Biodiversity of coral reef cryptobiota shuffles but does not decline under the combined stressors of ocean warming and acidification

Ocean-warming and acidification are predicted to reduce coral reef biodiversity, but the combined effects of these stressors on overall biodiversity are largely unmeasured. Here, we examined the individual and combined effects of elevated temperature (+2 °C) and reduced pH (−0.2 units) on the biodiversity of coral reef communities that developed on standardized sampling units over a 2-y mesocosm experiment. Biodiversity and species composition were measured using amplicon sequencing libraries targeting the cytochrome oxidase I (COI) barcoding gene. Ocean-warming significantly increased species richness relative to present-day control conditions, whereas acidification significantly reduced richness. Contrary to expectations, species richness in the combined future ocean treatment with both warming and acidification was not significantly different from the present-day control treatment. Rather than the predicted collapse of biodiversity under the dual stressors, we find significant changes in the relative abundance but not in the occurrence of species, resulting in a shuffling of coral reef community structure among the highly species-rich cryptobenthic community. The ultimate outcome of altered community structure for coral reef ecosystems will depend on species-specific ecological functions and community interactions. Given that most species on coral reefs are members of the understudied cryptobenthos, holistic research on reef communities is needed to accurately predict diversity–function relationships and ecosystem responses to future climate conditions.

As the concentration of atmospheric carbon dioxide (pCO₂) continues to rise, marine biodiversity is predicted to decline due to ocean-warming and acidification (1). Warming seas and increased acidity are expected to disproportionately affect marine ecosystems built by calcifying biota (2–4). Coral reefs are among the most sensitive marine ecosystems affected by global stressors, because the primary ecosystem engineers, calcifying scleractinian corals and coralline algae, show direct physiological responses to both elevated temperature and acidification, resulting in strong indirect effects on habitat structure and community composition (5, 6). In this century alone, record-breaking sea surface temperature anomalies have resulted in widespread coral mortality (7, 8), leading to a reduction in topographic complexity (9) and a shift in community composition (10, 11). Likewise, in situ observations of coral reefs along naturally occurring gradients of acidification have shown declines in habitat complexity (5, 6) and diversity (12, 13), as well as changes in community structure (14, 15). The combination of both thermal stress and acidification stress over the coming decades is predicted to have synergistic negative effects on reef resilience (2, 3, 16) by eroding the reef framework (17), shifting the structural dominance away from calcifiers and severely diminishing the biodiversity of this iconic ecosystem (2, 4). Coral reefs occupy less than 1% of the seafloor but house over 25% of all marine species; the loss of biodiversity due to anthropogenic stressors is predicted to lead to the functional collapse of these ecosystems later this century (2, 4, 18, 19). However, future projections of the combined effects of increased temperature and acidity on biodiversity have typically been derived from reviews and meta-analyses based on short-term, single-species experimental manipulations (20–23) or from in situ observations of a handful of taxa along natural gradients of seawater chemistry or temperature (5, 7, 12, 13, 24).Although such studies have informed our understanding of how some reef communities may change in the future, tradeoffs also exist for each approach in understanding climate impacts on biodiversity. Natural gradient studies do not simultaneously incorporate end-of-the-century levels of both acidification and warming, and short-term perturbation experiments are typically performed over days to weeks on single focal species. While short-term perturbation experiments across life stages have been instrumental in understanding how changes in ocean temperature, chemistry, and their combined effects influence organismal physiology (25, 26), they do not include diurnal or seasonal environmental changes (27–29) or realistic multispecies communities, which inherently excludes the roles of environmental variation and ecological interactions from contributing to the measured responses. Species interactions could be critical to experimental outcomes because they can modify population growth rates, behavior, consumption, reproduction, production, the efficacy of defensive structures, and resource availability, thereby influencing species densities, composition, and richness through competition, facilitation, or predation (30–34). Ultimately, species interactions determine whether ecosystem functions are maintained or diminished under altered environmental conditions (35–37). Thus, there is a pressing need for long-term, multispecies experimental work to understand the responses of complex communities to future climate change scenarios.Here, we examined the independent and combined effects of ocean-warming and acidification on the biodiversity of coral reef communities in long-term (2-y) mesocosms. In experimental flow-through mesocosms that received unfiltered seawater drawn from an adjacent reef slope, we examined the cryptobiota communities that developed on standardized habitats (two-tiered Autonomous Reef Monitoring Structures, or ARMS) (38) in each of four treatments: present-day pH and temperature (Control treatment), ocean acidification (−0.2 pH units—Acidified treatment), ocean-warming (+2 °C—Heated treatment), and future ocean combined stressors (−0.2 pH units and +2 °C—Acidified-Heated treatment) (SI Appendix, Fig. S1). These experimental ocean-warming and acidification conditions reflect those predicted for the late 21st century given current commitments under the Paris Climate Accord (roughly intermediate between Representative Concentration Pathways RCP 6.0 and RCP 8.5) (39).Each mesocosm was initially established with a 2-cm layer of carbonate reef sand and gravel as well as pieces of reef rubble (three replicate 10- to 20-cm pieces randomly divided among mesocosms) collected from the adjacent reef, thereby including natural infaunal and surface-attached communities. A juvenile (3- to 8-cm) Convict surgeonfish (Acanthurus triostegus), a generalist grazer on benthic algae, a Threadfin butterflyfish (Chaetodon auriga), a generalist grazer on noncoral invertebrates, and five herbivorous reef snails (Trochus sp.) were added to each tank to provide the essential ecological functions of herbivory and predation in the mesocosms at biomass values approximating Hawaiian reefs (40). Finally, the eight regionally most common reef-building coral species (Montipora capitata, Montipora flabellata, Montipora patula, Pocillopora acuta, Pocillopora meandrina, Porites compressa, Porites evermanni, and Porites lobata) were added as small fragments to each the mesocosms for an initial coral cover of ∼10% to begin the experiment. The corals and rubble were placed on a plastic grate 6 cm above the sediments to simulate their attachment to hard substrate in nature, and the ARMS were placed underneath the grate to simulate the location of the cryptobenthic habitat (SI Appendix, Fig. S2). Among the added species, only one species of coral was extirpated from a single treatment. Thus, we target the cryptobenthic community here, because they comprise the vast majority of biodiversity on coral reefs (41) and show significant community responses to our experimental treatments. Furthermore, due to the challenges associated with surveying the cryptobiota using visual census, these organisms are often overlooked in coral reef climate change research despite their essential roles in nutrient cycling, cementation, trophodynamics, and other ecological processes (42–45). As studies are increasingly pointing toward the critical functional importance of this community in food webs and the maintenance of biodiversity on coral reefs (43, 45, 46), there is a need to diminish the existing knowledge gap on both taxonomic composition and ecosystem function of this community in response to climate change.After two years of exposure, we examined the coral reef community that had developed on each ARMS unit. We generated amplicon sequence libraries targeting cytochrome oxidase I (COI) (the most extensive barcode database currently available) from each unit to test whether species richness, community composition (occurrence), or community structure (relative abundance) of the cryptobenthic community changed with treatment. This experimental study evaluates the richness and composition of an entire coral reef community which developed over a multiyear time frame under predicted future ocean conditions.