Physiologically informed organismal climatologies reveal unexpected spatiotemporal trends in temperature.

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.

Expanding ocean protection and peace: a window for science diplomacy in the Gulf.

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.

Conceptualizing Human-Nature Relationships: Implications of Human Exceptionalist Thinking for Sustainability and Conservation.

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.

Evenness, biodiversity, and ecosystem function of intertidal communities along the Italian coasts: Experimental short-term response to ambient and extreme air temperatures.

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.

Coastal upwelling generates cryptic temperature refugia.

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.

Physiological determinants of biogeography: The importance of metabolic depression to heat tolerance.

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.

High resolution spatiotemporal patterns of seawater temperatures across the Belize Mesoamerican Barrier Reef.

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.

Mapping physiology: biophysical mechanisms define scales of climate change impacts.

The rocky intertidal zone is a highly dynamic and thermally variable ecosystem, where the combined influences of solar radiation, air temperature and topography can lead to differences greater than 15°C over the scale of centimetres during aerial exposure at low tide. For most intertidal organisms this small-scale heterogeneity in microclimates can have enormous influences on survival and physiological performance. However, the potential ecological importance of environmental heterogeneity in determining ecological responses to climate change remains poorly understood. We present a novel framework for generating spatially explicit models of microclimate heterogeneity and patterns of thermal physiology among interacting organisms. We used drone photogrammetry to create a topographic map (digital elevation model) at a resolution of 2 × 2 cm from an intertidal site in Massachusetts, which was then fed into to a model of incident solar radiation based on sky view factor and solar position. These data were in turn used to drive a heat budget model that estimated hourly surface temperatures over the course of a year (2017). Body temperature layers were then converted to thermal performance layers for organisms, using thermal performance curves, creating 'physiological landscapes' that display spatially and temporally explicit patterns of 'microrefugia'. Our framework shows how non-linear interactions between these layers lead to predictions about organismal performance and survivorship that are distinct from those made using any individual layer (e.g. topography, temperature) alone. We propose a new metric for quantifying the 'thermal roughness' of a site (RqT, the root mean square of spatial deviations in temperature), which can be used to quantify spatial and temporal variability in temperature and performance at the site level. These methods facilitate an exploration of the role of micro-topographic variability in driving organismal vulnerability to environmental change using both spatially explicit and frequency-based approaches.

Pido: Predictive Delay Optimization for Intertidal Wireless Sensor Networks.

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.

The duality of ocean acidification as a resource and a stressor.

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.

Conceptualizing ecosystem tipping points within a physiological framework.

Connecting the nonlinear and often counterintuitive physiological effects of multiple environmental drivers to the emergent impacts on ecosystems is a fundamental challenge. Unfortunately, the disconnect between the way "stressors" (e.g., warming) is considered in organismal (physiological) and ecological (community) contexts continues to hamper progress. Environmental drivers typically elicit biphasic physiological responses, where performance declines at levels above and below some optimum. It is also well understood that species exhibit highly variable response surfaces to these changes so that the optimum level of any environmental driver can vary among interacting species. Thus, species interactions are unlikely to go unaltered under environmental change. However, while these nonlinear, species-specific physiological relationships between environment and performance appear to be general, rarely are they incorporated into predictions of ecological tipping points. Instead, most ecosystem-level studies focus on varying levels of "stress" and frequently assume that any deviation from "normal" environmental conditions has similar effects, albeit with different magnitudes, on all of the species within a community. We consider a framework that realigns the positive and negative physiological effects of changes in climatic and nonclimatic drivers with indirect ecological responses. Using a series of simple models based on direct physiological responses to temperature and ocean pCO 2, we explore how variation in environment-performance relationships among primary producers and consumers translates into community-level effects via trophic interactions. These models show that even in the absence of direct mortality, mismatched responses resulting from often subtle changes in the physical environment can lead to substantial ecosystem-level change.

Untangling the roles of microclimate, behaviour and physiological polymorphism in governing vulnerability of intertidal snails to heat stress.

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.

How ocean acidification can benefit calcifiers.

Reduction in seawater pH due to rising levels of anthropogenic carbon dioxide (CO2) in the world's oceans is a major force set to shape the future of marine ecosystems and the ecological services they provide [1,2]. In particular, ocean acidification is predicted to have a detrimental effect on the physiology of calcifying organisms [3]. Yet, the indirect effects of ocean acidification on calcifying organisms, which may counter or exacerbate direct effects, is uncertain. Using volcanic CO2 vents, we tested the indirect effects of ocean acidification on a calcifying herbivore (gastropod) within the natural complexity of an ecological system. Contrary to predictions, the abundance of this calcifier was greater at vent sites (with near-future CO2 levels). Furthermore, translocation experiments demonstrated that ocean acidification did not drive increases in gastropod abundance directly, but indirectly as a function of increased habitat and food (algal biomass). We conclude that the effect of ocean acidification on algae (primary producers) can have a strong, indirect positive influence on the abundance of some calcifying herbivores, which can overwhelm any direct negative effects. This finding points to the need to understand ecological processes that buffer the negative effects of environmental change.

Nutrients influence the thermal ecophysiology of an intertidal macroalga: multiple stressors or multiple drivers?

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.

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.

Physiologically grounded metrics of model skill: a case study estimating heat stress in intertidal populations.

Models of ecological responses to climate change fundamentally assume that predictor variables, which are often measured at large scales, are to some degree diagnostic of the smaller-scale biological processes that ultimately drive patterns of abundance and distribution. Given that organisms respond physiologically to stressors, such as temperature, in highly non-linear ways, small modelling errors in predictor variables can potentially result in failures to predict mortality or severe stress, especially if an organism exists near its physiological limits. As a result, a central challenge facing ecologists, particularly those attempting to forecast future responses to environmental change, is how to develop metrics of forecast model skill (the ability of a model to predict defined events) that are biologically meaningful and reflective of underlying processes. We quantified the skill of four simple models of body temperature (a primary determinant of physiological stress) of an intertidal mussel, Mytilus californianus, using common metrics of model performance, such as root mean square error, as well as forecast verification skill scores developed by the meteorological community. We used a physiologically grounded framework to assess each model's ability to predict optimal, sub-optimal, sub-lethal and lethal physiological responses. Models diverged in their ability to predict different levels of physiological stress when evaluated using skill scores, even though common metrics, such as root mean square error, indicated similar accuracy overall. Results from this study emphasize the importance of grounding assessments of model skill in the context of an organism's physiology and, especially, of considering the implications of false-positive and false-negative errors when forecasting the ecological effects of environmental change.

Can we predict ectotherm responses to climate change using thermal performance curves and body temperatures?

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.

Interacting environmental mosaics drive geographic variation in mussel performance and predation vulnerability.

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.

Thermal tolerance and climate warming sensitivity in tropical snails.

Tropical ectotherms are predicted to be especially vulnerable to climate change because their thermal tolerance limits generally lie close to current maximum air temperatures. This prediction derives primarily from studies on insects and lizards and remains untested for other taxa with contrasting ecologies. We studied the HCT (heat coma temperatures) and ULT (upper lethal temperatures) of 40 species of tropical eulittoral snails (Littorinidae and Neritidae) inhabiting exposed rocky shores and shaded mangrove forests in Oceania, Africa, Asia and North America. We also estimated extremes in animal body temperature at each site using a simple heat budget model and historical (20 years) air temperature and solar radiation data. Phylogenetic analyses suggest that HCT and ULT exhibit limited adaptive variation across habitats (mangroves vs. rocky shores) or geographic locations despite their contrasting thermal regimes. Instead, the elevated heat tolerance of these species (HCT = 44.5 ± 1.8°C and ULT = 52.1 ± 2.2°C) seems to reflect the extreme temperature variability of intertidal systems. Sensitivity to climate warming, which was quantified as the difference between HCT or ULT and maximum body temperature, differed greatly between snails from sunny (rocky shore; Thermal Safety Margin, TSM = -14.8 ± 3.3°C and -6.2 ± 4.4°C for HCT and ULT, respectively) and shaded (mangrove) habitats (TSM = 5.1 ± 3.6°C and 12.5 ± 3.6°C). Negative TSMs in rocky shore animals suggest that mortality is likely ameliorated during extreme climatic events by behavioral thermoregulation. Given the low variability in heat tolerance across species, habitat and geographic location account for most of the variation in TSM and may adequately predict the vulnerability to climate change. These findings caution against generalizations on the impact of global warming across ectothermic taxa and highlight how the consideration of nonmodel animals, ecological transitions, and behavioral responses may alter predictions of studies that ignore these biological details.