Impacts of Climate Change on Marine Foundation Species.

Marine foundation species are the biotic basis for many of the world's coastal ecosystems, providing structural habitat, food, and protection for myriad plants and animals as well as many ecosystem services. However, climate change poses a significant threat to foundation species and the ecosystems they support. We review the impacts of climate change on common marine foundation species, including corals, kelps, seagrasses, salt marsh plants, mangroves, and bivalves. It is evident that marine foundation species have already been severely impacted by several climate change drivers, often through interactive effects with other human stressors, such as pollution, overfishing, and coastal development. Despite considerable variation in geographical, environmental, and ecological contexts, direct and indirect effects of gradual warming and subsequent heatwaves have emerged as the most pervasive drivers of observed impact and potent threat across all marine foundation species, but effects from sea level rise, ocean acidification, and increased storminess are expected to increase. Documented impacts include changes in the genetic structures, physiology, abundance, and distribution of the foundation species themselves and changes to their interactions with other species, with flow-on effects to associated communities, biodiversity, and ecosystem functioning. We discuss strategies to support marine foundation species into the Anthropocene, in order to increase their resilience and ensure the persistence of the ecosystem services they provide.

Multiscale stability of an intertidal kelp (Postelsia palmaeformis) near its northern range edge through a period of prolonged heatwaves.

BACKGROUND AND AIMS: Climate change, including gradual changes and extreme weather events, is driving widespread species losses and range shifts. These climatic changes are felt acutely in intertidal ecosystems, where many organisms live close to their thermal limits and experience the extremes of both marine and terrestrial environments. A recent series of multiyear heatwaves in the northeast Pacific Ocean might have impacted species even towards their cooler, northern range edges. Among them, the high intertidal kelp Postelsia palmaeformis has traits that could make it particularly vulnerable to climate change, but it is critically understudied. METHODS: In 2021 and 2022, we replicated in situ and aerial P. palmaeformis surveys that were conducted originally in 2006 and 2007, in order to assess the state of northern populations following recent heatwaves. Changes in P. palmaeformis distribution, extent, density and morphometrics were assessed between these two time points over three spatial scales, ranging from 250 m grid cells across the entire 167 km study region, to within grid cells and the individual patch. KEY RESULTS: We found evidence consistent with population stability at all three scales: P. palmaeformis remained present in all 250 m grid cells in the study region where it was previously found, and neither the extent within cells nor the patch density changed significantly between time points. However, there was evidence of slight distributional expansion, increased blade lengths and a shift to earlier reproductive timing. CONCLUSIONS: We suggest that apparent long-term stability of P. palmaeformis might be attributable to thermal buffering near its northern range edge and from the wave-exposed coastlines it inhabits, which may have decreased the impacts of heatwaves. Our results highlight the importance of multiscale assessments when examining changes within species and populations, in addition to the importance of dispersal capability and local conditions in regulating the responses of species to climate change.

Marine heatwaves threaten cryptic coral diversity and erode associations among coevolving partners.

Climate change-amplified marine heatwaves can drive extensive mortality in foundation species. However, a paucity of longitudinal genomic datasets has impeded understanding of how these rapid selection events alter cryptic genetic structure. Heatwave impacts may be exacerbated in species that engage in obligate symbioses, where the genetics of multiple coevolving taxa may be affected. Here, we tracked the symbiotic associations of reef-building corals for 6 years through a prolonged heatwave, including known survivorship for 79 of 315 colonies. Coral genetics strongly predicted survival of the ubiquitous coral, Porites (massive growth form), with variable survival (15 to 61%) across three morphologically indistinguishable-but genetically distinct-lineages. The heatwave also disrupted strong associations between these coral lineages and their algal symbionts (family Symbiodiniaceae), with symbiotic turnover in some colonies, resulting in reduced specificity across lineages. These results highlight how heatwaves can threaten cryptic genotypes and decouple otherwise tightly coevolved relationships between hosts and symbionts.

Tipping points and interactive effects of chronic human disturbance and acute heat stress on coral diversity.

Multiple anthropogenic stressors co-occur ubiquitously in natural ecosystems. However, multiple stressor studies often produce conflicting results, potentially because the nature and direction of stressor interactions depends upon the strength of the underlying stressors. Here, we first examine how coral α- and ß-diversities vary across sites spanning a gradient of chronic local anthropogenic stress before and after a prolonged marine heatwave. Developing a multiple stressor framework that encompasses non-discrete stressors, we then examine interactions between the continuous and discrete stressors. We provide evidence of additive effects, antagonistic interactions (with heatwave-driven turnover in coral community composition diminishing as the continuous stressor increased), and tipping points (at which the response of coral Hill-richness to stressors changed from additive to near synergistic). We show that community-level responses to multiple stressors can vary, and even change qualitatively, with stressor intensity, underscoring the importance of examining complex, but realistic continuous stressors to understand stressor interactions and their ecological impacts.

Transformation of coral communities subjected to an unprecedented heatwave is modulated by local disturbance.

Corals are imminently threatened by climate change-amplified marine heatwaves. However, how to conserve coral reefs remains unclear, since those without local anthropogenic disturbances often seem equally or more susceptible to thermal stress as impacted ones. We disentangle this apparent paradox, revealing that the relationship between reef disturbance and heatwave impacts depends upon the scale of biological organization. We show that a tropical heatwave of globally unprecedented duration (~1 year) culminated in an 89% loss of hard coral cover. At the community level, losses depended on pre-heatwave community structure, with undisturbed sites, which were dominated by competitive corals, undergoing the greatest losses. In contrast, at the species level, survivorship of individual corals typically declined as local disturbance intensified. Our study reveals both that prolonged heatwaves projected under climate change will still have winners and losers and that local disturbance can impair survival of coral species even under such extreme conditions.

Macroalgae exhibit diverse responses to human disturbances on coral reefs.

Scientists and managers rely on indicator taxa such as coral and macroalgal cover to evaluate the effects of human disturbance on coral reefs, often assuming a universally positive relationship between local human disturbance and macroalgae. Despite evidence that macroalgae respond to local stressors in diverse ways, there have been few efforts to evaluate relationships between specific macroalgae taxa and local human-driven disturbance. Using genus-level monitoring data from 1205 sites in the Indian and Pacific Oceans, we assess whether macroalgae percent cover correlates with local human disturbance while accounting for factors that could obscure or confound relationships. Assessing macroalgae at genus level revealed that no genera were positively correlated with all human disturbance metrics. Instead, we found relationships between the division or genera of algae and specific human disturbances that were not detectable when pooling taxa into a single functional category, which is common to many analyses. The convention to use percent cover of macroalgae as an indication of local human disturbance therefore likely obscures signatures of local anthropogenic threats to reefs. Our limited understanding of relationships between human disturbance, macroalgae taxa, and their responses to human disturbances impedes the ability to diagnose and respond appropriately to these threats.

Microclimate predicts kelp forest extinction in the face of direct and indirect marine heatwave effects.

Marine heatwaves threaten the persistence of kelp forests globally. However, the observed responses of kelp forests to these events have been highly variable on local scales. Here, we synthesize distribution data from an environmentally diverse region to examine spatial patterns of canopy kelp persistence through an unprecedented marine heatwave. We show that, although often overlooked, temperature variation occurring at fine spatial scales (i.e., a few kilometers or less) can be a critical driver of kelp forest persistence during these events. Specifically, though kelp forests nearly all persisted toward the cool outer coast, inshore areas were >3°C warmer at the surface and experienced extensive kelp loss. Although temperatures remained cool at depths below the thermocline, kelp persistence in these thermal refugia was strongly constrained by biotic interactions, specifically urchin populations that increased during the heatwave and drove transitions to urchin barrens in deeper rocky habitat. Urchins were, however, largely absent from mixed sand and cobble benthos, leading to an unexpected association between bottom substrate and kelp forest persistence at inshore sites with warm surface waters. Our findings demonstrate both that warm microclimates increase the risk of habitat loss during marine heatwaves and that biotic interactions modified by these events will modulate the capacity of cool microclimates to serve as thermal refugia.

Inconsistent Patterns of Microbial Diversity and Composition Between Highly Similar Sequencing Protocols: A Case Study With Reef-Building Corals.

16S rRNA gene profiling (amplicon sequencing) is a popular technique for understanding host-associated and environmental microbial communities. Most protocols for sequencing amplicon libraries follow a standardized pipeline that can differ slightly depending on laboratory facility and user. Given that the same variable region of the 16S gene is targeted, it is generally accepted that sequencing output from differing protocols are comparable and this assumption underlies our ability to identify universal patterns in microbial dynamics through meta-analyses. However, discrepant results from a combined 16S rRNA gene dataset prepared by two labs whose protocols differed only in DNA polymerase and sequencing platform led us to scrutinize the outputs and challenge the idea of confidently combining them for standard microbiome analysis. Using technical replicates of reef-building coral samples from two species, Montipora aequituberculata and Porites lobata, we evaluated the consistency of alpha and beta diversity metrics between data resulting from these highly similar protocols. While we found minimal variation in alpha diversity between platform, significant differences were revealed with most beta diversity metrics, dependent on host species. These inconsistencies persisted following removal of low abundance taxa and when comparing across higher taxonomic levels, suggesting that bacterial community differences associated with sequencing protocol are likely to be context dependent and difficult to correct without extensive validation work. The results of this study encourage caution in the statistical comparison and interpretation of studies that combine rRNA gene sequence data from distinct protocols and point to a need for further work identifying mechanistic causes of these observed differences.

Dominance determines fish community biomass in a temperate seagrass ecosystem.

Biodiversity and ecosystem function are often correlated, but there are multiple hypotheses about the mechanisms underlying this relationship. Ecosystem functions such as primary or secondary production may be maximized by species richness, evenness in species abundances, or the presence or dominance of species with certain traits. Here, we combine surveys of natural fish communities (conducted in July and August 2016) with morphological trait data to examine relationships between biodiversity and ecosystem function (quantified as fish community biomass) across 14 subtidal eelgrass meadows in the Northeast Pacific (54°N, 130°W). We employ both taxonomic and functional trait measures of diversity to investigate whether ecosystem function is best predicted by species diversity (complementarity hypothesis) or by the presence or dominance of species with particular trait values (selection or dominance hypotheses). After controlling for environmental variation, we find that fish community biomass is maximized when taxonomic richness and functional evenness are low, and in communities dominated by species with particular trait values, specifically those associated with benthic habitats and prey capture. While previous work on fish communities has found that species richness is often positively correlated with ecosystem function, our results instead highlight the capacity for regionally prevalent and locally dominant species to drive ecosystem function in moderately diverse communities. We discuss these alternate links between community composition and ecosystem function and consider their divergent implications for ecosystem valuation and conservation prioritization.

Promoting inclusive metrics of success and impact to dismantle a discriminatory reward system in science.

Success and impact metrics in science are based on a system that perpetuates sexist and racist "rewards" by prioritizing citations and impact factors. These metrics are flawed and biased against already marginalized groups and fail to accurately capture the breadth of individuals' meaningful scientific impacts. We advocate shifting this outdated value system to advance science through principles of justice, equity, diversity, and inclusion. We outline pathways for a paradigm shift in scientific values based on multidimensional mentorship and promoting mentee well-being. These actions will require collective efforts supported by academic leaders and administrators to drive essential systemic change.

Effects of climate-change-driven gradual and acute temperature changes on shark and ray species.

Climate change is altering distributions and abundances of marine species through both gradual and acute changes in temperature and productivity. Due to their high mobility and metabolic rates, elasmobranchs (sharks and rays) are likely to redistribute across latitudes and depths as they thermoregulate, but little is known about their responses to these climatic changes, which could vary widely across this diverse group of species. Here, we assessed how species with differing mobility and ecology responded to gradual changes in daily sea surface temperature (SST) and acute temperature anomalies, caused by the El Niño-Southern Oscillation (ENSO), at Cocos Island, Costa Rica, the site of multiple marine heatwaves. We used generalized linear mixed models to analyse 34,342 records of relative abundance or frequency of occurrence for seven shark and ray species collected in 27 years (1993-2019) by a dive company. We compared effect sizes for SST and the Oceanic Niño Index across the different species, which vary widely in body size and mobility. Large, mobile species responded strongly but inconsistently to temperature. For scalloped hammerhead sharks Sphyrna lewini, a 1℃ rise in SST reduced counts by over 14%, and dropped the occurrence of their large schools by almost one-fifth (19.4%). Mobula ray occurrence also declined substantially with a few degrees rise in SST, whereas tiger shark Galeocerdo cuvier occurrence sharply increased. These species also had divergent responses to the ENSO: S. lewini and G. cuvier were sighted with greater frequency during La Niña events, and their abundance dropped considerably during El Niño events-over a twofold decline between a strong La Niña and strong El Niño for S. lewini. In contrast, Mobula rays showed little response to ENSO. The smaller and sedentary Triaenodon obesus exhibited the weakest response of all species to both SST and the ENSO, reflecting its lower metabolic rates and mobility. Climate change will continue to impact elasmobranchs, even for smaller and more localized species, with the potential to impact the effectiveness of marine protected areas (MPAs). Our results compel further work on the diversity of elasmobranch responses to environmental change.

Early effects of COVID-19 on US fisheries and seafood consumption.

The US seafood sector is susceptible to shocks, both because of the seasonal nature of many of its domestic fisheries and its global position as a top importer and exporter of seafood. However, many data sets that could inform science and policy during an emerging event do not exist or are only released months or years later. Here, we synthesize multiple data sources from across the seafood supply chain, including unconventional real-time data sets, to show the relative initial responses and indicators of recovery during the COVID-19 pandemic. We synthesized news articles from January to September 2020 that reported effects of COVID-19 on the US seafood sector, including processor closures, shortened fishing seasons and loss of revenue. Concerning production and distribution, we assessed past and present landings and trade data and found substantial declines in fresh seafood catches (-40%), imports (-37%) and exports (-43%) relative to the previous year, while frozen seafood products were generally less affected. Google search trends and seafood market foot traffic data suggest consumer demand for seafood from restaurants dropped by upwards of 70% during lockdowns, with recovery varying by state. However, these declines were partially offset by an increase (270%) in delivery and takeout service searches. Our synthesis of open-access data sets and media reports shows widespread, but heterogeneous, ramifications of COVID-19 across the seafood sector, implying that policymakers should focus support on states and sub-sectors most affected by the pandemic: fishery-dependent communities, processors, and fisheries and aquaculture that focus on fresh products.

Dynamic symbioses reveal pathways to coral survival through prolonged heatwaves.

Prospects for coral persistence through increasingly frequent and extended heatwaves seem bleak. Coral recovery from bleaching is only known to occur after temperatures return to normal, and mitigation of local stressors does not appear to augment coral survival. Capitalizing on a natural experiment in the equatorial Pacific, we track individual coral colonies at sites spanning a gradient of local anthropogenic disturbance through a tropical heatwave of unprecedented duration. Unexpectedly, some corals survived the event by recovering from bleaching while still at elevated temperatures. These corals initially had heat-sensitive algal symbiont communities, endured bleaching, and then recovered through proliferation of heat-tolerant symbionts. This pathway to survival only occurred in the absence of strong local stressors. In contrast, corals in highly disturbed areas were already dominated by heat-tolerant symbionts, and despite initially resisting bleaching, these corals had no survival advantage in one species and 3.3 times lower survival in the other. These unanticipated connections between disturbance, coral symbioses and heat stress resilience reveal multiple pathways to coral survival through future prolonged heatwaves.

Increased diversity and concordant shifts in community structure of coral-associated Symbiodiniaceae and bacteria subjected to chronic human disturbance.

Both coral-associated bacteria and endosymbiotic algae (Symbiodiniaceae spp.) are vitally important for the biological function of corals. Yet little is known about their co-occurrence within corals, how their diversity varies across coral species, or how they are impacted by anthropogenic disturbances. Here, we sampled coral colonies (n = 472) from seven species, encompassing a range of life history traits, across a gradient of chronic human disturbance (n = 11 sites on Kiritimati [Christmas] atoll) in the central equatorial Pacific, and quantified the sequence assemblages and community structure of their associated Symbiodiniaceae and bacterial communities. Although Symbiodiniaceae alpha diversity did not vary with chronic human disturbance, disturbance was consistently associated with higher bacterial Shannon diversity and richness, with bacterial richness by sample almost doubling from sites with low to very high disturbance. Chronic disturbance was also associated with altered microbial beta diversity for Symbiodiniaceae and bacteria, including changes in community structure for both and increased variation (dispersion) of the Symbiodiniaceae communities. We also found concordance between Symbiodiniaceae and bacterial community structure, when all corals were considered together, and individually for two massive species, Hydnophora microconos and Porites lobata, implying that symbionts and bacteria respond similarly to human disturbance in these species. Finally, we found that the dominant Symbiodiniaceae ancestral lineage in a coral colony was associated with differential abundances of several distinct bacterial taxa. These results suggest that increased beta diversity of Symbiodiniaceae and bacterial communities may be a reliable indicator of stress in the coral microbiome, and that there may be concordant responses to chronic disturbance between these communities at the whole-ecosystem scale.

Chronic disturbance modulates symbiont (Symbiodiniaceae) beta diversity on a coral reef.

Chronic disturbance can disrupt ecological interactions including the foundational symbiosis between reef-building corals and the dinoflagellate family Symbiodiniaceae. Symbiodiniaceae are photosynthetic endosymbionts necessary for coral survival, but many Symbiodiniaceae can also be found free-living in the environment. Since most coral species acquire new Symbiodiniaceae from the environment each generation, free-living Symbiodiniaceae represent important pools for coral symbiont acquisition. Yet, little is known about the diversity of, or impacts of disturbance on, free-living Symbiodiniaceae. To determine how chronic and pulse disturbances influence Symbiodiniaceae communities, we sampled three reef habitat compartments - sediment, water, and coral (Pocillopora grandis, Montipora aequituberculata, Porites lobata) - at sites exposed to different levels of chronic anthropogenic disturbance, before, during, and after a major storm. Almost no (4%) Symbiodiniaceae amplicon sequence variants (ASVs) were found in all three compartments, and over half were found uniquely in coral. Sites experiencing chronic disturbance were typically associated with higher symbiont beta diversity (i.e., variability and turnover) across reef habitat compartments. Pulse stress, from the storm, exhibited some influence on symbiont beta diversity but the effect was inconsistent. This suggests that in this ecosystem, the effects of chronic disturbance are more prominent than temporal variability during a pulse disturbance for shaping symbiont communities.

Direct and indirect effects of climate change-amplified pulse heat stress events on coral reef fish communities.

Climate change-amplified temperature anomalies pose an imminent threat to coral reef ecosystems. While much focus has been placed on the effects of heat stress on scleractinian corals-including bleaching, mortality, and loss of reef structural complexity-and many studies have documented changes to reef fish communities arising indirectly from shifts in benthic composition, the direct impacts of heat stress on reef fish are much less well understood. Here, we quantify the direct and indirect effects of heat stress on reef fishes, using underwater visual censuses of coral reef fish communities conducted before, during, and after the 2015-2016 El Niño-induced global coral bleaching event. Surveys took place at the epicenter of this event, at 16 sites on Kiritimati (Republic of Kiribati; central equatorial Pacific) spanning across a gradient of local human disturbance. We expected that heat stress would have both direct and indirect negative effects on the reef fish community, with direct effects resulting from physiological stress during the event and indirect effects manifesting afterward as a consequence of coral mortality, and that the ability of fish communities to recover following the heat stress would depend on levels of local human disturbance. We found that total reef fish biomass and abundance declined by >50% during heat stress, likely as a result of vertical migration of fish to cooler waters. One year after the cessation of heat stress, however, total biomass, abundance, and species richness had recovered to, or even exceeded, pre-heat stress levels. However, the biomass of corallivores declined by over 70% following severe coral loss, and reefs exposed to higher levels of local human disturbance showed impaired recovery following the heat stress. These findings enhance understanding of the projected impacts of climate change-associated marine heatwaves on reef fishes, and highlight the interacting effects of local and global stressors on this vital component of coral reef ecosystems.

Differences in δ15 N and δ13 C between embryonic and maternal tissues of the ovoviviparous bluntnose sixgill shark Hexanchus griseus.

Stable nitrogen (δ15 N) and carbon (δ13 C) isotope ratios from muscle, liver and yolk were analysed from the mother and embryos of an ovoviviparous shark, Hexanchus griseus. Embryonic liver and muscle had similar δ15 N and δ13 C ratios or were depleted in heavy isotopes, compared to the same maternal somatic and reproductive yolk tissues, but no relationship existed between δ15 N or δ13 C and embryo length, as expected, because a switch to placental nourishment is lacking in this species. This study expands the understanding of maternal nourishment and embryonic stable isotope differences in ovoviviparous sharks.

Effective fisheries management instrumental in improving fish stock status.

Marine fish stocks are an important part of the world food system and are particularly important for many of the poorest people of the world. Most existing analyses suggest overfishing is increasing, and there is widespread concern that fish stocks are decreasing throughout most of the world. We assembled trends in abundance and harvest rate of stocks that are scientifically assessed, constituting half of the reported global marine fish catch. For these stocks, on average, abundance is increasing and is at proposed target levels. Compared with regions that are intensively managed, regions with less-developed fisheries management have, on average, 3-fold greater harvest rates and half the abundance as assessed stocks. Available evidence suggests that the regions without assessments of abundance have little fisheries management, and stocks are in poor shape. Increased application of area-appropriate fisheries science recommendations and management tools are still needed for sustaining fisheries in places where they are lacking.

Using baited remote underwater videos (BRUVs) to characterize chondrichthyan communities in a global biodiversity hotspot.

Threatened chondrichthyan diversity is high in developing countries where scarce resources, limited data, and minimal stakeholder support often render conservation efforts challenging. As such, data on many species, including many evolutionarily distinct endemics, is poor in these countries and their conservation status and habitat needs remain uncertain. Here, we used baited remote underwater videos (BRUVs; n = 419) conducted at 167 sites over two years to assess the frequency of occurrence (FO), relative abundance, diversity, and structure of chondrichthyan assemblages in one of the world's chondrichthyan biodiversity and endemism hotspots, South Africa. We compared chondrichthyan assemblages across three habitat types, and between unprotected and protected areas (a small marine protected area [MPA] and a larger, seasonal whale sanctuary). Although in total we observed 18 chondrichthyan species (11 families), over half of all observations were of just two species from the same family of mesopredatory endemic catsharks; only 8.8% were larger shark species. These mesopredatory species do not appear to be threatened, but some skates and larger shark species, including some endemics, were much rarer. Overall chondrichthyan FO was high (81% of all BRUVs); FO was higher in kelp (100% of BRUVS) and reef (93%) sites than at sites in sandy habitat (63%), which had a distinct chondrichthyan community. Independent of habitat, the chondrichthyan community did not relate strongly to protection. Because sites with kelp and reef habitat were rare in the whale sanctuary, this protected area had a lower chondrichthyan FO (67% of BRUVs) than either unprotected sites (81%) or those in the small MPA (98%), as well as having lower chondrichthyan relative abundance and species richness. Our study provides evidence of the importance of distinct habitat types to different chondrichthyan species, and suggests that even small MPAs can protect critical habitats, such that they may provide safe refuge for endemic species as anthropogenic pressures increase.