Conservation of thermal physiology in tropical intertidal snails following an evolutionary transition to a cooler ecosystem: climate change implications.

Predictions for animal responses to climate warming usually assume that thermal physiology is adapted to present-day environments, and seldom consider the influence of evolutionary background. Little is known about the conservation of warm-adapted physiology following an evolutionary transition to a cooler environment. We used cardiac thermal performance curves (cTPCs) of six neritid gastropod species to study physiological thermal trait variation associated with a lineage transition from warmer rocky shores to cooler mangroves. We distinguished between functional thermal performance traits, related to energy homeostasis (slope gradient, slope curvature, HRmax, maximum cardiac activity and Topt, the temperature that maximizes cardiac activity) and a trait that limits performance (ULT, the upper lethal temperature). Considering the theory of optimal thermal performance, we predicted that the functional traits should be under greater selective pressure to change directionally and in magnitude than the thermal limit, which is redundant in the cooler environment. We found little variation in all traits across species, habitats and ecosystems, despite a ~20°C reduction in maximum habitat temperature in the mangrove species over 50 million years. While slope gradient was significantly lowered in the mangrove species, the effect difference was negated by greater thermal plasticity in the rocky shore species. ULT showed the least variation and suggested thermal specialization in the warmest habitat studied. The observed muted variation of the functional traits among the species may be explained by their limited role in energy acquisition and rather their association with heat tolerance adaptation, which is redundant in the mangrove species. These findings have implications for the conservation of habitat of intertidal gastropods that transition to cooler environments. Furthermore, they highlight the significance of evolutionary history and physiological conservation when predicting species responses to climate change.

Mismatch between the ecological processes driving early life-stage dynamics of bivalves at two contrasting French Polynesian lagoons.

The pearl-farming industry depends mostly on the natural recruitment of pearl oysters. Little is known about the relative influence of different ecological processes on the natural recruitment of pearl oysters across biogeographical scales. Spatio-temporal dynamics of bivalve larvae and spats were described at Ahe and Mangareva, 1500 km apart across French Polynesia. We quantified the effect of candidate environmental predictors on the dynamics of larvae. Both lagoons showed similar temporal dynamics with twice more larvae and 6 times more spat in Ahe. Pinctada maculata spat were more abundant than for P. margaritifera at both lagoons. While the temporal dynamics in larvae abundance were best explained by a positive effect of temperature in Ahe, the dynamics in Mangareva were poorly predicted by the environmental variables, meaning bivalve early-life stages perform better in Ahe than Mangareva suggesting a mismatch between the relevant environmental forces driving larval dynamics at these two contrasting lagoons.

Gene expression plasticity, genetic variation and fatty acid remodelling in divergent populations of a tropical bivalve species.

Ocean warming challenges marine organisms' resilience, especially for species experiencing temperatures close to their upper thermal limits. A potential increase in thermal tolerance might significantly reduce the risk of population decline, which is intrinsically linked to variability in local habitat temperatures. Our goal was to assess the plastic and genetic potential of response to elevated temperatures in a tropical bivalve model, Pinctada margaritifera. We benefit from two ecotypes for which local environmental conditions are characterized by either large diurnal variations in the tide pools (Marquesas archipelago) or low mean temperature with stable to moderate seasonal variations (Gambier archipelago). We explored the physiological basis of individual responses to elevated temperature, genetic divergence as well as plasticity and acclimation by combining lipidomic and transcriptomic approaches. We show that P. margaritifera has certain capacities to adjust to long-term elevated temperatures that was thus far largely underestimated. Genetic variation across populations overlaps with gene expression and involves the mitochondrial respiration machinery, a central physiological process that contributes to species thermal sensitivity and their distribution ranges. Our results present evidence for acclimation potential in P. margaritifera and urge for longer term studies to assess populations resilience in the face of climate change.

Le réchauffement des océans remet en question la résilience des organismes marins, en particulier pour les espèces connaissant des températures proches de leurs limites thermiques supérieures. Une augmentation potentielle de la tolérance thermique pourrait ainsi réduire considérablement le risque de déclin de la population. L'objectif de cette étude était d'évaluer le potentiel plastique et génétique de la réponse à l'exposition courte et chronique à températures élevées chez une espèce de bivalve tropical, Pinctada margaritifera. Ce modèle bénéficie de l'existence de deux écotypes pour lesquels les conditions environnementales locales sont caractérisées soit par de fortes variations diurnes associées aux marées (archipel des Marquises) soit par une température moyenne plus basse et des variations saisonnières prononcées (archipel des Gambier). Nous avons exploré les bases physiologiques des réponses individuelles ainsi que la divergence génétique et quantifié la plasticité en combinant des approches lipidomique et transcriptomique. Nous montrons que P. margaritifera possède des capacités d'acclimatation à des températures élevées sur le long terme jusqu'à présent largement sous-estimées. La divergence génétique entre populations est par ailleurs associée à des différences d'expression des gènes et implique la machinerie respiratoire mitochondriale, un processus physiologique central qui contribue à la sensibilité thermique des espèces et à leurs répartitions. Nos résultats présentent les bases des potentiels d'acclimatation chez P. margaritifera et soulignent l'importance d'études à plus long terme pour évaluer la résilience des populations face au changement climatique.

Informing spread predictions of two alien snails using movement traits.

Invasive alien species are a growing global problem, and aquatic ecosystems have been regarded as particularly vulnerable. Biological invasions can alter ecosystem functioning, threaten native biodiversity and burden the global economy. Understanding alien species ability to disperse via locomotion following arrival to new environments is critical for prediction of spread rates. Here, we quantified in-field densities and compared movement traits between two widespread invasive alien snails, Tarebia granifera and Physa acuta. We measured the: (i) net distance and velocity to determine dispersal potential; and (ii) turning angles (both absolute and relative) and straightness index as proxies for exploratory behaviour. Tarebia granifera exhibited a significantly greater velocity and covered a significantly larger net distance (i.e., greater spread rate) than Physa acuta. In-field densities were marked for both species (T. granifera: mean 351 individuals m-2; P. acuta: mean 235 individuals m-2), but differed spatially. The exploratory behavior (i.e., mean or absolute turning angles and straightness index) did not differ significantly between the two alien species; both species showed a slight tendency to turn counterclockwise. The present study suggests a more rapid capacity to self-disperse in T. granifera than P. acuta, which could facilitate rapid spread within and between aquatic systems. Thus, this current study highlights the often-overlooked role of animal behaviour in promoting invasion; this autecological information can help inform predictive models for the spread of alien snails within freshwater ecosystems.

Dynamic Energy Budget model suggests feeding constraints and physiological stress in black-lip pearl oysters, 5 years post mass-mortality event.

Mass-mortality events of marine species can disturb the structure of communities. While identifying the causes of mass-mortality events is crucial for implementing recovery strategies, monitoring is challenging in remote locations. Black-lip pearl oysters (Pinctada margaritifera) are farmed for producing black pearls within remote atolls of French Polynesia. Previous mass-mortality events have resulted in the collapse of oysters and other species; however, the causes and conditions that favour recovery are unclear. We investigated the potential for oyster population recovery 5 years after a mortality event at Takaroa Atoll (Tuamotu Archipelago). Temperature, food availability (total chlorophyll-a), growth and reproduction were monitored. Growth was also simulated using a Dynamic Energy Budget model. Despite favourable conditions, reduced growth and reproduction signalled an energetic deficit. The model overpredicted growth, and supported the hypotheses that individuals are unable to profit from the phytoplankton available and maintenance costs are high in Takaroa, ultimately explaining their poor physiological condition.

Ectoparasites reduce scope for growth in a rocky-shore mussel (Perna perna) by raising maintenance costs.

Endolithic cyanobacteria are ubiquitous colonisers of organic and inorganic carbonate substrata that frequently attack the shells of mussels, eroding the shell to extract carbon, often with population infestation rates of >80%. This reduces host physiological condition and ultimately leads to shell collapse and mortality, compromising the services provided by these important ecosystem engineers. While the ecological implications of this and similar interactions have been examined, our understanding of the underlying mechanisms driving the physiological responses of infested hosts remains limited. Using field and laboratory experiments, we assessed the energetic costs of cyanobacterial infestation to the intertidal brown mussel (Perna perna). In the field we found that growth (measured as both increase in shell length and rate of biomineralization) and reproductive potential of clean mussels are greater than those of infested individuals. To explore the mechanisms behind these effects, we compared the energy allocation of parasite-free and infested mussels using the scope for growth (SFG) framework. This revealed a lower SFG in parasitized mussels attributed to an energetic imbalance caused by increased standard metabolic rates, without compensation through increased feeding or reduced excretion of ammonia. Separate laboratory assays showed no differences in calcium uptake rates, indicating that infested mussels do not compensate for shell erosion through increased mineralization. This suggests that the increased maintenance costs detected reflect repair of the organic component of the inner nacreous layer of the shell, an energetically more demanding process than mineralization. Thus, parasite-inflicted damage reduces SFG directly through the need for increased basal metabolic rate to drive shell repair without compensatory increases in energy intake. This study provides a first perspective of the physiological mechanisms underlying this parasite-host interaction, a critical step towards a comprehensive understanding of the ecological processes driving dynamics of this intertidal ecosystem engineer.

Opposing life stage-specific effects of ocean warming at source and sink populations of range-shifting coral-reef fishes.

Climate change is altering the latitudinal distributions of species, with their capacity to keep pace with a shifting climate depending on the stochastic expression of population growth rates, and the influence of compensatory density feedback on age-specific survival rates. We use population-abundance time series at the leading edge of an expanding species' range to quantify the contribution of stochastic environmental drivers and density feedbacks to the dynamics of life stage-specific population growth. Using a tropical, range-shifting Indo-Pacific damselfish (Abudefduf vaigiensis) as a model organism, we applied variants of the phenomenological Gompertz-logistic model to a 14-year dataset to quantify the relative importance of density feedback and stochastic environmental drivers on the separate and aggregated population growth rates of settler and juvenile life stages. The top-ranked models indicated that density feedback negatively affected the growth of tropical settlers and juveniles. Rates of settlement were negatively linked to temperatures experienced by parents at potential source populations in the tropics, but their subsequent survival and that of juveniles increased with the temperatures experienced at the temperate sink. Including these stochastic effects doubled the deviance explained by the models, corroborating an important role of temperature. By incorporating sea-surface temperature projections for the remainder of this century into these models, we anticipate improved conditions for the population growth of juvenile coral-reef fishes, but not for settlers in temperate ecosystems. Previous research has highlighted the association between temperature and the redistribution of species. Our analyses reveal the contrasting roles of different life stages in the dynamics of range-shifting species responding to climate change, as they transition from vagrancy to residency in their novel ranges.

Dietary generalism accelerates arrival and persistence of coral-reef fishes in their novel ranges under climate change.

Climate change is redistributing marine and terrestrial species globally. Life-history traits mediate the ability of species to cope with novel environmental conditions, and can be used to gauge the potential redistribution of taxa facing the challenges of a changing climate. However, it is unclear whether the same traits are important across different stages of range shifts (arrival, population increase, persistence). To test which life-history traits most mediate the process of range extension, we used a 16-year dataset of 35 range-extending coral-reef fish species and quantified the importance of various traits on the arrival time (earliness) and degree of persistence (prevalence and patchiness) at higher latitudes. We show that traits predisposing species to shift their range more rapidly (large body size, broad latitudinal range, long dispersal duration) did not drive the early stages of redistribution. Instead, we found that as diet breadth increased, the initial arrival and establishment (prevalence and patchiness) of climate migrant species in temperate locations occurred earlier. While the initial incursion of range-shifting species depends on traits associated with dispersal potential, subsequent establishment hinges more on a species' ability to exploit novel food resources locally. These results highlight that generalist species that can best adapt to novel food sources might be most successful in a future ocean.

Applicability of Dynamic Energy Budget (DEB) models across steep environmental gradients.

Robust ecological forecasting requires accurate predictions of physiological responses to environmental drivers. Energy budget models facilitate this by mechanistically linking biology to abiotic drivers, but are usually ground-truthed under relatively stable physical conditions, omitting temporal/spatial environmental variability. Dynamic Energy Budget (DEB) theory is a powerful framework capable of linking individual fitness to environmental drivers and we tested its ability to accommodate variability by examining model predictions across the rocky shore, a steep ecotone characterized by wide fluctuations in temperature and food availability. We parameterized DEB models for co-existing mid/high-shore (Mytilus galloprovincialis) and mid/low-shore (Perna perna) mussels on the south coast of South Africa. First, we assumed permanently submerged conditions, and then incorporated metabolic depression under low tide conditions, using detailed data of tidal cycles, body temperature and variability in food over 12 months at three sites. Models provided good estimates of shell length for both species across the shore, but predictions of gonadosomatic index were consistently lower than observed. Model disagreement could reflect the effects of details of biology and/or difficulties in capturing environmental variability, emphasising the need to incorporate both. Our approach provides guidelines for incorporating environmental variability and long-term change into mechanistic models to improve ecological predictions.

Decoupling of behavioural and physiological thermal performance curves in ectothermic animals: a critical adaptive trait.

Thermal performance curves (TPCs) represent an increasingly popular tool in ecology for anticipating species responses to climate change. TPC theory has been developed using species that experience similar temperatures during activity and at rest and consequently exhibit thermal ranges for activity that closely coincide with their physiological thermal tolerances. Many species, however, experience other stressors, such as desiccation, that limit active behaviour at temperatures below the maximum values experienced. As a result, activity is constrained to a narrow thermal window that is a subset of the range of temperatures that can be tolerated physiologically. This results in a decoupling of behavioural and physiological TPCs that does not conform to the present paradigm. To test the generality of TPC theory, we measured thermal responses for behaviour (crawling speed) and physiological tolerance (heart rate) for six rocky shore gastropods spanning a thermal/desiccation stress gradient. We hypothesized a positive relationship between shore level and the degree of decoupling of behavioural and physiological TPCs. This prediction was confirmed, and was explained by the extension of the physiological TPC beyond the range of the behavioural TPC. Decoupling of behavioural and physiological TPCs is central to predicting accurately the fitness dynamics of ectothermic species subject to multiple stressors. We believe that this decoupling should be explicitly considered as an adaptive trait defining an organism's thermal niche.

Long-term, high frequency in situ measurements of intertidal mussel bed temperatures using biomimetic sensors.

At a proximal level, the physiological impacts of global climate change on ectothermic organisms are manifest as changes in body temperatures. Especially for plants and animals exposed to direct solar radiation, body temperatures can be substantially different from air temperatures. We deployed biomimetic sensors that approximate the thermal characteristics of intertidal mussels at 71 sites worldwide, from 1998-present. Loggers recorded temperatures at 10-30 min intervals nearly continuously at multiple intertidal elevations. Comparisons against direct measurements of mussel tissue temperature indicated errors of ~2.0-2.5 °C, during daily fluctuations that often exceeded 15°-20 °C. Geographic patterns in thermal stress based on biomimetic logger measurements were generally far more complex than anticipated based only on 'habitat-level' measurements of air or sea surface temperature. This unique data set provides an opportunity to link physiological measurements with spatially- and temporally-explicit field observations of body temperature.

Personality, foraging behavior and specialization: integrating behavioral and food web ecology at the individual level.

Behavioral traits and diet were traditionally thought to be highly plastic within individuals. This view was espoused in the widespread use of optimality models, which broadly predict that individuals can modify behavioral traits and diet across ecological contexts to maximize fitness. Yet, research conducted over the past 15 years supports an alternative view; fundamental behavioral traits (e.g., activity level, exploration, sociability, boldness and aggressiveness) and diet often vary among individuals and this variation persists over time and across contexts. This phenomenon has been termed animal personality with regard to behavioral traits and individual specialization with regard to diet. While these aspects of individual-level phenotypic variation have been thus far studied in isolation, emerging evidence suggests that personality and individual specialization may covary, or even be causally related. Building on this work, we present the overarching hypothesis that animal personality can drive specialization through individual differences in various aspects of consumer foraging behavior. Specifically, we suggest pathways by which consumer personality traits influence foraging activity, risk-dependent foraging, roles in social foraging groups, spatial aspects of foraging and physiological drivers of foraging, which in turn can lead to consistent individual differences in food resource use. These pathways provide a basis for generating testable hypotheses directly linking animal personality to ecological dynamics, a major goal in contemporary behavioral ecology.

An adaptable toolkit to assess commercial fishery costs and benefits related to marine protected area network design.

Around the world, governments are establishing Marine Protected Area (MPA) networks to meet their commitments to the United Nations Convention on Biological Diversity. MPAs are often used in an effort to conserve biodiversity and manage fisheries stocks. However, their efficacy and effect on fisheries yields remain unclear. We conducted a case-study on the economic impact of different MPA network design strategies on the Atlantic cod ( Gadus morhua) fisheries in Canada. The open-source R toolbox that we developed to analyze this case study can be customized to conduct similar analyses for other systems. We used a spatially-explicit individual-based model of population growth and dispersal coupled with a fisheries management and harvesting component. We found that MPA networks that both protect the target species' habitat (particularly the spawning grounds), and were spatially optimized to improve population connectivity had the highest net present value (i.e., were most profitable for the fishing industry). These higher profits were achieved primarily by reducing the distance travelled for fishing and reducing the probability of a moratorium event. These findings add to a growing body of knowledge demonstrating the importance of incorporating population connectivity in the MPA planning process, as well as the ability of this R toolbox to explore ecological and economic consequences of alternative MPA network designs.

A Dynamic Energy Budget (DEB) model for the keystone predator Pisaster ochraceus.

We present a Dynamic Energy Budget (DEB) model for the quintessential keystone predator, the rocky-intertidal sea star Pisaster ochraceus. Based on first principles, DEB theory is used to illuminate underlying physiological processes (maintenance, growth, development, and reproduction), thus providing a framework to predict individual-level responses to environmental change. We parameterized the model for P. ochraceus using both data from the literature and experiments conducted specifically for the DEB framework. We devoted special attention to the model's capacity to (1) describe growth trajectories at different life-stages, including pelagic larval and post-metamorphic phases, (2) simulate shrinkage when prey availability is insufficient to meet maintenance requirements, and (3) deal with the combined effects of changing body temperature and food supply. We further validated the model using an independent growth data set. Using standard statistics to compare model outputs with real data (e.g. Mean Absolute Percent Error, MAPE) we demonstrated that the model is capable of tracking P. ochraceus' growth in length at different life-stages (larvae: MAPE = 12.27%; post-metamorphic, MAPE = 9.22%), as well as quantifying reproductive output index. However, the model's skill dropped when trying to predict changes in body mass (MAPE = 24.59%), potentially because of the challenge of precisely anticipating spawning events. Interestingly, the model revealed that P. ochraceus reserves contribute little to total biomass, suggesting that animals draw energy from structure when food is limited. The latter appears to drive indeterminate growth dynamics in P. ochraceus. Individual-based mechanistic models, which can illuminate underlying physiological responses, offer a viable framework for forecasting population dynamics in the keystone predator Pisaster ochraceus. The DEB model herein represents a critical step in that direction, especially in a period of increased anthropogenic pressure on natural systems and an observed recent decline in populations of this keystone species.

Tipping points, thresholds and the keystone role of physiology in marine climate change research.

The ongoing and future effects of global climate change on natural and human-managed ecosystems have led to a renewed interest in the concept of ecological thresholds or tipping points. While generalizations such as poleward range shifts serve as a useful heuristic framework to understand the overall ecological impacts of climate change, sophisticated approaches to management require spatially and temporally explicit predictions that move beyond these oversimplified models. Most approaches to studying ecological thresholds in marine ecosystems tend to focus on populations, or on non-linearities in physical drivers. Here we argue that many of the observed thresholds observed at community and ecosystem levels can potentially be explained as the product of non-linearities that occur at three scales: (a) the mechanisms by which individual organisms interact with their ambient habitat, (b) the non-linear relationship between organismal physiological performance and variables such as body temperature and (c) the indirect effects of physiological stress on species interactions such as competition and predation. We explore examples at each of these scales in detail and explain why a failure to consider these non-linearities - many of which can be counterintuitive - can lead to Type II errors (a failure to predict significant ecological responses to climate change). Specifically, we examine why ecological thresholds can occur well before concomitant thresholds in physical drivers are observed, i.e. how even small linear changes in the physical environment can lead to ecological tipping points. We advocate for an integrated framework that combines biophysical, ecological and physiological methods to generate hypotheses that can be tested using experimental manipulation as well as hindcasting and nowcasting of observed change, on a spatially and temporally explicit basis.