptation can provide pathways to the persistence of coral reef worldwide22. Scleractinian corals, the foundation species of tropical fishes in changing oceans. reefs, show high sensitivity to thermal extremes, which has led to the Here, we quantify cryptobenthic community structure, species- rapid global decline of coral reef ecosystems23.Inthewakeoflosing and population-specific physiological and dietary traits, and coral habitat, communities of the most prominent reef consumers, contributions to ecosystem functioning in the world’s hottest, teleost fishes, also decline or shift in composition24–27,which most extreme coral reef environment, the southeastern Arabian directly affects the provision of resources to people dependent on Gulf, and we compare the resulting patterns with the spatially reef fisheries28. Although recent evidence suggests that some fish proximate, but more thermally moderate, Gulf of Oman. Speci- specieswillbeabletocopewith(orevenbenefit from) live coral fically, the goal of our study was to (1) describe cryptobenthic fish loss, at least in the short term28–31,tropicalreeffishes are typically assemblages across the two locations, (2) identify organismal adapted to a relatively narrow suite of environmental conditions. traits that permit or preclude existence in the Arabian Gulf, and Thus, reef fishesmayalsobevulnerabletothedirecteffectsof (3) determine the consequences of these results for the produc- climate change on, for instance, sea surface temperatures13,32,33. tion, provision, and renewal of cryptobenthic fish biomass21. Consequently, the responses of reef fishes to ongoing changes in We show that cryptobenthic fish assemblages in the Arabian Gulf their environment might be as important as indirect, habitat- are much less diverse and abundant compared to the nearby Gulf mediated responses34–36. of Oman. Yet, thermal tolerances of cryptobenthic fish species While other environmental factors (such as salinity or oxygen indicate that all species found in the Gulf of Oman should be able saturation) have considerable effects on reef fish physiology37, to withstand the thermal extremes of the southern Arabian Gulf. temperature is by far the most commonly investigated environ- However, population-specific differences in ingested prey and mental stressor for reef fishes. Despite marked differences in body condition in three species that occur in both locations species-specific tolerances to higher temperatures38–43, most reef suggest that the environmental extremes of the southern Arabian fish species suffer from non-lethal44