Climate-Change Impacts on Cephalopods: A Meta-Analysis.

Aside from being one of the most fascinating groups of marine organisms, cephalopods play a major role in marine food webs, both as predators and as prey, while representing key living economic assets, namely for artisanal and subsistence fisheries worldwide. Recent research suggests that cephalopods are benefitting from ongoing environmental changes and the overfishing of certain fish stocks (i.e., of their predators and/or competitors), putting forward the hypothesis that this group may be one of the few "winners" of climate change. While many meta-analyses have demonstrated negative and overwhelming consequences of ocean warming (OW), acidification (OA), and their combination for a variety of marine taxa, such a comprehensive analysis is lacking for cephalopod molluscs. In this context, the existing literature was surveyed for peer-reviewed articles featuring the sustained (≥24 h) and controlled exposure of cephalopod species (Cephalopoda class) to these factors, applying a comparative framework of mixed-model meta-analyses (784 control-treatment comparisons, from 47 suitable articles). Impacts on a wide set of biological categories at the individual level (e.g., survival, metabolism, behavior, cell stress, growth) were evaluated and contrasted across different ecological attributes (i.e., taxonomic lineages, climates, and ontogenetic stages). Contrary to what is commonly assumed, OW arises as a clear threat to cephalopods, while OA exhibited more restricted impacts. In fact, OW impacts were ubiquitous across different stages of ontogeny, taxonomical lineages (i.e., octopuses, squids, and cuttlefish). These results challenge the assumption that cephalopods benefit from novel ocean conditions, revealing an overarching negative impact of OW in this group. Importantly, we also identify lingering literature gaps, showing that most studies to date focus on OW and early life stages of mainly temperate species. Our results raise the need to consolidate experimental efforts in a wider variety of taxa, climate regions, life stages, and other key environmental stressors, such as deoxygenation and hypoxia, to better understand how cephalopods will cope with future climate change.

Gymnodinium catenatum Paralytic Shellfish Toxin Production and Photobiological Responses under Marine Heat Waves.

Marine heatwaves (MHWs) have doubled in frequency since the 1980s and are projected to be exacerbated during this century. MHWs have been shown to trigger harmful algal blooms (HABs), with severe consequences to marine life and human populations. Within this context, this study aims to understand, for the first time, how MHWs impact key biological and toxicological parameters of the paralytic shellfish toxin (PST) producer Gymnodinium catenatum, a dinoflagellate inhabiting temperate and tropical coastal waters. Two MHW were simulated-category I (i.e., peak: 19.9 °C) and category IV (i.e., peak: 24.1 °C)-relative to the estimated baseline in the western coast of Portugal (18.5 °C). No significant changes in abundance, size, and photosynthetic efficiency were observed among treatments. On the other hand, chain-formation was significantly reduced under category IV MHW, as was PSP toxicity and production of some PST compounds. Overall, this suggests that G. catenatum may have a high tolerance to MHWs. Nevertheless, some sublethal effects may have occurred since chain-formation was affected, suggesting that these growth conditions may be sub-optimal for this population. Our study suggests that the increase in frequency, intensity, and duration of MHWs may lead to reduced severity of G. catenatum blooms.

Impacts of Low Oxygen on Marine Life: Neglected, but a Crucial Priority for Research.

AbstractGlobal ocean O2 content has varied significantly across the eons, both shaping and being shaped by the evolutionary history of life on planet Earth. Indeed, past O2 fluctuations have been associated with major extinctions and the reorganization of marine biota. Moreover, its most recent iteration-now anthropogenically driven-represents one of the most prominent challenges for both marine ecosystems and human societies, with ocean deoxygenation being regarded as one of the main drivers of global biodiversity loss. Yet ocean deoxygenation has received far less attention than concurrent environmental variables of marine climate change, namely, ocean warming and acidification, particularly in the field of experimental marine ecology. Together with the lack of consistent criteria defining gradual and acute changes in O2 content, a general lack of multifactorial studies featuring all three drivers and their interactions prevents an adequate interpretation of the potential effects of extreme and gradual deoxygenation. We present a comprehensive overview of the interplay between O2 and marine life across space and time and discuss the current knowledge gaps and future steps for deoxygenation research. This work may also contribute to the ongoing call for an integrative perspective on the combined effects of these three drivers of change for marine organisms and ecosystems worldwide.

Integrative Approaches to Understanding Organismal Responses to Aquatic Deoxygenation.

AbstractOxygen bioavailability is declining in aquatic systems worldwide as a result of climate change and other anthropogenic stressors. For aquatic organisms, the consequences are poorly known but are likely to reflect both direct effects of declining oxygen bioavailability and interactions between oxygen and other stressors, including two-warming and acidification-that have received substantial attention in recent decades and that typically accompany oxygen changes. Drawing on the collected papers in this symposium volume ("An Oxygen Perspective on Climate Change"), we outline the causes and consequences of declining oxygen bioavailability. First, we discuss the scope of natural and predicted anthropogenic changes in aquatic oxygen levels. Although modern organisms are the result of long evolutionary histories during which they were exposed to natural oxygen regimes, anthropogenic change is now exposing them to more extreme conditions and novel combinations of low oxygen with other stressors. Second, we identify behavioral and physiological mechanisms that underlie the interactive effects of oxygen with other stressors, and we assess the range of potential organismal responses to oxygen limitation that occur across levels of biological organization and over multiple timescales. We argue that metabolism and energetics provide a powerful and unifying framework for understanding organism-oxygen interactions. Third, we conclude by outlining a set of approaches for maximizing the effectiveness of future work, including focusing on long-term experiments using biologically realistic variation in experimental factors and taking truly cross-disciplinary and integrative approaches to understanding and predicting future effects.

Projecting Future Climate Change-Mediated Impacts in Three Paralytic Shellfish Toxins-Producing Dinoflagellate Species.

Toxin-producing microalgae present a significant environmental risk for ecosystems and human societies when they reach concentrations that affect other aquatic organisms or human health. Harmful algal blooms (HAB) have been linked to mass wildlife die-offs and human food poisoning episodes, and climate change has the potential to alter the frequency, magnitude, and geographical extent of such events. Thus, a framework of species distribution models (SDMs), employing MaxEnt modeling, was used to project changes in habitat suitability and distribution of three key paralytic shellfish toxin (PST)-producing dinoflagellate species (i.e., Alexandrium catenella, A. minutum, and Gymnodinium catenatum), up to 2050 and 2100, across four representative concentration pathway scenarios (RCP-2.6, 4.5, 6.0, and 8.5; CMIP5). Despite slightly different responses at the regional level, the global habitat suitability has decreased for all the species, leading to an overall contraction in their tropical and sub-tropical ranges, while considerable expansions are projected in higher latitudes, particularly in the Northern Hemisphere, suggesting poleward distributional shifts. Such trends were exacerbated with increasing RCP severity. Yet, further research is required, with a greater assemblage of environmental predictors and improved occurrence datasets, to gain a more holistic understanding of the potential impacts of climate change on PST-producing species.

Impacts of Climate Change on the Biogeography of Three Amnesic Shellfish Toxin Producing Diatom Species.

Harmful algal blooms (HABs) are considered one of the main risks for marine ecosystems and human health worldwide. Climate change is projected to induce significant changes in species geographic distribution, and, in this sense, it is paramount to accurately predict how it will affect toxin-producing microalgae. In this context, the present study was intended to project the potential biogeographical changes in habitat suitability and occurrence distribution of three key amnesic shellfish toxin (AST)-producing diatom species (i.e., Pseudo-nitzschia australis, P. seriata, and P. fraudulenta) under four different climate change scenarios (i.e., RCP-2.6, 4.5, 6.0, and 8.5) up to 2050 and 2100. For this purpose, we applied species distribution models (SDMs) using four abiotic predictors (i.e., sea surface temperature, salinity, current velocity, and bathymetry) in a MaxEnt framework. Overall, considerable contraction and potential extirpation were projected for all species at lower latitudes together with projected poleward expansions into higher latitudes, mainly in the northern hemisphere. The present study aims to contribute to the knowledge on the impacts of climate change on the biogeography of toxin-producing microalgae species while at the same time advising the correct environmental management of coastal habitats and ecosystems.

First indication of deleterious impacts in white-seabream larvae (Diplodus sargus) survival and behaviour following acute venlafaxine exposure.

Wastewater effluents are teeming with organisms, nutrients and chemical substances which water treatment processes fail to remove. Among these substances, pharmaceuticals such as antidepressants are a frequent occurrence, and have been reported to lead to severe effects in the physiology and behaviour of non-target marine species across taxa. Venlafaxine (VFX) is one of the most consistently prescribed substances for the treatment of human depressive disorders, acting as a serotonin and norepinephrine reuptake inhibitor. In the present study, the potential effects of this antidepressant on the survival and key behaviours (i.e. movement, aggression and foraging) of white seabream (Diplodus sargus) larvae were addressed. Larvae were submitted to an acute exposure of two different VFX treatments (low concentration, 10 µg L-1; and high concentration, 100 µg L-1) for a total of 48 h. Sampling took place after 24 and 48 h of exposure. Overall, results showed a significant effect of a two-day exposure to VFX in larvae of D. sargus. Survival was significantly reduced by exposure to a high concentration, but behavioural effects of antidepressant exposure were subtle: i.e. increased attack frequency and temporary modulation of capture success. Further research efforts should be directed towards evaluating the potential chronic effects of antidepressants in marine species, if we are to anticipate possible pressures on natural populations, and effectively advice policymakers towards the investment in new and more efficient methods of wastewater treatments.

Ocean warming and acidification may challenge the riverward migration of glass eels.

The dramatic decline of European eel ( Anguilla anguilla) populations over recent decades has attracted considerable attention and concern. Furthermore, little is known about the sensitivity of the early stages of eels to projected future environmental change. Here, we investigated, for the first time, the potential combined effects of ocean warming (OW; Δ + 4°C; 18°C) and acidification (OA; Δ - 0.4 pH units) on the survival and migratory behaviour of A. anguilla glass eels, namely their preference towards riverine cues (freshwater and geosmin). Recently arrived individuals were exposed to isolated and combined OW and OA conditions for 100 days, adjusting for the salinity gradients associated with upstream migration. A two-choice test was used to investigate migratory activity and shifts in preference towards freshwater environments. While OW decreased survival and increased migratory activity, OA appears to hinder migratory response, reducing the preference for riverine cues. Our results suggest that future conditions could potentially favour an early settlement of glass eels, reducing the proportion of fully migratory individuals. Further research into the effects of climate change on eel migration and habitat selection is needed to implement efficient conservation plans for this critically endangered species.

Hypercapnia-induced disruption of long-distance mate-detection and reduction of energy expenditure in a coastal keystone crustacean.

Ocean acidification (OA) has been shown to disrupt behavioural responses either by affecting metabolic processes, or by effectively impairing an organisms' ability to gather and assess information and make decisions. Given the lack of information regarding the effects of high CO2 on olfactory-mediated mating behaviours in crustaceans, the possible chemosensory disruption in male mate-tracking in the keystone amphipod (Gammarus locusta) was assessed (after a two-generation acclimation to high CO2 conditions). In a series of behavioural trials, the response time, first direction of movement and the proportion of time spent in the presence of female scent cues were quantified. The possibility of high CO2-induced metabolic changes was assessed through routine metabolic rate (RMR) quantification. We found that hypercapnia was responsible for inducing a delay in response time latency and effectively disrupted accurate female cue-tracking. Moreover, RMR were significantly reduced under high CO2 in both genders. Such finding supports the hypothesis of hypercapnia-induced metabolic depression, which potentially underpins the increased latency in response time verified. Overall, the present study hints the potential disruption of chemosensory-dependent sexual behaviours, through some degree of chemosensory and metabolic disruption. These results emphasize the need for further behavioural tests regarding chemosensory communication in amphipods and energy metabolism, and suggest cascading consequences for the species' reproductive success and overall fitness in a future less alkaline ocean.

Transgenerational deleterious effects of ocean acidification on the reproductive success of a keystone crustacean (Gammarus locusta).

Ocean acidification (OA) poses a global threat to marine biodiversity. Notwithstanding, marine organisms may maintain their performance under future OA conditions, either through acclimation or evolutionary adaptation. Surprisingly, the transgenerational effects of high CO2 exposure in crustaceans are still poorly understood. For the first time, the present study investigated the transgenerational effect of OA, from hatching to maturity, of a key amphipod species (Gammarus locusta). Negative transgenerational effects were observed on survival of the acidified lineage, resulting in significant declines (10-15%) compared to the control groups in each generation. Mate-guarding duration was also significantly reduced under high CO2 and this effect was not alleviated by transgenerational acclimation, indicating that precopulatory behaviours can be disturbed under a future high CO2 scenario. Although OA may initially stimulate female investment, transgenerational exposure led to a general decline in egg number and fecundity. Overall, the present findings suggest a potential fitness reduction of natural populations of G. locusta in a future high CO2 ocean, emphasizing the need of management tools towards species' sustainability.