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A quantitative understanding of physiological thermal responses is vital for forecasting species distributional shifts in response to climate change. Many studies have focused on metabolic rate as a global metric for analyzing the sublethal effects of changing environments on physiology. Thermal performance curves (TPCs) have been suggested as a viable analytical framework, but standard TPCs may not fully capture physiological responses, due in part to failure to consider the process of metabolic depression. We derived a model based on the nonlinear regression of biological temperature-dependent rate processes and built a heart rate data set for 26 species of intertidal molluscs distributed from 33°S to ~40°N. We then calculated physiological thermal performance limits with continuous heating using T 1 / 2 H , the temperature at which heart rate is decreased to 50% of the maximal rate, as a more realistic measure of upper thermal limits. Results indicate that heat-induced metabolic depression of cardiac performance is a common adaptive response that allows tolerance of harsh environments. Furthermore, our model accounted for the high inter-individual variability in the shape of cardiac TPCs. We then used these TPCs to calculate physiological thermal safety margins (pTSM), the difference between the maximal operative temperature (95th percentile of field temperatures) and T 1 / 2 H of each individual. Using pTSMs, we developed a physiological species distribution model (pSDM) to forecast future geographic distributions. pSDM results indicate that climate-induced species range shifts are potentially less severe than predicted by a simple correlative SDM. Species with metabolic depression below the optimum temperature will be more thermal resistant at their warm trailing edges. High intraspecific variability further suggests that models based on species-level vulnerability to environmental change may be problematic. This multi-scale, mechanistic understanding that incorporates metabolic depression and inter-individual variability in thermal response enables better predictions about the relationship between thermal stress and species distributions.
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Termotolerancia , Adaptación Fisiológica , Cambio Climático , Calor , TemperaturaRESUMEN
Ecologically dominant species often define ecosystem states, but as human disturbances intensify, their subordinate counterparts increasingly displace them. We consider the duality of disturbance by examining how environmental drivers can simultaneously act as a stressor to dominant species and as a resource to subordinates. Using a model ecosystem, we demonstrate that CO2 -driven interactions between species can account for such reversals in dominance; i.e., the displacement of dominants (kelp forests) by subordinates (turf algae). We established that CO2 enrichment had a direct positive effect on productivity of turfs, but a negligible effect on kelp. CO2 enrichment further suppressed the abundance and feeding rate of the primary grazer of turfs (sea urchins), but had an opposite effect on the minor grazer (gastropods). Thus, boosted production of subordinate producers, exacerbated by a net reduction in its consumption by primary grazers, accounts for community change (i.e., turf displacing kelp). Ecosystem collapse, therefore, is more likely when resource enrichment alters competitive dominance of producers, and consumers fail to compensate. By recognizing such duality in the responses of interacting species to disturbance, which may stabilize or exacerbate change, we can begin to understand how intensifying human disturbances determine whether or not ecosystems undergo phase shifts.
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Ecosistema , Kelp , Animales , Dióxido de Carbono , Humanos , Concentración de Iones de Hidrógeno , Agua de MarRESUMEN
Intertidal habitats are among the harshest environments on the planet, and have emerged as a model system for exploring the ecological impacts of global climate change. Deploying reliable instrumentation to measure environmental conditions such as temperature is challenging in this environment. The application of wireless sensor networks (WSNs) shows considerable promise as a means of optimizing continuous data collection, but poor link quality and unstable connections between nodes, caused by harsh physical environmental conditions, bring about a delay problem. In this paper, we model and analyze the components of delays in an intertidal wireless sensor network system (IT-WSN). We show that, by properly selecting routing pathways, it is feasible to improve delay. To this end, we propose a Predictive Delay Optimization (Pido) framework, which provides a new metric for routing path selection. Pido incorporates delay introduced by both link quality and node conditions, and designs a classifier to predict future conditions of nodes, i.e., the likely time of aerial exposure at low tide in this case. We evaluate the performance of Pido in both a real IT-WSN system and a large-scale simulation, the result demonstrates that Pido decreases up to 73% of delays on average with limited overhead.
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Biogeographic distributions are driven by cumulative effects of smaller scale processes. Thus, vulnerability of animals to thermal stress is the result of physiological sensitivities to body temperature (Tb), microclimatic conditions, and behavioural thermoregulation. To understand interactions among these variables, we analysed the thermal tolerances of three species of intertidal snails from different latitudes along the Chinese coast, and estimated potential Tb in different microhabitats at each site. We then empirically determined the temperatures at which heart rate decreased sharply with rising temperature (Arrhenius breakpoint temperature, ABT) and at which it fell to zero (flat line temperature, FLT) to calculate thermal safety margins (TSM). Regular exceedance of FLT in sun-exposed microhabitats, a lethal effect, was predicted for only one mid-latitude site. However, ABTs of some individuals were exceeded at sun-exposed microhabitats in most sites, suggesting physiological impairment for snails with poor behavioural thermoregulation and revealing inter-individual variations (physiological polymorphism) of thermal limits. An autocorrelation analysis of Tb showed that predictability of extreme temperatures was lowest at the hottest sites, indicating that the effectiveness of behavioural thermoregulation is potentially lowest at these sites. These results illustrate the critical roles of mechanistic studies at small spatial scales when predicting effects of climate change.
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Calor , Microclima , Caracoles/fisiología , Estrés Fisiológico , Animales , Cambio ClimáticoRESUMEN
Urbanization of coastlines is leading to increased introduction of nutrients from the terrestrial environment to nearshore habitats. While such nutrient influxes can be detrimental to coastal marine organisms due to increased eutrophication and subsequent reduced oxygen, they could also have positive effects (i.e., increased food availability) on species that are nitrogen-limited such as macroalgae. Nutrient enrichment in this environment thus has the potential to counteract some of the negative impacts of increasing temperatures, at least for some species. Characterizing the physiological response of organisms to simultaneous changes in multiple drivers such as these is an important first step in predicting how global climate change may lead to ecological responses at more local levels. We evaluated how nutrient enrichment (i.e., nitrogen availability) affected the growth of Fucus vesiculosus, a foundational macroalgal species in the North Atlantic rocky intertidal zone, and found that nutrient-enriched algal blades showed a significant increase in tissue growth compared to individuals grown under ambient conditions. We further quantified net photosynthesis by ambient and nutrient-enriched tissues at saturating irradiance over a range of temperature conditions (6-30°C). Respiration was unaffected by nutrient treatment; however, there was a significant increase in photosynthetic oxygen production for nutrient-enriched tissue compared to ambient, but only at elevated (≥18°C) temperatures. This study contributes to a growing body of literature showing the complexity of responses to changes in multiple drivers, and highlights the importance of studying the impacts of global climate change within the context of more local environmental conditions.
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Cambio Climático , Fucus/crecimiento & desarrollo , Fucus/metabolismo , Nitrógeno/metabolismo , Fotosíntesis , Calor/efectos adversos , Massachusetts , Nutrientes/metabolismo , Algas Marinas/crecimiento & desarrollo , Algas Marinas/metabolismoRESUMEN
Although theory suggests geographic variation in species' performance is determined by multiple niche parameters, little consideration has been given to the spatial structure of interacting stressors that may shape local and regional vulnerability to global change. Here, we use spatially explicit mosaics of carbonate chemistry, food availability and temperature spanning 1280 km of coastline to test whether persistent, overlapping environmental mosaics mediate the growth and predation vulnerability of a critical foundation species, the mussel Mytilus californianus. We find growth was highest and predation vulnerability was lowest in dynamic environments with frequent exposure to low pH seawater and consistent food. In contrast, growth was lowest and predation vulnerability highest when exposure to low pH seawater was decoupled from high food availability, or in exceptionally warm locations. These results illustrate how interactions among multiple drivers can cause unexpected, yet persistent geographic mosaics of species performance, interactions and vulnerability to environmental change.
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Ambiente , Mytilus/fisiología , Conducta Predatoria , Animales , California , Concentración de Iones de Hidrógeno , Oregon , Agua de Mar/química , TemperaturaRESUMEN
Thermal performance curves (TPCs), which quantify how an ectotherm's body temperature (Tb ) affects its performance or fitness, are often used in an attempt to predict organismal responses to climate change. Here, we examine the key - but often biologically unreasonable - assumptions underlying this approach; for example, that physiology and thermal regimes are invariant over ontogeny, space and time, and also that TPCs are independent of previously experienced Tb. We show how a critical consideration of these assumptions can lead to biologically useful hypotheses and experimental designs. For example, rather than assuming that TPCs are fixed during ontogeny, one can measure TPCs for each major life stage and incorporate these into stage-specific ecological models to reveal the life stage most likely to be vulnerable to climate change. Our overall goal is to explicitly examine the assumptions underlying the integration of TPCs with Tb , to develop a framework within which empiricists can place their work within these limitations, and to facilitate the application of thermal physiology to understanding the biological implications of climate change.
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Adaptación Fisiológica , Regulación de la Temperatura Corporal , Cambio Climático , Animales , Ambiente , Modelos Biológicos , Factores de TiempoRESUMEN
Body temperature is universally recognized as a dominant driver of biological performance. Although the critical distinction between the temperature of an organism and its surrounding habitat has long been recognized, it remains common practice to assume that trends in air temperature-collected via remote sensing or weather stations-are diagnostic of trends in animal temperature and thus of spatiotemporal patterns of physiological stress and mortality risk. Here, by analysing long-term trends recorded by biomimetic temperature sensors designed to emulate intertidal mussel temperature across the US Pacific Coast, we show that trends in maximal organismal temperature ('organismal climatologies') during aerial exposure can differ substantially from those exhibited by co-located environmental data products. Specifically, using linear regression to compare maximal organismal and environmental (air temperature) climatologies, we show that not only are the magnitudes of body and air temperature markedly different, as expected, but so are their temporal trends at both local and biogeographic scales, with some sites showing significant decadal-scale increases in organismal temperature despite reductions in air temperature, or vice versa. The idiosyncratic relationship between the spatiotemporal patterns of organismal and air temperatures suggests that environmental climatology cannot be statistically corrected to serve as an accurate proxy for organismal climatology. Finally, using quantile regression, we show that spatiotemporal trends vary across the distribution of organismal temperature, with extremes shifting in different directions and at different rates than average metrics. Overall, our results highlight the importance of quantifying changes in the entire distribution of temperature to better predict biological performance and dispel the notion that raw or 'corrected' environmental (and specially air temperature) climatologies can be used to predict organismal temperature trends. Hence, despite their widespread coverage and availability, the severe limitations of environmental climatologies suggest that their role in conservation and management policy should be carefully considered.
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As on land, oceans exhibit high temporal and spatial temperature variation. This "ocean weather" contributes to the physiological and ecological processes that ultimately determine the patterns of species distribution and abundance, yet is often unrecognized, especially in tropical oceans. Here, we tested the paradigm of temperature stability in shallow waters (<12.5 m) across different zones of latitude. We collated hundreds of in situ, high temporal-frequency ocean temperature time series globally to produce an intuitive measure of temperature variability, ranging in scale from quarter-diurnal to annual time spans. To estimate organismal sensitivity of ectotherms (i.e. microbes, algae, and animals whose body temperatures depend upon ocean temperature), we computed the corresponding range of biological rates (such as metabolic rate or photosynthesis) for each time span, assuming an exponential relationship. We found that subtropical regions had the broadest temperature ranges at time spans equal to or shorter than a month, while temperate and tropical systems both exhibited narrow (i.e. stable) short-term temperature range estimates. However, temperature-dependent biological rates in tropical regions displayed greater ranges than in temperate systems. Hence, our results suggest that tropical ectotherms may be relatively more sensitive to short-term thermal variability. We also highlight previously unexplained macroecological patterns that may be underpinned by short-term temperature variability.
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Body temperature is a more pertinent variable to physiological stress than ambient air temperature. Modeling and empirical studies on the impacts of climate change on ectotherms usually assume that body temperature within organisms is uniform. However, many ectotherms show significant within-body temperature heterogeneity. The relationship between regional heterothermy and the response of ectotherms to sublethal and lethal conditions remains underexplored. We quantified within-body thermal heterogeneity in an intertidal sea star (Pisaster ochraceus) during aerial exposure at low tide to examine the lethal and sublethal effects of temperatures of different body regions. In manipulative experiments, we measured the temperature of the arms and central disc, as well as survival and arm abscission under extreme aerial conditions. Survival was related strongly to central disc temperature. Arms were generally warmer than the central disc in individuals that survived aerial heating, but we found the reverse in those that died. When the central disc reached sublethal temperatures of 31-35°C, arms reached temperatures of 33-39°C, inducing arm abscission. The absolute temperature of individual arms was a poor predictor of arm abscission, but the arms lost were consistently the hottest at the within-individual scale. Therefore, the vital region of this sea star may remain below the lethal threshold under extreme conditions, possibly through water movement from the arms to the central disc and/or evaporative cooling, but at the cost of increased risk of arm abscission. Initiation of arm abscission seems to reflect a whole-organism response while death occurs as a result of stress acting directly on central disc tissues.
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Regulación de la Temperatura Corporal , Estrellas de Mar/anatomía & histología , Estrellas de Mar/fisiología , Olas de Marea , Animales , Fenómenos Biomecánicos , California , Extremidades/anatomía & histología , Estrés Fisiológico , TemperaturaRESUMEN
The ways in which people conceptualize the human-nature relationship have significant implications for proenvironmental values and attitudes, sustainable behavior, and environmental policy measures. Human exceptionalism (HE) is one such conceptual framework, involving the belief that humans and human societies exist independently of the ecosystems in which they are embedded, promoting a sharp ontological boundary between humans and the rest of the natural world. In this paper, we introduce HE in more depth, exploring the impact of HE on perceptions of the human-nature relationship, the role of culture in HE, and speculating on the origins of HE. We consider potential implications for environmental decision-making, conservation and environmental science, and promoting proenvironmental behavior. We present empirical evidence on the pervasiveness and consequences of HE in WEIRD (Western, Educated, Industrialized, Rich and Democratic) populations, and potential interventions. Finally, we close with implications of human-exceptionalist thinking on other sustainability-related fields, including conservation practices, nature management, climate change adaptation, and environmental science. Understanding the cognitive and social drivers of this disconnect is vital on a planet now dominated by environmental change, as not only are humans increasingly impacted by natural disasters, but the choices they make can have ever more dire consequences for the sustainability of ecosystems.
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Cambio Climático , Ecosistema , Humanos , PensamientoRESUMEN
Biodiversity can promote ecosystem functioning in both terrestrial and marine environments, emphasizing the necessity of biodiversity conservation in order to preserve critical ecosystem functions and associated services. However, the role of biodiversity in buffering ecosystem functioning under extreme events caused by climate change remains a major scientific issue, especially for intertidal systems experiencing stressors from both terrestrial and marine drivers. We performed a regional-scale field experiment along the Italian coast to investigate the response of unmanipulated intertidal communities (by using a natural biodiversity gradient) to low tide aerial exposure to both ambient and short-term extreme temperatures. We specifically investigated the relationship between Biodiversity and Ecosystem Functioning (BEF) using different biodiversity indexes (species richness, functional diversity and evenness) and the response of the intertidal communities' ecosystem functioning (community respiration rates). Furthermore, we investigated which other environmental variables could influence the BEF relationship. We show that evenness explained a greater variation in intertidal community ecosystem functioning under both temperature conditions. Species richness (the most often used diversity metric in BEF research) was unrelated to ecosystem functioning, while functional diversity was significantly related to respiration under ambient but not extreme temperatures. We highlight the importance of the short-term thermal history of the communities (measured as body temperature) in the BEF relationship as it was consistently identified as the best predictor or response under both temperature conditions. However, Chlorophyll a in seawater and variation in sea surface temperature also contributed to the BEF relationship under ambient but not under extreme conditions, showing that short-duration climate-driven events can overcome local physiological adaptations. Our findings support the importance of the BEF relationship in intertidal communities, implying that systems with more diverse and homogeneous communities may be able to mitigate the effects of extreme temperatures.
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Ecosistema , Clorofila ARESUMEN
The ecological state of the Persian or Arabian Gulf (hereafter 'Gulf') is in sharp decline. Calls for comprehensive ecosystem-based management approaches and transboundary conservation have gone largely unanswered, despite mounting marine threats made worse by climate change. The region's long-standing political tensions add additional complexity, especially now as some Gulf countries will soon adopt ambitious goals to protect their marine environments as part of new global environmental commitments. The recent interest in global commitments comes at a time when diplomatic relations among all Gulf countries are improving. There is a window of opportunity for Gulf countries to meet global marine biodiversity conservation commitments, but only if scientists engage in peer-to-peer diplomacy to build trust, share knowledge and strategize marine conservation options across boundaries. The Gulf region needs more ocean diplomacy and coordination; just as critically, it needs actors at its science-policy interface to find better ways of adapting cooperative models to fit its unique marine environment, political context and culture. We propose a practical agenda for scientist-led diplomacy in the short term and lines of research from which to draw (e.g. co-production, knowledge exchange) to better design future science diplomacy practices and processes suited to the Gulf's setting.
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Climate warming experiments generally test the ecological effects of constant treatments while neglecting the influence of more realistic patterns of environmental fluctuations. Thus, little is known regarding how the temporal interaction between multiple episodes of thermal stress influences biotic interactions. We measured the sensitivity of predation rate in an intertidal sea star to changing levels of temporal coincidence of underwater and aerial thermal stress events. In laboratory trials, we controlled for intensity, variance and temporal patterning of both underwater and aerial body temperature. Predation rate decreased as underwater and aerial thermal stress episodes became temporally non-coincident, despite a similar intensity and variance among treatments. Experiments under constant conditions were a poor predictor of more complex environmental scenarios because of these strong temporal interactions. Such temporal interactions may be widespread in various ecosystems, suggesting a strong need for empirical studies and models that link environmental complexity, physiology, behaviour and species interactions.
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Calor , Mytilus , Conducta Predatoria , Estrellas de Mar , Estrés Fisiológico , Animales , Temperatura Corporal , California , Cambio Climático , Ecosistema , Conducta Alimentaria , Modelos EstadísticosRESUMEN
The emerging field of mechanistic niche modelling aims to link the functional traits of organisms to their environments to predict survival, reproduction, distribution and abundance. This approach has great potential to increase our understanding of the impacts of environmental change on individuals, populations and communities by providing functional connections between physiological and ecological response to increasingly available spatial environmental data. By their nature, such mechanistic models are more data intensive in comparison with the more widely applied correlative approaches but can potentially provide more spatially and temporally explicit predictions, which are often needed by decision makers. A poorly explored issue in this context is the appropriate level of temporal resolution of input data required for these models, and specifically the error in predictions that can be incurred through the use of temporally averaged data. Here, we review how biomechanical principles from heat-transfer and metabolic theory are currently being used as foundations for mechanistic niche models and consider the consequences of different temporal resolutions of environmental data for modelling the niche of a behaviourally thermoregulating terrestrial lizard. We show that fine-scale temporal resolution (daily) data can be crucial for unbiased inference of climatic impacts on survival, growth and reproduction. This is especially so for species with little capacity for behavioural buffering, because of behavioural or habitat constraints, and for detecting temporal trends. However, coarser-resolution data (long-term monthly averages) can be appropriate for mechanistic studies of climatic constraints on distribution and abundance limits in thermoregulating species at broad spatial scales.
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Fenómenos Ecológicos y Ambientales , Lagartos/fisiología , Animales , Fenómenos Biomecánicos/fisiología , Regulación de la Temperatura Corporal/fisiología , Simulación por Computador , Metabolismo Energético/fisiología , Modelos Biológicos , Análisis de Regresión , Factores de TiempoRESUMEN
Understanding the effects of climate-mediated environmental variation on the distribution of organisms is critically important in an era of global change. We used wavelet analysis to quantify the spatiotemporal (co)variation in daily water temperature for predicting the distribution of cryptic refugia across 16 intertidal sites that were characterized as 'no', 'weak' or 'strong' upwelling and spanned 2000 km of the European Atlantic Coast. Sites experiencing weak upwelling exhibited high synchrony in temperature but low levels of co-variability at monthly to weekly timescales, whereas the opposite was true for sites experiencing strong upwelling. This suggests upwelling generates temporal thermal refugia that can promote organismal performance by both supplying colder water that mitigates thermal stress during hot Summer months and ensuring high levels of fine-scale variation in temperature that reduce the duration of thermal extremes. Additionally, pairwise correlograms based on the Pearson-product moment correlation coefficient and wavelet coherence revealed scale dependent trends in temperature fluctuations across space, with a rapid decay in strong upwelling sites at monthly and weekly timescales. This suggests upwelling also generates spatial thermal refugia that can 'rescue' populations from unfavorable conditions at local and regional scales. Overall, this study highlights the importance of identifying cryptic spatiotemporal refugia that emerge from fine-scale environmental variation to map potential patterns of organismal performance in a rapidly changing world.
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Clima , Refugio de Fauna , Temperatura , Estaciones del Año , Agua , EcosistemaRESUMEN
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.
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Cambio Climático , Ecosistema , Modelos Teóricos , Adaptación Fisiológica , Animales , Monitoreo del Ambiente , Océanos y Mares , Dinámica Poblacional , Temperatura , Factores de TiempoRESUMEN
Predicting when, where and with what magnitude climate change is likely to affect the fitness, abundance and distribution of organisms and the functioning of ecosystems has emerged as a high priority for scientists and resource managers. However, even in cases where we have detailed knowledge of current species' range boundaries, we often do not understand what, if any, aspects of weather and climate act to set these limits. This shortcoming significantly curtails our capacity to predict potential future range shifts in response to climate change, especially since the factors that set range boundaries under those novel conditions may be different from those that set limits today. We quantitatively examine a nine-year time series of temperature records relevant to the body temperatures of intertidal mussels as measured using biomimetic sensors. Specifically, we explore how a 'climatology' of body temperatures, as opposed to long-term records of habitat-level parameters such as air and water temperatures, can be used to extrapolate meaningful spatial and temporal patterns of physiological stress. Using different metrics that correspond to various aspects of physiological stress (seasonal means, cumulative temperature and the return time of extremes) we show that these potential environmental stressors do not always occur in synchrony with one another. Our analysis also shows that patterns of animal temperature are not well correlated with simple, commonly used metrics such as air temperature. Detailed physiological studies can provide guidance to predicting the effects of global climate change on natural ecosystems but only if we concomitantly record, archive and model environmental signals at appropriate scales.
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Cambio Climático , Ambiente , Meteorología , Estrés Fisiológico , Animales , Temperatura Corporal , Clima , Humanos , Estaciones del Año , Transducción de Señal/fisiologíaRESUMEN
Coral reefs are under increasingly severe threat from climate change and other anthropogenic stressors. Anomalously high seawater temperatures in particular are known to cause coral bleaching (loss of algal symbionts in the family Symbiodiniaceae), which frequently leads to coral mortality. Remote sensing of sea surface temperature (SST) has served as an invaluable tool for monitoring physical conditions that can lead to bleaching events over relatively large scales (e.g. few kms to 100 s of kms). But, it is also well known that seawater temperatures within a site can vary significantly across depths due to the combined influence of solar heating of surface waters, water column thermal stratification, and cooling from internal waves and upwelling. We deployed small autonomous benthic temperature sensors at depths ranging from 0-40 m in fore reef, back reef, and lagoonal reef habitats on the Belize Mesoamerican Barrier Reef System from 2000-2019. These data can be used to calculate depth-specific climatologies across reef depths and sites, and emphasize the dynamic and spatially-variable nature of coral reef physical environments.