Consequences of kelp forest ecosystem shifts and predictors of persistence through multiple stressors.

Ecological communities can be stable over multiple generations, or rapidly shift into structurally and functionally different configurations. In kelp forest ecosystems, overgrazing by sea urchins can abruptly shift forests into alternative states that are void of macroalgae and primarily dominated by actively grazing sea urchins. Beginning in 2014, a sea urchin outbreak along the central coast of California resulted in a patchy mosaic of remnant forests interspersed with sea urchin barrens. In this study, we used a 14-year subtidal monitoring dataset of invertebrates, algae, and fishes to explore changes in community structure associated with the loss of forests. We found that the spatial mosaic of barrens and forests resulted in a region-wide shift in community structure. However, the magnitude of kelp forest loss and taxonomic-level consequences were spatially heterogeneous. Taxonomic diversity declined across the region, but there were no declines in richness for any group, suggesting compositional redistribution. Baseline ecological and environmental conditions, and sea urchin behaviour, explained the persistence of forests through multiple stressors. These results indicate that spatial heterogeneity in preexisting ecological and environmental conditions can explain patterns of community change.

Large potential impacts of marine heatwaves on ecosystem functioning.

Ocean warming is driving significant changes in the structure and functioning of marine ecosystems, shifting species' biogeography and phenology, changing body size and biomass and altering the trophodynamics of the system. Particularly, extreme temperature events such as marine heatwaves (MHWs) have been increasing in intensity, duration and frequency. MHWs are causing large-scale impacts on marine ecosystems, such as coral bleaching, mass mortality of seagrass meadows and declines in fish stocks and other marine organisms in recent decades. In this study, we developed and applied a dynamic version of the EcoTroph trophodynamic modelling approach to study the cascading effects of individual MHW on marine ecosystem functioning. We simulated theoretical user-controlled ecosystems and explored the consequences of various assumptions of marine species mortality along the food web, associated with different MHW intensities. We show that an MHW can lead to a significant biomass reduction of all consumers, with the severity of the declines being dependent on species trophic levels (TLs) and biomes, in addition to the characteristics of MHWs. Biomass of higher TLs declines more than lower TLs under an MHW, leading to changes in ecosystem structure. While tropical ecosystems are projected to be sensitive to low-intensity MHWs, polar and temperate ecosystems are expected to be impacted by more intense MHWs. The estimated time to recover from MHW impacts is twice as long for polar ecosystems and one-third longer for temperate biomes compared with tropical biomes. This study highlights the importance of considering extreme weather events in assessing the effects of climate change on the structures and functions of marine ecosystems.

Microbiome ecological memory and responses to repeated marine heatwaves clarify variation in coral bleaching and mortality.

Microbiomes are essential features of holobionts, providing their hosts with key metabolic and functional traits like resistance to environmental disturbances and diseases. In scleractinian corals, questions remain about the microbiome's role in resistance and resilience to factors contributing to the ongoing global coral decline and whether microbes serve as a form of holobiont ecological memory. To test if and how coral microbiomes affect host health outcomes during repeated disturbances, we conducted a large-scale (32 exclosures, 200 colonies, and 3 coral species sampled) and long-term (28 months, 2018-2020) manipulative experiment on the forereef of Mo'orea, French Polynesia. In 2019 and 2020, this reef experienced the two most severe marine heatwaves on record for the site. Our experiment and these events afforded us the opportunity to test microbiome dynamics and roles in the context of coral bleaching and mortality resulting from these successive and severe heatwaves. We report unique microbiome responses to repeated heatwaves in Acropora retusa, Porites lobata, and Pocillopora spp., which included: microbiome acclimatization in A. retusa, and both microbiome resilience to the first marine heatwave and microbiome resistance to the second marine heatwave in Pocillopora spp. Moreover, observed microbiome dynamics significantly correlated with coral species-specific phenotypes. For example, bleaching and mortality in A. retusa both significantly increased with greater microbiome beta dispersion and greater Shannon Diversity, while P. lobata colonies had different microbiomes across mortality prevalence. Compositional microbiome changes, such as changes to proportions of differentially abundant putatively beneficial to putatively detrimental taxa to coral health outcomes during repeated heat stress, also correlated with host mortality, with higher proportions of detrimental taxa yielding higher mortality in A. retusa. This study reveals evidence for coral species-specific microbial responses to repeated heatwaves and, importantly, suggests that host-dependent microbiome dynamics may provide a form of holobiont ecological memory to repeated heat stress.

Extreme and compound ocean events are key drivers of projected low pelagic fish biomass.

Ocean extreme events, such as marine heatwaves, can have harmful impacts on marine ecosystems. Understanding the risks posed by such extreme events is key to develop strategies to predict and mitigate their effects. However, the underlying ocean conditions driving severe impacts on marine ecosystems are complex and often unknown as risks to marine ecosystems arise not only from hazards but also from the interactions between hazards, exposure and vulnerability. Marine ecosystems may not be impacted by extreme events in single drivers but rather by the compounding effects of moderate ocean anomalies. Here, we employ an ensemble climate-impact modeling approach that combines a global marine fish model with output from a large ensemble simulation of an Earth system model, to identify the key ocean ecosystem drivers associated with the most severe impacts on the total biomass of 326 pelagic fish species. We show that low net primary productivity is the most influential driver of extremely low fish biomass over 68% of the ocean area considered by the model, especially in the subtropics and the mid-latitudes, followed by high temperature and low oxygen in the eastern equatorial Pacific and the high latitudes. Severe biomass loss is generally driven by extreme anomalies in at least one ocean ecosystem driver, except in the tropics, where a combination of moderate ocean anomalies is sufficient to drive extreme impacts. Single moderate anomalies never drive extremely low fish biomass. Compound events with either moderate or extreme ocean conditions are a necessary condition for extremely low fish biomass over 78% of the global ocean, and compound events with at least one extreme variable are a necessary condition over 61% of the global ocean. Overall, our model results highlight the crucial role of extreme and compound events in driving severe impacts on pelagic marine ecosystems.

Warming and hypoxia reduce the performance and survival of northern bay scallops (Argopecten irradians irradians) amid a fishery collapse.

Warming temperatures and diminishing dissolved oxygen (DO) concentrations are among the most pervasive drivers of global coastal change. While regions of the Northwest Atlantic Ocean are experiencing greater than average warming, the combined effects of thermal and hypoxic stress on marine life in this region are poorly understood. Populations of the northern bay scallop, Argopecten irradians irradians across the northeast United States have experienced severe declines in recent decades. This study used a combination of high-resolution (~1 km) satellite-based temperature records, long-term temperature and DO records, field and laboratory experiments, and high-frequency measures of scallop cardiac activity in an ecosystem setting to quantify decadal summer warming and assess the vulnerability of northern bay scallops to thermal and hypoxic stress across their geographic distribution. From 2003 to 2020, significant summer warming (up to ~0.2°C year-1 ) occurred across most of the bay scallop range. At a New York field site in 2020, all individuals perished during an 8-day estuarine heatwave that coincided with severe diel-cycling hypoxia. Yet at a Massachusetts site with comparable DO levels but lower daily mean temperatures, mortality was not observed. A 96-h laboratory experiment recreating observed daily temperatures of 25 or 29°C, and normoxia or hypoxia (22.2% air saturation), revealed a 120-fold increased likelihood of mortality in the 29°C-hypoxic treatment compared with control conditions, with scallop clearance rates also reduced by 97%. Cardiac activity measurements during a field deployment indicated that low DO and elevated daily temperatures modulate oxygen consumption rates and likely impact aerobic scope. Collectively, these findings suggest that concomitant thermal and hypoxic stress can have detrimental effects on scallop physiology and survival and potentially disrupt entire fisheries. Recovery of hypoxic systems may benefit vulnerable fisheries under continued warming.

Can marine heatwaves affect the fatty acid composition and energy budget of the tropical fish Zebrasoma scopas?

Marine heatwaves (MHWs) are extreme weather events featuring abnormally high seawater temperature, and expected to increase in frequency, duration and severity over this century. The impacts of these phenomena on physiological performance of coral reef species require understanding. This study aimed to evaluate the effects of a simulated MHW (category IV; ΔT = +2 °C, 11 days) (after exposure and 10-day recovery period) on fatty acid (FA) composition (as a biochemical indicator) and energy budget (i.e., growth, G, excretion (faecal, F and nitrogenous losses, U), respiration, R and food consumption, C) of a juvenile tropical surgeonfish species (Zebrasoma scopas). Significant and different changes were found under MHW scenario for some of the most abundant FA and respective groups (i.e., an increase in the contents of 14:0, 18:1n-9, ΣMonounsaturated (ΣMUFA) and 18:2n-6; and a decrease in the levels of 16:0, ΣSaturated (ΣSFA), 18:1n-7, 22:5n-3 and ΣPolyunsaturated (ΣPUFA)). The contents of 16:0 and ΣSFA were also significantly lower after MHW exposure compared to control (CTRL). Additionally, lower feed efficiency (FE), relative growth rate (RGR) and specific growth rate in terms of wet weight (SGRw), as well as higher energy loss for respiration were observed under MHW exposure conditions in comparison with CTRL and MHW recovery period. The energy proportion channelled for faeces dominated the mode of energy allocation, followed by growth in both treatments (after exposure). After MHW recovery, this trend was reversed, and a higher percentage was spent for growth and a lower fraction for faeces than in the MHW exposure period. Overall, FA composition, growth rates and energy loss for respiration of Z. Scopas were the physiological parameters most influenced (mainly in a negative way) by an 11-day MHW event. The observed effects in this tropical species can be exacerbated with increasing intensity and frequency of these extreme events.

The effect of simulated marine heatwaves on green-lipped mussels, Perna canaliculus: A near-natural experimental approach.

Marine heatwaves (MHW) are projected for the foreseeable future, affecting aquaculture species, such as the New Zealand green-lipped mussel (Perna canaliculus). Thermal stress alters mussel physiology highlighting the adaptive capacity that allows survival in the face of heatwaves. Within this study, adult mussels were subjected to three different seawater temperature regimes: 1) low (sustained 18 °C), 2) medium MHW (18-24 °C, using a +1 °C per week ramp) and 3) high MHW (18-24 °C, using a +2 °C per week ramp). Sampling was performed over 11 weeks to establish the effects of temperature on P. canaliculus survival, condition, specific immune response parameters, and the haemolymph metabolome. A transient 25.5-26.5 °C exposure resulted in 61 % mortality, with surviving animals showing a metabolic adjustment within aerobic energy production, enabling the activation of molecular defence mechanisms. Utilisation of immune functions were seen within the cytology results where temperature stress affected the percentage of superoxide-positive haemocytes and haemocyte counts. From the metabolomics results an increase in antioxidant metabolites were seen in the high MHW survivors, possibly to counteract molecular damage. In the high MHW exposure group, mussels utilised anaerobic metabolism in conjunction with aerobic metabolism to produce energy, to uphold biological functions and survival. The effect of exposure time was mainly seen on very long-, and long chain fatty acids, with increases observed at weeks seven and eight. These changes were likely due to the membrane storage functions of fatty acids, with decreases at week eleven attributed to energy metabolism functions. This study supports the use of integrated analytical tools to investigate the response of marine organisms to heatwaves. Indeed, specific metabolic pathways and cellular markers are now highlighted for future investigations aimed at targeted measures. This research contributes to a larger program aimed to identify resilient mussel traits and support aquaculture management.

Live-fast-die-young: Carryover effects of heatwave-exposed adult urchins on the development of the next generation.

With rising ocean temperatures, extreme weather events such as marine heatwaves (MHWs) are increasing in frequency and duration, pushing marine life beyond their physiological limits. The potential to respond to extreme conditions through physiological acclimatization, and pass on resistance to the next generation, fundamentally depends on the capacity of an organism to cope within their thermal tolerance limits. To elucidate whether heat conditioning of parents could benefit offspring development, we exposed adult sea urchins (Heliocidaris erythrogramma) to ambient summer (23°C), moderate (25°C) or strong (26°C) MHW conditions for 10 days. Offspring were then reared at constant temperature along a thermal gradient (22-28°C) and development was tracked to the 14-day juvenile stage. Progeny from the MHW-conditioned adults developed through to metamorphosis faster than those of ambient conditioned parents, with most individuals from the moderate and strong heatwaves developing to the larval stage across all temperatures. In contrast, the majority of offspring from the control summer temperature died before metamorphosis at temperatures above 25°C (moderate MHW). Juveniles produced from the strong MHW-conditioned adults were also larger across all temperatures, with the largest juveniles in the 26°C treatment. In contrast, the smallest juveniles were from control (current-day summer) parents (and reared at 22 and 25°C). Surprisingly, initial survival was higher in the progeny of MHW exposed parents, even at temperatures hotter than predicted MHWs (28°C). Importantly, however, there was substantial mortality of juveniles from the strong MHW parents by day 14. Therefore, while carryover effects of parental conditioning to MHWs resulted in faster growing, larger progeny, this benefit will only persist beyond the more sensitive juvenile stage and enhance survival if conditions return promptly to normal seasonal temperatures within current thermal tolerance limits.

Four decades of climatic fluctuations and fish recruitment stability across a marine-freshwater gradient.

Investigating the effects of climatic variability on biological diversity, productivity, and stability is key to understanding possible futures for ecosystems under accelerating climate change. A critical question for estuarine ecosystems is, how does climatic variability influence juvenile recruitment of different fish species and life histories that use estuaries as nurseries? Here we examined spatiotemporal abundance trends and environmental responses of 18 fish species that frequently spend the juvenile stage rearing in the San Francisco Estuary, CA, USA. First, we constructed multivariate autoregressive state-space models using age-0 fish abundance, freshwater flow (flow), and sea surface temperature data (SST) collected over four decades. Next, we calculated coefficients of variation (CV) to assess portfolio effects (1) within and among species, life histories (anadromous, marine opportunist, or estuarine dependent), and the whole community; and (2) within and among regions of the estuary. We found that species abundances varied over space and time (increasing, decreasing, or dynamically stable); and in 83% of cases, in response to environmental conditions (wet/dry, cool/warm periods). Anadromous species responded strongly to flow in the upper estuary, marine opportunist species responded to flow and/or SST in the lower estuary, and estuarine dependent species had diverse responses across the estuary. Overall, the whole community when considered across the entire estuary had the lowest CV, and life histories and species provided strong biological insurance to the portfolio (2.4- to 3.5-fold increases in stability, respectively). Spatial insurance also increased stability, although to a lesser extent (up to 1.6-fold increases). Our study advances the notion that fish recruitment stability in estuaries is controlled by biocomplexity-life history diversity and spatiotemporal variation in the environment. However, intensified drought and marine heatwaves may increase the risk of multiple consecutive recruitment failures by synchronizing species dynamics and trajectories via Moran effects, potentially diminishing estuarine nursery function.

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.

Pulse disturbances in age-structured populations: Life history predicts initial impact and recovery time.

Understanding population responses to discrete 'pulsed' environmental disturbances is essential to conservation and adaptive management. Populations of concern can be driven to low levels by disturbance, and understanding interspecific differences in recovery trajectories is necessary for evaluating management options. We analysed single-species models to investigate the demographic and management factors determining the two components of population 'resilience': the magnitude of initial impact on population abundance, and duration of the recovery time. We simulated age-structured populations with density-dependent recruitment, subjected to a pulse disturbance consisting of a period of increased mortality of either the juvenile age class or all age classes, and calculated both impact and return time. For illustration, we used demographic parameters from a suite of 16 fish species. We formulated the model as a renewal equation, allowing us to describe disturbance impacts mathematically as a convolution. We also included nonlinear dynamics, representing populations that recover to a steady state; this is more realistic (in most cases) than prior analyses of resilience in linear models without density-dependence. When the disturbance affected only one or a few young age-classes, longevity was the major life-history determinant of impact and recovery time. Shorter-lived species endured greater impacts when disturbed because each age class is a greater proportion of the population. However, shorter-lived species also had faster recovery times, for the same reason. When disturbance affected adult age-classes, the impact was more immediate and no longer affected by species' longevity, though the effect of longevity on recovery time remained. These results improve our understanding of interspecific differences in resilience and increase our ability to make predictions for adaptive management. Additionally, formulating the problem as a renewal equation and using mathematical convolutions allows us to quantify how disturbances with different time courses (not just an immediate, constant level of disturbance but gradually increasing or decreasing levels of disturbance) would have different effects on population resilience: delayed responses for species in which biomass is concentrated in older age classes, and for disturbances that become progressively more severe.

Entender las respuestas de la población a perturbaciones ambientales, específicamente a pulsadas individuales, es esencial para la conservación y la gestión adaptativa. Las poblaciones de interés pueden reducirse a niveles bajas debido a la perturbación, y es necesario entender las diferencias interespecíficas en las trayectorias de recuperación para evaluar las opciones de gestión. Analizamos modelos para especies individuales para investigar los factores demográficos y de gestión que determinan los dos componentes de la 'resiliencia' de la población: la magnitud del impacto inicial sobre la abundancia de la población y la duración del tiempo de recuperación. Simulamos poblaciones estructuradas por edad con reclutamiento que depende de la densidad, las sometimos a una perturbación pulsada que consiste en un período de mayor mortalidad del grupo etário juvenil o de todos los grupos etários, y calculamos tanto el impacto como el tiempo de retorno. A modo de ilustración, utilizamos parámetros demográficos de un conjunto de 16 especies de peces. Formulamos el modelo como una ecuación de renovación, lo que nos permite describir matemáticamente los impactos de las perturbaciones como una convolución. También incluimos dinámicas no lineales que representan poblaciones que se recuperan hacia un estado estable; esto es más realista (en la mayoría de los casos) que los análisis previos de resiliencia en modelos lineales sin la dependencia de la densidad. Cuando la perturbación ha afectado a uno o a algunos pocos grupos etários jóvenes, la longevidad fue el principal determinante de la historia de vida del impacto y el tiempo de recuperación. Las especies de vida más corta sufrieron mayores impactos cuando fueron perturbadas porque cada grupo etáreo representa una mayor proporción de la población. Sin embargo, las especies con vidas más cortas también tuvieron tiempos de recuperación más rápidos, por la misma razón. Cuando la perturbación afectó a los grupos etários adultos, el impacto fue más inmediato y ya no se vio afectado por la longevidad de las especies, aunque se mantuvo el efecto de la longevidad sobre el tiempo de recuperación. Estos resultados mejoran nuestra comprensión de las diferencias interespecíficas de la resiliencia y aumentan nuestra capacidad para hacer predicciones con fin a la gestión adaptativa. Además, formular el problema como una ecuación de renovación y usar convoluciones matemáticas nos permite cuantificar cómo las perturbaciones con distintos lapsos de tiempo (no solo un nivel de perturbación constante e inmediato, sino niveles de perturbación que aumentan o disminuyen gradualmente) tendrían diferentes efectos sobre la resiliencia de la población: respuestas tardías para especies en las que la biomasa se concentra en grupos etários de mayor edad y para perturbaciones que se vuelven progresivamente más severas.

Episodes of high recruitment buffer against climate-driven mass mortality events in a North Pacific seabird population.

Longitudinal studies of marked animals provide an opportunity to assess the relative contributions of survival and reproductive output to population dynamics and change. Cassin's auklets are a long-lived seabird that maximizes annual reproductive effort in resource-rich years through a behaviour called double brooding, the initiation of a second breeding attempt following the success of the first during the same season. Our objective was to explore whether double brooding influenced population change by contributing a greater number of future recruits. We fit temporal symmetry models to 32 years of mark-recapture data of Cassin's auklets to infer the mechanisms underlying the observed variability in per capita recruitment rates. We found that periodic peaks in recruitment were explained by an increase in available nest sites, the proportion of the population double brooding 4 years prior, and spring upwelling conditions. Estimates of population change suggests a relatively stable population throughout the time series, attributable to a 'floating' demographic class of sexually mature individuals excluded from breeding by competition which quickly fill vacant sites following periods of low adult survival. Our results highlight the importance of recruitment in maintaining the population of a long-lived seabird periodically impacted by adverse environmental conditions.

Marine heatwave challenges solutions to human-wildlife conflict.

Despite the increasing frequency and magnitude of extreme climate events, little is known about how their impacts flow through social and ecological systems or whether management actions can dampen deleterious effects. We examined how the record 2014-2016 Northeast Pacific marine heatwave influenced trade-offs in managing conflict between conservation goals and human activities using a case study on large whale entanglements in the U.S. west coast's most lucrative fishery (the Dungeness crab fishery). We showed that this extreme climate event diminished the power of multiple management strategies to resolve trade-offs between entanglement risk and fishery revenue, transforming near win-win to clear win-lose outcomes (for whales and fishers, respectively). While some actions were more cost-effective than others, there was no silver-bullet strategy to reduce the severity of these trade-offs. Our study highlights how extreme climate events can exacerbate human-wildlife conflict, and emphasizes the need for innovative management and policy interventions that provide ecologically and socially sustainable solutions in an era of rapid environmental change.

Heatwave-induced synchrony within forage fish portfolio disrupts energy flow to top pelagic predators.

During the Pacific marine heatwave of 2014-2016, abundance and quality of several key forage fish species in the Gulf of Alaska were simultaneously reduced throughout the system. Capelin (Mallotus catervarius), sand lance (Ammodytes personatus), and herring (Clupea pallasii) populations were at historically low levels, and within this community abrupt declines in portfolio effects identify trophic instability at the onset of the heatwave. Although compensatory changes in age structure, size, growth or energy content of forage fish were observed to varying degrees among all these forage fish, none were able to fully mitigate adverse impacts of the heatwave, which likely included both top-down and bottom-up forcing. Notably, changes to the demographic structure of forage fish suggested size-selective removals typical of top-down regulation. At the same time, changes in zooplankton communities may have driven bottom-up regulation as copepod community structure shifted toward smaller, warm water species, and euphausiid biomass was reduced owing to the loss of cold-water species. Mediated by these impacts on the forage fish community, an unprecedented disruption of the normal pelagic food web was signaled by higher trophic level disruptions during 2015-2016, when seabirds, marine mammals, and groundfish experienced shifts in distribution, mass mortalities, and reproductive failures. Unlike decadal-scale variability underlying ecosystem regime shifts, the heatwave appeared to temporarily overwhelm the ability of the forage fish community to buffer against changes imposed by warm water anomalies, thereby eliminating any ecological advantages that may have accrued from having a suite of coexisting forage species with differing life-history compensations.

Early developmental stages of native populations of Ciona intestinalis under increased temperature are affected by local habitat history.

Temperature modulates marine ectotherm physiology, influencing survival, abundance and species distribution. While native species could be susceptible to ocean warming, thermal tolerance might favour the spread of non-native species. Determining the success of invasive species in response to climate change is confounded by the cumulative, synergistic or antagonistic effects of environmental drivers, which vary at a geographical and temporal scale. Thus, an organism's acclimation or adaptive potential could play an important evolutionary role by enabling or conditioning species tolerance to stressful environmental conditions. We investigated developmental performance of early life stages of the ascidian Ciona intestinalis (derived from populations of anthropogenically impacted and control sites) to an extreme weather event (i.e. marine heatwave). Fertilization rate, embryo and larval development, settlement, metamorphosis success and juvenile heart rate were assessed as experimental endpoints. With the exception of fertilization and heart rates, temperature influenced all analysed endpoints. C. intestinalis derived from control sites were the most negatively affected by increased temperature conditions. By contrast, C. intestinalis from anthropogenically impacted sites showed a positive response to thermal stress, with a higher proportion of larvae development, settlement and metamorphosis success being observed under increased temperature conditions. No differences were observed for heart rates between sampled populations and experimental temperature conditions. Moreover, interaction between temperature and populations was statistically significant for embryo and larvae development, and metamorphosis. We hypothesize that selection resulting from anthropogenic forcing could shape stress resilience of species in their native range and subsequently confer advantageous traits underlying their invasive potential.

Predicting the distribution of foraging seabirds during a period of heightened environmental variability.

Quantifying the links between the marine environment, prey occurrence, and predator distribution is the first step towards identifying areas of biological importance for marine spatial planning. Events such as marine heatwaves result in an anomalous change in the physical environment, which can lead to shifts in the structure, biomass, and distribution of lower trophic levels. As central-place foragers, seabirds are vulnerable to changes in their foraging grounds during the breeding season. We first quantified spatiotemporal variability in the occurrence and biomass of prey in response to an abrupt change in oceanography as a result of a marine heatwave event. Secondly, using multivariate techniques and machine learning, we investigated if differences in the foraging technique and prey of seabirds resulted in varying responses to changes in prey occurrence and the environment over a 2.5-yr period. We found that the main variables correlated with seabird distribution were also important in structuring the occurrence and biomass of prey; sea-surface temperature (SST), current speed, mixed-layer depth, and bathymetry. Both zooplankton biomass and the occurrence of fish schools exhibited negative relationships with temperature, and temperature was subsequently an important variable in determining seabird distribution. We were able to establish correlations between the distribution of prey and the spatiotemporal distribution of albatross, little penguins and common-diving petrels. We were unable to find a correlation between the distribution of prey and that of short-tailed shearwaters and fairy prions. For high-use coastal areas, the delineation of important foraging regions is essential to balance human use of an area with the needs of marine predators, particularly seabirds.

Loss of predation risk from apex predators can exacerbate marine tropicalization caused by extreme climatic events.

Extreme climatic events (ECEs) and predator removal represent some of the most widespread stressors to ecosystems. Though species interactions can alter ecological effects of climate change (and vice versa), it is less understood whether, when and how predator removal can interact with ECEs to exacerbate their effects. Understanding the circumstances under which such interactions might occur is critical because predator loss is widespread and ECEs can generate rapid phase shifts in ecosystems which can ultimately lead to tropicalization. Our goal was to determine whether loss of predation risk may be an important mechanism governing ecosystem responses to extreme events, and whether the effects of such events, such as tropicalization, can occur even when species range shifts do not. Specifically, our goal was to experimentally simulate the loss of an apex predator, the tiger shark Galeocerdo cuvier effects on a recently damaged seagrass ecosystem of Shark Bay, Australia by applying documented changes to risk-sensitive grazing of dugong Dugong dugon herbivores. Using a 16-month-field experiment established in recently disturbed seagrass meadows, we used previous estimates of risk-sensitive dugong foraging behaviour to simulate altered risk-sensitive foraging densities and strategies of dugongs consistent with apex predator loss, and tracked seagrass responses to the simulated grazing. Grazing treatments targeted and removed tropical seagrasses, which declined. However, like in other mixed-bed habitats where dugongs forage, treatments also incidentally accelerated temperate seagrass losses, revealing that herbivore behavioural changes in response to predator loss can exacerbate ECE and promote tropicalization, even without range expansions or introductions of novel species. Our results suggest that changes to herbivore behaviours triggered by loss of predation risk can undermine ecological resilience to ECEs, particularly where long-lived herbivores are abundant. By implication, ongoing losses of apex predators may combine with increasingly frequent ECEs to amplify climate change impacts across diverse ecosystems and large spatial scales.

Depth moderates loss of marine foundation species after an extreme marine heatwave: could deep temperate reefs act as a refuge?

Marine heatwaves (MHWs) have been documented around the world, causing widespread mortality of numerous benthic species on shallow reefs (less than 15 m depth). Deeper habitats are hypothesized to be a potential refuge from environmental extremes, though we have little understanding of the response of deeper benthic communities to MHWs. Here, we show how increasing depth moderates the response of seaweed- and coral-dominated benthic communities to an extreme MHW across a subtropical-temperate biogeographical transition zone. Benthic community composition and key habitat-building species were characterized across three depths (15, 25 and 40 m) before and several times after the 2011 Western Australian MHW to assess resistance during and recovery after the heatwave. We found high natural variability in benthic community composition along the biogeographic transition zone and across depths with a clear shift in the composition after the MHW in shallow (15 m) sites but a lot less in deeper communities (40 m). Most importantly, key habitat-building seaweeds such as Ecklonia radiata and Syctothalia dorycarpa which had catastrophic losses on shallow reefs, remained and were less affected in deeper communities. Evidently, deep reefs have the potential to act as a refuge during MHWs for the foundation species of shallow reefs in this region.

Background nutrient concentration determines phytoplankton bloom response to marine heatwaves.

Ocean temperature extreme events such as marine heatwaves are expected to intensify in coming decades due to anthropogenic global warming. Reported ecological and economic impacts of marine heatwaves include coral bleaching, local extinction of mangrove and kelp forests and elevated mortalities of invertebrates, fishes, seabirds and marine mammals. In contrast, little is known about the impacts of marine heatwaves on microbes that regulate biogeochemical processes in the ocean. Here we analyse the daily output of a near-global ocean physical-biogeochemical model simulation to characterize the impacts of marine heatwaves on phytoplankton blooms in 23 tropical and temperate oceanographic regions from 1992 to 2014. The results reveal regionally coherent anomalies of shallower surface mixing layers and lower surface nitrate concentrations during marine heatwaves. These anomalies exert counteracting effects on phytoplankton growth through light and nutrient limitation. Consequently, the responses of phytoplankton blooms are mixed, but can be related to the background nutrient conditions of the study regions. The blooms are weaker during marine heatwaves in nutrient-poor waters, whereas in nutrient-rich waters, the heatwave blooms are stronger. The corresponding analyses of sea-surface temperature, chlorophyll a and nitrate based on satellite observations and in situ climatology support this relationship between phytoplankton bloom anomalies and background nitrate concentration. Given that nutrient-poor waters are projected to expand globally in the 21st century, this study suggests increased occurrence of weaker blooms during marine heatwaves in coming decades, with implications for higher trophic levels and biogeochemical cycling of key elements.

Too hot to handle: Unprecedented seagrass death driven by marine heatwave in a World Heritage Area.

The increased occurrence of extreme climate events, such as marine heatwaves (MHWs), has resulted in substantial ecological impacts worldwide. To date, metrics of thermal stress within marine systems have focussed on coral communities, and less is known about measuring stress relevant to other primary producers, such as seagrasses. An extreme MHW occurred across the Western Australian coastline in the austral summer of 2010-2011, exposing marine communities to summer seawater temperatures 2-5°C warmer than average. Using a combination of satellite imagery and in situ assessments, we provide detailed maps of seagrass coverage across the entire Shark Bay World Heritage Area (ca. 13,000 km2 ) before (2002 and 2010) and after the MHW (2014 and 2016). Our temporal analysis of these maps documents the single largest loss in dense seagrass extent globally (1,310 km2 ) following an acute disturbance. Total change in seagrass extent was spatially heterogeneous, with the most extensive declines occurring in the Western Gulf, Wooramel Bank and Faure Sill. Spatial variation in seagrass loss was best explained by a model that included an interaction between two heat stress metrics, the most substantial loss occurring when degree heating weeks (DHWm) was ≥10 and the number of days exposed to extreme sea surface temperature during the MHW (DaysOver) was ≥94. Ground truthing at 622 points indicated that change in seagrass cover was predominantly due to loss of Amphibolis antarctica rather than Posidonia australis, the other prominent seagrass at Shark Bay. As seawater temperatures continue to rise and the incidence of MHWs increase globally, this work will provide a basis for identifying areas of meadow degradation, or stability and recovery, and potential areas of resilience.