Climate change and population persistence in a hibernating marsupial.

Climate change has physiological consequences on organisms, ecosystems and human societies, surpassing the pace of organismal adaptation. Hibernating mammals are particularly vulnerable as winter survival is determined by short-term physiological changes triggered by temperature. In these animals, winter temperatures cannot surpass a certain threshold, above which hibernators arouse from torpor, increasing several fold their energy needs when food is unavailable. Here, we parameterized a numerical model predicting energy consumption in heterothermic species and modelled winter survival at different climate change scenarios. As a model species, we used the arboreal marsupial monito del monte (genus Dromiciops), which is recognized as one of the few South American hibernators. We modelled four climate change scenarios (from optimistic to pessimistic) based on IPCC projections, predicting that northern and coastal populations (Dromiciops bozinovici) will decline because the minimum number of cold days needed to survive the winter will not be attained. These populations are also the most affected by habitat fragmentation and changes in land use. Conversely, Andean and other highland populations, in cooler environments, are predicted to persist and thrive. Given the widespread presence of hibernating mammals around the world, models based on simple physiological parameters, such as this one, are becoming essential for predicting species responses to warming in the short term.

Perspectives on embryo maturation and seed quality in a global climate change scenario.

Global climate change has already brought noticeable alterations to multiple regions of our planet, including increased CO2 concentrations and changes in temperature. Several important steps of plant growth and development, such as embryogenesis, can be affected by such environmental changes; for instance, they affect how stored nutrients are used during early stages of seed germination during the transition from heterotrophic to autotrophic metabolism-a critical period for the seedling's survival. In this article, we briefly describe relevant processes that occur during embryo maturation and account for nutrient accumulation, which are sensitive to environmental change. Most of the nutrients stored in the seed during its development-including carbohydrates, lipids, and proteins, depending on the species-accumulate during the seed maturation stage. It is also known that iron, a key micronutrient for various electron transfer processes in plant cells, accumulates during embryo maturation. The existing literature indicates that climate change can not only affect the quality of the seed, in terms of total nutritional content, but also affect seed production. We discuss the potential effects of temperature and CO2 increases from an embryo-autonomous point of view, in an attempt to separate the effects on the parent plant from those on the embryo.

Fitness surfaces and local thermal adaptation in Drosophila along a latitudinal gradient.

Local adaptation is commonly cited to explain species distribution, but how fitness varies along continuous geographical gradients is not well understood. Here, we combine thermal biology and life-history theory to demonstrate that Drosophila populations along a 2500 km latitudinal cline are adapted to local conditions. We measured how heat tolerance and viability rate across eight populations varied with temperature in the laboratory and then simulated their expected cumulative Darwinian fitness employing high-resolution temperature data from their eight collection sites. Simulations indicate a trade-off between annual survival and cumulative viability, as both mortality and the recruitment of new flies are predicted to increase in warmer regions. Importantly, populations are locally adapted and exhibit the optimal combination of both traits to maximize fitness where they live. In conclusion, our method is able to reconstruct fitness surfaces employing empirical life-history estimates and reconstructs peaks representing locally adapted populations, allowing us to study geographic adaptation in silico.

Intra and interspecific variation in thermal performance and critical limits in anurans from southern Chile.

The relationship between temperature and performance can be illustrated through a thermal performance curve (TPC), which has proven useful in describing various aspects of ectotherms' thermal ecology and evolution. The parameters of the TPC can vary geographically due to large-scale variations in environmental conditions. However, only some studies have attempted to quantify how thermal performance varies over relatively small spatial scales, even in the same location or consistently among individuals within a species. Here, we quantified individual and species variation in thermal sensitivity of locomotor performance in five amphibia Eupsophus species found in the temperate rainforests of southern Chile and compared their estimates against co-occurring species that exhibit a substantially more extensive distributional range. We measured critical thermal limits and jumping performance under five different temperatures. Our results suggest that thermal responses are relatively conserved along the phylogeny, as the locomotor performance and thermal windows for activity remained narrow in Eupsophus species when compared against results observed for Batrachyla taeniata and Rhinella spinulosa. Additionally, we found significant individual differences in locomotor performance within most species, with individual consistency in performance observed across varied temperatures. Further analyses explored the influence of body size on locomotor performance and critical thermal limits within and between species. Our results suggest a trade-off scenario between thermal tolerance breadth and locomotor performance, where species exhibiting broader thermal ranges might have compromised performance. Interestingly, these traits seem partly mediated by body size variations, raising questions about potential ecological implications.

Beyond a single temperature threshold: Applying a cumulative thermal stress framework to plant heat tolerance.

Most plant thermal tolerance studies focus on single critical thresholds, which limit the capacity to generalise across studies and predict heat stress under natural conditions. In animals and microbes, thermal tolerance landscapes describe the more realistic, cumulative effects of temperature. We tested this in plants by measuring the decline in leaf photosynthetic efficiency (FV/FM) following a combination of temperatures and exposure times and then modelled these physiological indices alongside recorded environmental temperatures. We demonstrate that a general relationship between stressful temperatures and exposure durations can be effectively employed to quantify and compare heat tolerance within and across plant species and over time. Importantly, we show how FV/FM curves translate to plants under natural conditions, suggesting that environmental temperatures often impair photosynthetic function. Our findings provide more robust descriptors of heat tolerance in plants and suggest that heat tolerance in disparate groups of organisms can be studied with a single predictive framework.

Rapid turnover of a pea aphid superclone mediated by thermal endurance in central Chile.

Global change drivers are imposing novel conditions on Earth's ecosystems at an unprecedented rate. Among them, biological invasions and climate change are of critical concern. It is generally thought that strictly asexual populations will be more susceptible to rapid environmental alterations due to their lack of genetic variability and, thus, of adaptive responses. In this study, we evaluated the persistence of a widely distributed asexual lineage of the alfalfa race of the pea aphid, Acyrthosiphon pisum, along a latitudinal transect of approximately 600 km in central Chile after facing environmental change for a decade. Based on microsatellite markers, we found an almost total replacement of the original aphid superclone by a new variant. Considering the unprecedented warming that this region has experienced in recent years, we experimentally evaluated the reproductive performance of these two A. pisum lineages at different thermal regimes. The new variant exhibits higher rates of population increase at warmer temperatures, and computer simulations employing a representative temperature dataset suggest that it might competitively displace the original superclone. These results support the idea of a superclone turnover mediated by differential reproductive performance under changing temperatures.

Temperature variability and metabolic adaptation in terrestrial and aquatic ectotherms.

Thermodynamics is a major factor determining rates of energy expenditure, rates of biochemical dynamics, and ultimately the biological and ecological processes linked with resilience to global warming in ectothermic organisms. Nonetheless, whether ectothermic organisms exhibit general adaptive metabolic responses to cope with worldwide variation in thermal conditions has remained as an open question. Here we combine a model comparison approach with a global dataset of standard metabolic rates (SMR), including 1,160 measurements across 788 species of aquatic invertebrates, insects, fishes, amphibians and reptiles, to investigate the association between metabolic rates and environmental temperatures in their respective habitats. Our analyses suggest that variation in SMR after removing allometric and thermodynamic effects is best explained by the temperature range encountered across seasons, which always provided a better fit than the average temperature for the hottest and coldest month and mean annual temperatures. This pattern was consistent across taxonomic groups and robust to sensitivity analyses. Nonetheless, aquatic and terrestrial lineages responded differently to seasonality, with SMR declining - 6.8% °C-1 of thermal range across seasons in aquatic organisms and increasing 2.8% °C-1 in terrestrial organisms. These responses may reflect alternative strategies to mitigate the impact of increments in warmer temperatures on energy expenditure, either by means of metabolic reduction in thermally homogeneous water bodies or effective behavioral thermoregulation to exploit temperature heterogeneity on land.

Long-term forecast of thermal mortality with climate warming in riverine amphipods.

Forecasting long-term consequences of global warming requires knowledge on thermal mortality and how heat stress interacts with other environmental stressors on different timescales. Here, we describe a flexible analytical framework to forecast mortality risks by combining laboratory measurements on tolerance and field temperature records. Our framework incorporates physiological acclimation effects, temporal scale differences and the ecological reality of fluctuations in temperature, and other factors such as oxygen. As a proof of concept, we investigated the heat tolerance of amphipods Dikerogammarus villosus and Echinogammarus trichiatus in the river Waal, the Netherlands. These organisms were acclimated to different temperatures and oxygen levels. By integrating experimental data with high-resolution field data, we derived the daily heat mortality probabilities for each species under different oxygen levels, considering current temperatures as well as 1 and 2°C warming scenarios. By expressing heat stress as a mortality probability rather than a upper critical temperature, these can be used to calculate cumulative annual mortality, allowing the scaling up from individuals to populations. Our findings indicate a substantial increase in annual mortality over the coming decades, driven by projected increases in summer temperatures. Thermal acclimation and adequate oxygenation improved heat tolerance and their effects were magnified on longer timescales. Consequently, acclimation effects appear to be more effective than previously recognized and crucial for persistence under current temperatures. However, even in the best-case scenario, mortality of D. villosus is expected to approach 100% by 2100, while E. trichiatus appears to be less vulnerable with mortality increasing to 60%. Similarly, mortality risks vary spatially: In southern, warmer rivers, riverine animals will need to shift from the main channel toward the cooler head waters to avoid thermal mortality. Overall, this framework generates high-resolution forecasts on how rising temperatures, in combination with other environmental stressors such as hypoxia, impact ecological communities.

Temperature adaptation and its impact on the shape of performance curves in Drosophila populations.

Understanding how species adapt to different temperatures is crucial to predict their response to global warming, and thermal performance curves (TPCs) have been employed recurrently to study this topic. Nevertheless, fundamental questions regarding how thermodynamic constraints and evolution interact to shape TPCs in lineages inhabiting different environments remain unanswered. Here, we study Drosophila simulans along a latitudinal gradient spanning 3000 km to test opposing hypotheses based on thermodynamic constrains (hotter-is-better) versus biochemical adaptation (jack-of-all-temperatures) as primary determinants of TPCs variation across populations. We compare thermal responses in metabolic rate and the egg-to-adult survival as descriptors of organismal performance and fitness, respectively, and show that different descriptors of TPCs vary in tandem with mean environmental temperatures, providing strong support to hotter-is-better. Thermodynamic constraints also resulted in a strong negative association between maximum performance and thermal breadth. Lastly, we show that descriptors of TPCs for metabolism and egg-to-adult survival are highly correlated, providing evidence of co-adaptation, and that curves for egg-to-adult survival are systematically narrower and displaced toward lower temperatures. Taken together, our results support the pervasive role of thermodynamics constraining thermal responses in Drosophila populations along a latitudinal gradient, that are only partly compensated by evolutionary adaptation.

Phenotypic specialization of the pea aphid in its southern limit of distribution.

The success of biological invasions ultimately relies on phenotypic traits of the invasive species. Aphids, which include many important pests worldwide, may have been successful invading new environments partly because they can maximize reproductive output by becoming parthenogenetic and losing the sexual phase of their reproductive cycle. However, invasive populations of aphids invading wide ranges can face contrasting environmental conditions and requiring different phenotypic strategies. Besides transitions in their reproductive cycle, it is only partially known which phenotypic traits might be associated to the invasion success of aphid populations in extended novel ranges. Here, we used four genotypes of the pea aphid Acyrthosiphon pisum from two localities in Chile to test for phenotypic specialization that might explain their establishment and spread in habitats exhibiting contrasting environmental conditions. We show that lineages living at a higher latitude with low temperatures show, in addition to facultative sexual reproduction, smaller body sizes, lower metabolic rates and a higher tolerance to the cold than the obligate asexual lineages living in a mild weather, at the expense of fecundity. Conversely, at higher temperatures only asexual lineages were found, which exhibit larger body sizes, higher reproductive outputs and consequently enhanced demographic ability. As a result, in conjunction with the reproductive mode, lineage specialization in physiological and life-history traits could be taken into account as an important strategy for populations of pea aphid to effectively invade extended novel ranges comprising different climatic conditions.

Heat tolerance of marine ectotherms in a warming Antarctica.

Global warming is affecting the Antarctic continent in complex ways. Because Antarctic organisms are specialized to living in the cold, they are vulnerable to increasing temperatures, although quantitative analyses of this issue are currently lacking. Here we compiled a total of 184 estimates of heat tolerance belonging to 39 marine species and quantified how survival is affected concomitantly by the intensity and duration of thermal stress. Species exhibit thermal limits displaced toward colder temperatures, with contrasting strategies between arthropods and fish that exhibit low tolerance to acute heat challenges, and brachiopods, echinoderms, and molluscs that tend to be more sensitive to chronic exposure. These differences might be associated with mobility. A dynamic mortality model suggests that Antarctic organisms already encounter temperatures that might be physiologically stressful and indicate that these ecological communities are indeed vulnerable to ongoing rising temperatures.

El calentamiento global está afectando al continente antártico de formas complejas. Dado que los organismos antárticos están especializados a vivir en el frío, son vulnerables al aumento de las temperaturas, aunque en la actualidad hay carencia de análisis cuantitativos al respecto. Aquí recopilamos un total de 184 estimaciones de tolerancia al calor pertenecientes a 39 especies marinas, y cuantificamos cómo la supervivencia de estos organismos se ve afectada concomitantemente por la intensidad y la duración de un estrés térmico. Efectivamente las especies antárticas muestran límites térmicos desplazados hacia temperaturas más frías, con estrategias contrastadas entre los artrópodos y los peces que muestran una baja tolerancia a los desafíos térmicos agudos, y los braquiópodos, equinodermos y moluscos que tienden a ser más sensibles a la exposición crónica. Estas diferencias podrían estar asociadas con la movilidad. Un modelo dinámico de mortalidad sugiere que los organismos antárticos ya se enfrentan a temperaturas que podrían ser fisiológicamente estresantes e indican que estas comunidades ecológicas son realmente vulnerables al aumento continuo de las temperaturas.

Thermodynamic effects drive countergradient responses in the thermal performance of Littorina saxatilis across latitude.

Thermal performance curves (TPCs) provide a powerful framework to assess the evolution of thermal sensitivity in populations exposed to divergent selection regimes across latitude. However, there is a lack of consensus regarding the extent to which physiological adjustments that compensate for latitudinal temperature variation (metabolic cold adaptation; MCA) may alter the shape of TPCs, including potential repercussion on upper thermal limits. To address this, we compared TPCs for cardiac activity in latitudinally-separated populations of the intertidal periwinkle Littorina saxatilis. We applied a non-linear TPC modelling approach to explore how different metrics governing the shape of TPCs varied systematically in response to local adaptation and thermal acclimation. Both critical upper limits, and the temperatures at which cardiac performance was maximised, were higher in the northernmost (cold-adapted) population and displayed a countergradient latitudinal trend which was most pronounced following acclimation to low temperatures. We interpret this response as a knock-on consequence of increased standard metabolic rate in high latitude populations, indicating that physiological compensation associated with MCA may indirectly influence variation in upper thermal limits across latitude. Our study highlights the danger of assuming that variation in any one aspect of the TPC is adaptive without appropriate mechanistic and ecological context.

Biological trade-offs underpin coral reef ecosystem functioning.

Human impact increasingly alters global ecosystems, often reducing biodiversity and disrupting the provision of essential ecosystem services to humanity. Therefore, preserving ecosystem functioning is a critical challenge of the twenty-first century. Coral reefs are declining worldwide due to the pervasive effects of climate change and intensive fishing, and although research on coral reef ecosystem functioning has gained momentum, most studies rely on simplified proxies, such as fish biomass. This lack of quantitative assessments of multiple process-based ecosystem functions hinders local and regional conservation efforts. Here we combine global coral reef fish community surveys and bioenergetic models to quantify five key ecosystem functions mediated by coral reef fishes. We show that functions exhibit critical trade-offs driven by varying community structures, such that no community can maximize all functions. Furthermore, functions are locally dominated by few species, but the identity of dominant species substantially varies at the global scale. In fact, half of the 1,110 species in our dataset are functionally dominant in at least one location. Our results reinforce the need for a nuanced, locally tailored approach to coral reef conservation that considers multiple ecological functions beyond the effect of standing stock biomass.

Thermal tolerance in Drosophila: Repercussions for distribution, community coexistence and responses to climate change.

Here we combined controlled experiments and field surveys to determine if estimates of heat tolerance predict distributional ranges and phenology of different Drosophila species in southern South America. We contrasted thermal death time curves, which consider both magnitude and duration of the challenge to estimate heat tolerance, against the thermal range where populations are viable based on field surveys in an 8-year longitudinal study. We observed a strong correspondence of the physiological limits, the thermal niche for population growth, and the geographic ranges across studied species, which suggests that the thermal biology of different species provides a common currency to understand how species will respond to warming temperatures both at a local level and throughout their distribution range. Our approach represents a novel analytical toolbox to anticipate how natural communities of ectothermic organisms will respond to global warming.

Divergence in Thermal Physiology Could Contribute to Vertical Segregation in Intertidal Ecotypes of Littorina saxatilis.

AbstractThermal stress is a potentially important selective agent in intertidal marine habitats, but the role that thermal tolerance might play in local adaptation across shore height has been underexplored. Northwest Spain is home to two morphologically distinct ecotypes of the periwinkle Littorina saxatilis, separated by shore height and subject to substantial differences in thermal stress exposure. However, despite other biotic and abiotic drivers of ecotype segregation being well studied, their thermal tolerance has not been previously characterized. We investigated thermal tolerance across multiple life history stages by employing the thermal death time (TDT) approach to determine (i) whether the two ecotypes differ in thermal tolerance and (ii) how any differences vary with life history stage. Adults of the two ecotypes differed in their thermal tolerance in line with their shore position: the upper-shore ecotype, which experiences more extreme temperatures, exhibited greater endurance of thermal stress compared with the lower-shore ecotype. This difference was most pronounced at the highest temperatures tested. The proximate physiological basis for these differences is unknown but likely due to a multifarious interaction of traits affecting different parts of the TDT curve. Differences in tolerance between ecotypes were less pronounced in early life history stages but increased with ontogeny, suggesting partial divergence of this trait during development. Thermal tolerance could potentially play an important role in maintaining population divergence and genetic segregation between the two ecotypes, since the increased thermal sensitivity of the lower-shore ecotype may limit its dispersal onto the upper shore and so restrict gene flow.

Heterothermy as the Norm, Homeothermy as the Exception: Variable Torpor Patterns in the South American Marsupial Monito del Monte (Dromiciops gliroides).

Hibernation (i.e., multiday torpor) is considered an adaptive strategy of mammals to face seasonal environmental challenges such as food, cold, and/or water shortage. It has been considered functionally different from daily torpor, a physiological strategy to cope with unpredictable environments. However, recent studies have shown large variability in patterns of hibernation and daily torpor ("heterothermic responses"), especially in species from tropical and subtropical regions. The arboreal marsupial "monito del monte" (Dromiciops gliroides) is the last living representative of the order Microbiotheria and is known to express both short torpor episodes and also multiday torpor depending on environmental conditions. However, only limited laboratory experiments have documented these patterns in D. gliroides. Here, we combined laboratory and field experiments to characterize the heterothermic responses in this marsupial at extreme temperatures. We used intraperitoneal data loggers and simultaneous measurement of ambient and body temperatures (T A and T B, respectively) for analyzing variations in the thermal differential, in active and torpid animals. We also explored how this differential was affected by environmental variables (T A, natural photoperiod changes, food availability, and body mass changes), using mixed-effects generalized linear models. Our results suggest that: (1) individuals express short bouts of torpor, independently of T A and even during the reproductive period; (2) seasonal torpor also occurs in D. gliroides, with a maximum bout duration of 5 days and a mean defended T B of 3.6 ± 0.9°C (one individual controlled T B at 0.09°C, at sub-freezing T A); (3) the best model explaining torpor occurrence (Akaike information criteria weight = 0.59) discarded all predictor variables except for photoperiod and a photoperiod by food interaction. Altogether, these results confirm that this marsupial expresses a dynamic form of torpor that progresses from short torpor to hibernation as daylength shortens. These data add to a growing body of evidence characterizing tropical and sub-tropical heterothermy as a form of opportunistic torpor, expressed as daily or seasonal torpor depending on environmental conditions.

Spatial and temporal shift in the factors affecting the population dynamics of Calanus copepods in the North Sea.

The swap in abundance between two Calanus species in the North Sea during the 1980s constitutes a quintessential example of regime shift, with important ecosystemic and economic repercussions because these copepods constitute a major component of the diet of larval and juvenile cods. It is hypothesized that this transition was driven by gradual changes in primary productivity, the North Atlantic Oscillation (NAO) and sea surface temperatures (SST), and yet how these factors contribute to the population dynamics of these two species and the overall regime shift remains unclear. Here, we combine a highly resolved and spatially structured longitudinal dataset with population dynamics theory-based models to obtain a thorough and more detailed description of populations' responses to the regime shift observed in the North Sea. Our analyses highlight that this transition exhibits a clear spatial structure and involved a decoupling between the dynamics of Calanus finmarchicus and the NAO in western regions and between Calanus helgolandicus and SST in the eastern regions of the North Sea. Consequently, the observed switch in abundance between these species reflects the interaction between species-specific attributes, a well-defined spatial structure with a marked east-west axis and a decoupling between the ecological drivers and Calanus population dynamics following the shift. Succinctly, we suspect that higher water temperatures have favored C. helgolandicus and resulted in restrictive conditions for C. finmarchicus, eventually overshadowing the effects of NAO detected in historical records. Overall, our study illustrates how population dynamics theory can be successfully employed to disentangle the complex and multifactorial nature of a regime shift in response to gradually changing environmental conditions.

Thermal effects vary predictably across levels of organization: empirical results and theoretical basis.

Thermal performance curves have provided a common framework to study the impact of temperature in biological systems. However, few generalities have emerged to date. Here, we combine an experimental approach with theoretical analyses to demonstrate that performance curves are expected to vary predictably with the levels of biological organization. We measured rates of enzymatic reactions, organismal performance and population viability in Drosophila acclimated to different thermal conditions and show that performance curves become narrower with thermal optima shifting towards lower temperatures at higher levels or organization. We then explain these results on theoretical grounds, showing that this pattern reflects the cumulative impact of asymmetric thermal effects that piles up with complexity. These results and the proposed framework are important to understand how organisms, populations and ecological communities might respond to changing thermal conditions.

Energetic mechanisms for coping with changes in resource availability.

Given current anthropogenic alterations to many ecosystems and communities, it is becoming increasingly important to consider whether and how organisms can cope with changing resources. Metabolic rate, because it represents the rate of energy expenditure, may play a key role in mediating the link between resource conditions and performance and thereby how well organisms can persist in the face of environmental change. Here, we focus on the role that energy metabolism plays in determining organismal responses to changes in food availability over both short-term ecological and longer-term evolutionary timescales. Using a meta-analytical approach encompassing multiple species, we find that individuals with a higher metabolic rate grow faster under high food levels but slower once food levels decline, suggesting that the association between metabolism and life-history traits shifts along resource gradients. We also find that organisms can cope with changing resource availability through both phenotypic plasticity and genetically based evolutionary adaptation in their rates of energy metabolism. However, the metabolic rates of individuals within a population and of species within a lineage do not all respond in the same manner to changes in food availability. This diversity of responses suggests that there are benefits but also costs to changes in metabolic rate. It also underscores the need to examine not just the energy budgets of organisms within the context of metabolic rate but also how energy metabolism changes alongside other physiological and behavioural traits in variable environments.

Predicting temperature mortality and selection in natural Drosophila populations.

Average and extreme temperatures will increase in the near future, but how such shifts will affect mortality in natural populations is still unclear. We used a dynamic model to predict mortality under variable temperatures on the basis of heat tolerance laboratory measurements. Theoretical lethal temperatures for 11 Drosophila species under different warming conditions were virtually indistinguishable from empirical results. For Drosophila in the field, daily mortality predicted from ambient temperature records accumulate over weeks or months, consistent with observed seasonal fluctuations and population collapse in nature. Our model quantifies temperature-induced mortality in nature, which is crucial to study the effects of global warming on natural populations, and analyses highlight that critical temperatures are unreliable predictors of mortality.