Estimating the magnitude and sensitivity of energy fluxes for stickleback hosts and Schistocephalus solidus parasites using the metabolic theory of ecology.

Parasites are ubiquitous, yet their effects on hosts are difficult to quantify and generalize across ecosystems. One promising metric of parasitic impact uses the metabolic theory of ecology (MTE) to calculate energy flux, an estimate of energy lost to parasites. We investigated the feasibility of using metabolic scaling rules to compare the energetic burden of parasitism among individuals. Specifically, we found substantial sensitivity of energy flux estimates to input parameters used in the MTE equation when using available data from a model host-parasite system (Gasterosteus aculeatus and Schistocephalus solidus). Using literature values, size data from parasitized wild fish, and a respirometry experiment, we estimate that a single S. solidus tapeworm may extract up to 32% of its stickleback host's baseline metabolic energy requirement, and that parasites in multiple infections may collectively extract up to 46%. The amount of energy siphoned from stickleback to tapeworms is large but did not instigate an increase in respiration rate in the current study. This emphasizes the importance of future work focusing on how parasites influence ecosystem energetics. The approach of using the MTE to calculate energy flux provides great promise as a quantitative foundation for such estimates and provides a more concrete metric of parasite impact on hosts than parasite abundance alone.

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.

Building consensus around the assessment and interpretation of Symbiodiniaceae diversity.

Within microeukaryotes, genetic variation and functional variation sometimes accumulate more quickly than morphological differences. To understand the evolutionary history and ecology of such lineages, it is key to examine diversity at multiple levels of organization. In the dinoflagellate family Symbiodiniaceae, which can form endosymbioses with cnidarians (e.g., corals, octocorals, sea anemones, jellyfish), other marine invertebrates (e.g., sponges, molluscs, flatworms), and protists (e.g., foraminifera), molecular data have been used extensively over the past three decades to describe phenotypes and to make evolutionary and ecological inferences. Despite advances in Symbiodiniaceae genomics, a lack of consensus among researchers with respect to interpreting genetic data has slowed progress in the field and acted as a barrier to reconciling observations. Here, we identify key challenges regarding the assessment and interpretation of Symbiodiniaceae genetic diversity across three levels: species, populations, and communities. We summarize areas of agreement and highlight techniques and approaches that are broadly accepted. In areas where debate remains, we identify unresolved issues and discuss technologies and approaches that can help to fill knowledge gaps related to genetic and phenotypic diversity. We also discuss ways to stimulate progress, in particular by fostering a more inclusive and collaborative research community. We hope that this perspective will inspire and accelerate coral reef science by serving as a resource to those designing experiments, publishing research, and applying for funding related to Symbiodiniaceae and their symbiotic partnerships.

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.

Life history mediates the association between parasite abundance and geographic features.

Although parasites are ubiquitous in marine ecosystems, predicting the abundance of parasites present within marine ecosystems has proven challenging due to the unknown effects of multiple interacting environmental gradients and stressors. Furthermore, parasites often are considered as a uniform group within ecosystems despite their significant diversity. We aim to determine the potential importance of multiple predictors of parasite abundance in coral reef ecosystems, including reef area, island area, human population density, chlorophyll-a, host diversity, coral cover, host abundance and island isolation. Using a model selection approach within a database of more than 1,200 individual fish hosts and their parasites from 11 islands within the Pacific Line Islands archipelago, we reveal that geographic gradients, including island area and island isolation, emerged as the best predictors of parasite abundance. Life history moderated the relationship; parasites with complex life cycles increased in abundance with increasing island isolation, while parasites with direct life cycles decreased with increasing isolation. Direct life cycle parasites increased in abundance with increasing island area, although complex life cycle parasite abundance was not associated with island area. This novel analysis of a unique dataset indicates that parasite abundance in marine systems cannot be predicted precisely without accounting for the independent and interactive effects of each parasite's life history and environmental conditions.

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.

Pulse Heat Stress and Parasitism in a Warming World.

Infectious disease outbreaks emerged across the globe during the recent 2015-2016 El Niño event, re-igniting research interest in how climate events influence disease dynamics. While the relationship between long-term warming and the transmission of disease-causing parasites has received substantial attention, we do not yet know how pulse heat events - common phenomena in a warming world - will alter parasite transmission. The effects of pulse warming on ecological and evolutionary processes are complex and context dependent, motivating research to understand how climate oscillations drive host health and disease. Here, we develop a framework for evaluating and predicting the effects of pulse warming on parasitic infection. Specifically, we synthesize how pulse heat stress affects hosts, parasites, and the ecological interactions between them.

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.

Global patterns and impacts of El Niño events on coral reefs: A meta-analysis.

Impacts of global climate change on coral reefs are being amplified by pulse heat stress events, including El Niño, the warm phase of the El Niño Southern Oscillation (ENSO). Despite reports of extensive coral bleaching and up to 97% coral mortality induced by El Niño events, a quantitative synthesis of the nature, intensity, and drivers of El Niño and La Niña impacts on corals is lacking. Herein, we first present a global meta-analysis of studies quantifying the effects of El Niño/La Niña-warming on corals, surveying studies from both the primary literature and International Coral Reef Symposium (ICRS) Proceedings. Overall, the strongest signal for El Niño/La Niña-associated coral bleaching was long-term mean temperature; bleaching decreased with decreasing long-term mean temperature (n = 20 studies). Additionally, coral cover losses during El Niño/La Niña were shaped by localized maximum heat stress and long-term mean temperature (n = 28 studies). Second, we present a method for quantifying coral heat stress which, for any coral reef location in the world, allows extraction of remotely-sensed degree heating weeks (DHW) for any date (since 1982), quantification of the maximum DHW, and the time lag since the maximum DHW. Using this method, we show that the 2015/16 El Niño event instigated unprecedented global coral heat stress across the world's oceans. With El Niño events expected to increase in frequency and severity this century, it is imperative that we gain a clear understanding of how these thermal stress anomalies impact different coral species and coral reef regions. We therefore finish with recommendations for future coral bleaching studies that will foster improved syntheses, as well as predictive and adaptive capacity to extreme warming events.

Spatial and temporal patterns of mass bleaching of corals in the Anthropocene.

Tropical reef systems are transitioning to a new era in which the interval between recurrent bouts of coral bleaching is too short for a full recovery of mature assemblages. We analyzed bleaching records at 100 globally distributed reef locations from 1980 to 2016. The median return time between pairs of severe bleaching events has diminished steadily since 1980 and is now only 6 years. As global warming has progressed, tropical sea surface temperatures are warmer now during current La Niña conditions than they were during El Niño events three decades ago. Consequently, as we transition to the Anthropocene, coral bleaching is occurring more frequently in all El Niño-Southern Oscillation phases, increasing the likelihood of annual bleaching in the coming decades.

Trends in extinction risk for imperiled species in Canada.

Protecting and promoting recovery of species at risk of extinction is a critical component of biodiversity conservation. In Canada, the Committee on the Status of Endangered Wildlife in Canada (COSEWIC) determines whether species are at risk of extinction or extirpation, and has conducted these assessments since 1977. We examined trends in COSEWIC assessments to identify whether at-risk species that have been assessed more than once tended to improve, remain constant, or deteriorate in status, as a way of assessing the effectiveness of biodiversity conservation in Canada. Of 369 species that met our criteria for examination, 115 deteriorated, 202 remained unchanged, and 52 improved in status. Only 20 species (5.4%) improved to the point where they were 'not at risk', and five of those were due to increased sampling efforts rather than an increase in population size. Species outcomes were also dependent on the severity of their initial assessment; for example, 47% of species that were initially listed as special concern deteriorated between assessments. After receiving an at-risk assessment by COSEWIC, a species is considered for listing under the federal Species at Risk Act (SARA), which is the primary national tool that mandates protection for at-risk species. We examined whether SARA-listing was associated with improved COSEWIC assessment outcomes relative to unlisted species. Of 305 species that had multiple assessments and were SARA-listed, 221 were listed at a level that required identification and protection of critical habitat; however, critical habitat was fully identified for only 56 of these species. We suggest that the Canadian government should formally identify and protect critical habitat, as is required by existing legislation. In addition, our finding that at-risk species in Canada rarely recover leads us to recommend that every effort be made to actively prevent species from becoming at-risk in the first place.