Life on the edge: thermal optima for aerobic scope of equatorial reef fishes are close to current day temperatures

Equatorial populations of marine species are predicted to be most impacted by global warming because they could be adapted to a narrow range of temperatures in their local environment. We investigated the thermal range at which aerobic metabolic performance is optimum in equatorial populations of coral reef fish in northern Papua New Guinea. Four species of damselfishes and two species of cardinal fishes were held for 14 days at 29, 31, 33, and 34 °C, which incorporated their existing thermal range (29–31 °C) as well as projected increases in ocean surface temperatures of up to 3 °C by the end of this century. Resting and maximum oxygen consumption rates were measured for each species at each temperature and used to calculate the thermal reaction norm of aerobic scope. Our results indicate that one of the six species, Chromis atripectoralis, is already living above its thermal optimum of 29 °C. The other five species appeared to be living close to their thermal optima (ca. 31 °C). Aerobic scope was significantly reduced in all species, and approached zero for two species at 3 °C above current‐day temperatures. One species was unable to survive even short‐term exposure to 34 °C. Our results indicate that low‐latitude reef fish populations are living close to their thermal optima and may be more sensitive to ocean warming than higher‐latitude populations. Even relatively small temperature increases (2–3 °C) could result in population declines and potentially redistribution of equatorial species to higher latitudes if adaptation cannot keep pace.     

Large but uneven reduction in fish size across species in relation to changing sea temperatures

Ectotherms often attain smaller body sizes when they develop at higher temperatures. This phenomenon, known as the temperature–size rule, has important consequences for global fisheries, whereby ocean warming is predicted to result in smaller fish and reduced biomass. However, the generality of this phenomenon and the mechanisms that drive it in natural populations remain unresolved. In this study, we document the maximal size of 74 fish species along a steep temperature gradient in the Mediterranean Sea and find strong support for the temperature–size rule. Importantly, we additionally find that size reduction in active fish species is dramatically larger than for more sedentary species. As the temperature dependence of oxygen consumption depends on activity levels, these findings are consistent with the hypothesis that oxygen is a limiting factor shaping the temperature–size rule in fishes. These results suggest that ocean warming will result in a sharp, but uneven, reduction in fish size that will cause major shifts in size‐dependent interactions. Moreover, warming will have major implications for fisheries as the main species targeted for harvesting will show the most substantial declines in biomass.     

Warming temperatures and smaller body sizes: synchronous changes in growth of North Sea fishes

Decreasing body size has been proposed as a universal response to increasing temperatures. The physiology behind the response is well established for ectotherms inhabiting aquatic environments: as higher temperatures decrease the aerobic capacity, individuals with smaller body sizes have a reduced risk of oxygen deprivation. However, empirical evidence of this response at the scale of communities and ecosystems is lacking for marine fish species. Here, we show that over a 40‐year period six of eight commercial fish species in the North Sea examined underwent concomitant reductions in asymptotic body size with the synchronous component of the total variability coinciding with a 1–2 °C increase in water temperature. Smaller body sizes decreased the yield‐per‐recruit of these stocks by an average of 23%. Although it is not possible to ascribe these phenotypic changes unequivocally to temperature, four aspects support this interpretation: (i) the synchronous trend was detected across species varying in their life history and life style; (ii) the decrease coincided with the period of increasing temperature; (iii) the direction of the phenotypic change is consistent with physiological knowledge; and (iv) no cross‐species synchrony was detected in other species‐specific factors potentially impacting growth. Our findings support a recent model‐derived prediction that fish size will shrink in response to climate‐induced changes in temperature and oxygen. The smaller body sizes being projected for the future are already detectable in the North Sea.     

Climate change alters stability and species potential interactions in a large marine ecosystem

We have little empirical evidence of how large‐scale overlaps between large numbers of marine species may have altered in response to human impacts. Here, we synthesized all available distribution data (>1 million records) since 1992 for 61 species of the East Australian marine ecosystem, a global hot spot of ocean warming and continuing fisheries exploitation. Using a novel approach, we constructed networks of the annual changes in geographical overlaps between species. Using indices of changes in species overlap, we quantified changes in the ecosystem stability, species robustness, species sensitivity and structural keystone species. We then compared the species overlap indices with environmental and fisheries data to identify potential factors leading to the changes in distributional overlaps between species. We found that the structure of the ecosystem has changed with a decrease in asymmetrical geographical overlaps between species. This suggests that the ecosystem has become less stable and potentially more susceptible to environmental perturbations. Most species have shown a decrease in overlaps with other species. The greatest decrease in species overlap robustness and sensitivity to the loss of other species has occurred in the pelagic community. Some demersal species have become more robust and less sensitive. Pelagic structural keystone species, predominately the tunas and billfish, have been replaced by demersal fish species. The changes in species overlap were strongly correlated with regional oceanographic changes, in particular increasing ocean warming and the southward transport of warmer and saltier water with the East Australian Current, but less correlated with fisheries catch. Our study illustrates how large‐scale multispecies distribution changes can help identify structural changes in marine ecosystems associated with climate change.     

Climate effects on fish body size–trophic position relationship depend on ecosystem type

The energetic demand of consumers increases with body size and temperature. This implies that energetic constraints may limit the trophic position of larger consumers, which is expected to be lower in tropical than in temperate regions to compensate for energy limitation. Using a global dataset of 3635 marine and freshwater ray‐finned fish species, we addressed if and how climate affects the fish body size–trophic position relationship in both freshwater and marine ecosystems, while controlling for the effects of taxonomic affiliation. We observed significant fish body size–trophic position relationships for different ecosystems. However, only in freshwater systems larger tropical fish presented a significantly lower trophic position than their temperate counterparts. Climate did not affect the fish body size–trophic position relationship in marine systems. Our results suggest that larger tropical freshwater fish may compensate for higher energetic constraints feeding at lower trophic positions, compared to their temperate counterparts of similar body size. The lower latitudinal temperature range in marine ecosystems and/or their larger ecosystem size may attenuate and/or compensate for the energy limitation of larger marine fish. Based on our results, temperature may determine macroecological patterns of aquatic food webs, but its effect is contingent on ecosystem type. We suggest that freshwater ecosystems may be more sensitive to warming‐induced alterations in food web topology and food chain length than marine ecosystems.     

Designing connected marine reserves in the face of global warming

Marine reserves are widely used to protect species important for conservation and fisheries and to help maintain ecological processes that sustain their populations, including recruitment and dispersal. Achieving these goals requires well‐connected networks of marine reserves that maximize larval connectivity, thus allowing exchanges between populations and recolonization after local disturbances. However, global warming can disrupt connectivity by shortening potential dispersal pathways through changes in larval physiology. These changes can compromise the performance of marine reserve networks, thus requiring adjusting their design to account for ocean warming. To date, empirical approaches to marine prioritization have not considered larval connectivity as affected by global warming. Here, we develop a framework for designing marine reserve networks that integrates graph theory and changes in larval connectivity due to potential reductions in planktonic larval duration (PLD) associated with ocean warming, given current socioeconomic constraints. Using the Gulf of California as case study, we assess the benefits and costs of adjusting networks to account for connectivity, with and without ocean warming. We compare reserve networks designed to achieve representation of species and ecosystems with networks designed to also maximize connectivity under current and future ocean‐warming scenarios. Our results indicate that current larval connectivity could be reduced significantly under ocean warming because of shortened PLDs. Given the potential changes in connectivity, we show that our graph‐theoretical approach based on centrality (eigenvector and distance‐weighted fragmentation) of habitat patches can help design better‐connected marine reserve networks for the future with equivalent costs. We found that maintaining dispersal connectivity incidentally through representation‐only reserve design is unlikely, particularly in regions with strong asymmetric patterns of dispersal connectivity. Our results support previous studies suggesting that, given potential reductions in PLD due to ocean warming, future marine reserve networks would require more and/or larger reserves in closer proximity to maintain larval connectivity.     

CO2‐metabolism in early tetrapods revisited: inferences from osteological correlates of gills,skin and lung ventilation in the fossil record

One of the most important physiological changes during the conquest of land by vertebrates was the increasing reliance on lung breathing, with the concomitant decrease in importance of gill breathing. The main problem involved here was to cope with the excessive accumulation of CO₂ in the body and to avoid respiratory acidosis. In the past, several often mutually contradicting hypotheses of CO₂‐elimination via skin, lungs and gills in early tetrapods have been proposed, based on theoretical physiological considerations and comparison with extant air‐breathing fishes and amphibians. This study proposes a revised scenario of CO₂‐elimination in early tetrapods based on fossil evidence, that is recently identified osteological correlates of gills, skin structure and mode of lung ventilation. In stem tetrapods of the Devonian and Carboniferous, O₂‐uptake via the lungs by buccal pumping was decoupled from CO₂‐release via internal gills, and the rather gas‐impermeable skin played a minor role in gaseous exchange. The two main lineages of crown‐group tetrapods, the amphibian and amniote lineage, used different strategies of CO₂‐elimination. As in stem tetrapods, O₂‐uptake and CO₂‐release remained always largely decoupled in temnospondyls, which ventilated their lungs via buccal pumping and relied mainly on their internal gills for CO₂‐release. Temnospondyls were not able to reduce their internal gills before their skin became more gas permeable and their body size was reduced, to shift from internal gills to the skin as the major site of CO₂‐elimination, a pattern that is retained in most lissamphibians. In contrast, internal gills were lost very early in stem amniote evolution. This was associated with the evolution of the more effective aspiration pump that allowed the elimination of the bulk of CO₂ via the lungs, leading to a coupled O₂‐uptake and CO₂‐loss in stem amniotes and later in amniotes.     

Thermal growth potential of Atlantic cod by the end of the 21st century

Ocean warming may lead to smaller body sizes of marine ectotherms, because metabolic rates increase exponentially with temperature while the capacity of the cardiorespiratory system to match enhanced oxygen demands is limited. Here, we explore the impact of rising sea water temperatures on Atlantic cod (Gadus morhua), an economically important fish species. We focus on changes in the temperature‐dependent growth potential by a transfer function model combining growth observations with climate model ensemble temperatures. Growth potential is expressed in terms of asymptotic body weight and depends on water temperature. We consider changes between the periods 1985–2004 and 2081–2100, assuming that future sea water temperatures will evolve according to climate projections for IPCC AR5 scenario RCP8.5. Our model projects a response of Atlantic cod to future warming, differentiated according to ocean regions, leading to increases of asymptotic weight in the Barents Sea, while weights are projected to decline at the southern margin of the biogeographic range. Southern spawning areas will disappear due to thermal limitation of spawning stages. These projections match the currently observed biogeographic shifts and the temperature‐ and oxygen‐dependent decline in routine aerobic scope at southern distribution limits.     

Effects of river temperature and climate warming on stock‐specific survival of adult migrating Fraser River sockeye salmon (Oncorhynchus nerka)

Mean summer water temperatures in the Fraser River (British Columbia, Canada) have increased by ～1.5 °C since the 1950s. In recent years, record high river temperatures during spawning migrations of Fraser River sockeye salmon (Oncorhynchus nerka) have been associated with high mortality events, raising concerns about long‐term viability of the numerous natal stocks faced with climate warming. In this study, the effect of freshwater thermal experience on spawning migration survival was estimated by fitting capture–recapture models to telemetry data collected for 1474 adults (captured in either the ocean or river between 2002 and 2007) from four Fraser River sockeye salmon stock‐aggregates (Chilko, Quesnel, Stellako‐Late Stuart and Adams). Survival of Adams sockeye salmon was the most impacted by warm temperatures encountered in the lower river, followed by that of Stellako‐Late Stuart and Quesnel. In contrast, survival of Chilko fish was insensitive to the encountered river temperature. In all stocks, in‐river survival of ocean‐captured sockeye salmon was higher than that of river‐captured fish and, generally, the difference was more pronounced under warm temperatures. The survival–temperature relationships for ocean‐captured fish were used to predict historic (1961–1990) and future (2010–2099) survival under simulated lower river thermal experiences for the Quesnel, Stellako‐Late Stuart and Adams stocks. A decrease of 9–16% in survival of all these stocks was predicted by the end of the century if the Fraser River continues to warm as expected. However, the decrease in future survival of Adams sockeye salmon would occur only if fish continue to enter the river abnormally early, towards warmer periods of the summer, as they have done since 1995. The survival estimates and predictions presented here are likely optimistic and emphasize the need to consider stock‐specific responses to temperature and climate warming into fisheries management and conservation strategies.     

Navigating the complexity of ecological stability

Human actions challenge nature in many ways. Ecological responses are ineluctably complex, demanding measures that describe them succinctly. Collectively, these measures encapsulate the overall ‘stability’ of the system. Many international bodies, including the Intergovernmental Science‐Policy Platform on Biodiversity and Ecosystem Services, broadly aspire to maintain or enhance ecological stability. Such bodies frequently use terms pertaining to stability that lack clear definition. Consequently, we cannot measure them and so they disconnect from a large body of theoretical and empirical understanding. We assess the scientific and policy literature and show that this disconnect is one consequence of an inconsistent and one‐dimensional approach that ecologists have taken to both disturbances and stability. This has led to confused communication of the nature of stability and the level of our insight into it. Disturbances and stability are multidimensional. Our understanding of them is not. We have a remarkably poor understanding of the impacts on stability of the characteristics that define many, perhaps all, of the most important elements of global change. We provide recommendations for theoreticians, empiricists and policymakers on how to better integrate the multidimensional nature of ecological stability into their research, policies and actions.     

Development of the Gill System in Early Ontogenesis of the Zebrafish and Ninespine Stickleback

We studied specific features of development of the gill system during ontogenesis of the zebrafish Danio rerio and ninespine stickleback Pungitius pungitius, which differ in the rates of gill system, development. Although the development of sticklebacks proceeds in nature at lower temperatures than for zebrafish, the rate of gill formation in the former is higher. These differences are related to the specific conditions in which these fish develop: embryonic and larval development of the stickleback proceeds in bodies of water with a lower oxygen content than for zebrafish, and this results in the adaptive alteration of the rate of gill system development. Differentiation of gills in the zebrafish is accompanied by a manifold increase in the oxygen consumption rate. At different developmental stages, the incremental rates of oxygen consumption and increase in the body mass of the zebrafish larvae and fry differed significantly.     

Temperature‐dependent body size effects determine population responses to climate warming

Current understanding of animal population responses to rising temperatures is based on the assumption that biological rates such as metabolism, which governs fundamental ecological processes, scale independently with body size and temperature, despite empirical evidence for interactive effects. Here, we investigate the consequences of interactive temperature‐ and size scaling of vital rates for the dynamics of populations experiencing warming using a stage‐structured consumer‐resource model. We show that interactive scaling alters population and stage‐specific responses to rising temperatures, such that warming can induce shifts in population regulation and stage‐structure, influence community structure and govern population responses to mortality. Analysing experimental data for 20 fish species, we found size–temperature interactions in intraspecific scaling of metabolic rate to be common. Given the evidence for size–temperature interactions and the ubiquity of size structure in animal populations, we argue that accounting for size‐specific temperature effects is pivotal for understanding how warming affects animal populations and communities.     

鱼类对海洋升温与酸化的响应

自工业革命以来,空气中人为排放CO₂量增加,引起温室效应,导致地球表面温度升高和海水升温;同时,由于海-气界面气体交换,大气中CO₂部分溶解于海洋,引起海洋酸化。海洋升温加快鱼体内生化反应和代谢速率,并通过影响生长、觅食和繁殖等生命过程中能量供给,间接影响到鱼类种群分布、群落结构及生态系统的功能。而海水酸化会干扰海洋鱼类仔稚鱼的感觉和行为,增加其被捕食率,并削弱其野外生存能力,可能威胁自然种群补给量。综述了海洋升温、海洋酸化及其两者共同作用对海洋鱼类的影响,为预测鱼类响应全球海洋环境变化的响应趋势提供相关依据。     

Development of the gill system in early ontogenesis of Danio and nine spike stickleback

We studied specific features of development of the gill system during ontogenesis of the zebrafish Danio rerio and ninespine stickleback Pungitius pungitius, which differ in the rates of gill system, development. Although the development of sticklebacks proceeds in nature at lower temperatures than for zebrafish, the rate of gill formation in the former is higher. These differences are related to the specific conditions in which these fish develop: embryonic and larval development of the stickleback proceeds in bodies of water with a lower oxygen content than for zebrafish, and this results in the adaptive alteration of the rate of gill system development. Differentiation of gills in the zebrafish is accompanied by a manifold increase in the oxygen consumption rate. At different developmental stages, the incremental rates of oxygen consumption and increase in the body mass of the zebrafish larvae and fry differed significantly.     

The mid-domain effect cannot explain the diversity gradient of Nearctic birds

A recent explanation for diversity gradients proposes a ‘null model’ based on how species ranges are constrained by the geometry of bounded domains. We conduct a test of this hypothesis by comparing patterns predicted by two two‐dimensional geometric models against observed diversity patterns for terrestrially feeding Nearctic birds. Consistent with previous tests in two‐dimensional space, we find empirical support for the hypothesis to be very weak. We also point out a fundamental conceptual flaw in the hypothesis with respect to the key assumption that ranges can exist independently of the environment in which they are embedded that undermines its theoretical basis as well. We conclude that the mid‐domain effect has little empirical support and no theoretical support for its existence, and recommend that it be eliminated as a potential explanation for diversity gradients.     

Bystrow’s Paradox – gills,fossils, and the fish‐to‐tetrapod transition

Schoch, R.R. and Witzmann, F. 2011. Bystrow’s Paradox – gills, fossils, and the fish‐to‐tetrapod transition. —Acta Zoologica (Stockholm) 92 : 251–265. The issue of which breathing mechanism was used by the earliest tetrapods is still unsolved. Recent discoveries of stem tetrapods suggest the presence of internal gills and fish‐like underwater breathing. The same osteological features were used by Bystrow to infer a salamander‐like breathing through external gills in temnospondyl amphibians. This apparent contradiction – here called Bystrow’s Paradox – is resolved by reviewing the primary fossil evidence and the anatomy of the two gill types in extant taxa. Rather unexpectedly, we find that internal gills were present in a range of early crown tetrapods (temnospondyls), based on the anatomy of gill lamellae and location of branchial arteries on the ventral side of gill arch elements (ceratobranchials). Although it remains to be clarified which components are homologous in external and internal gills, both gill types are likely to have been present in Palaeozoic tetrapods – internal gills in aquatic adults of some taxa, and external gills in the larvae of these taxa and in larvae of numerous forms with terrestrial adults, which resorbed the external gills after the larval phase. Future developmental studies will hopefully clarify which mechanistic pathways are involved in gill formation and how these might have evolved.     

Adapt,move or die – how will tropical coral reef fishes cope with ocean warming?

Previous studies hailed thermal tolerance and the capacity for organisms to acclimate and adapt as the primary pathways for species survival under climate change. Here we challenge this theory. Over the past decade, more than 365 tropical stenothermal fish species have been documented moving poleward, away from ocean warming hotspots where temperatures 2–3 °C above long‐term annual means can compromise critical physiological processes. We examined the capacity of a model species – a thermally sensitive coral reef fish, Chromis viridis (Pomacentridae) – to use preference behaviour to regulate its body temperature. Movement could potentially circumvent the physiological stress response associated with elevated temperatures and may be a strategy relied upon before genetic adaptation can be effectuated. Individuals were maintained at one of six temperatures (23, 25, 27, 29, 31 and 33 °C) for at least 6 weeks. We compared the relative importance of acclimation temperature to changes in upper critical thermal limits, aerobic metabolic scope and thermal preference. While acclimation temperature positively affected the upper critical thermal limit, neither aerobic metabolic scope nor thermal preference exhibited such plasticity. Importantly, when given the choice to stay in a habitat reflecting their acclimation temperatures or relocate, fish acclimated to end‐of‐century predicted temperatures (i.e. 31 or 33 °C) preferentially sought out cooler temperatures, those equivalent to long‐term summer averages in their natural habitats (~29 °C). This was also the temperature providing the greatest aerobic metabolic scope and body condition across all treatments. Consequently, acclimation can confer plasticity in some performance traits, but may be an unreliable indicator of the ultimate survival and distribution of mobile stenothermal species under global warming. Conversely, thermal preference can arise long before, and remain long after, the harmful effects of elevated ocean temperatures take hold and may be the primary driver of the escalating poleward migration of species.     

Are fish in hot water? Effects of warming on oxidative stress metabolism in the commercial species Sparus aurata

Climate change is disturbing marine biological processes, and impacting goods and services provided to society. Physiological studies are a major contributor to the improvement of biological forecasting in the context of climate change. Oxidative stress biomarkers are useful tools to assess the metabolic status and health of organisms, improving management of wild and cultured populations. The aims of this study were to assess the health status and vulnerability of Sparus aurata juveniles toward ocean warming and heat wave events by (1) exposing fish to a thermal ramp from 18 °C until their Critical Thermal Maximum (≈35 °C) and (2) quantifying oxidative stress biomarkers in several organs, i.e. lipid peroxidation (LPO), catalase (CAT), superoxide dismutase (SOD), glutathione-S-transferase (GST), and cytochrome CYP1A. Fish showed signs of oxidative stress in every tissue tested (gills, muscle, liver, brain and intestine), the most affected being muscle and liver, which showed greater increases in LPO. In general, antioxidant enzymes increased their activity: CAT increased in every organ tested, GST increased in every organ except brain (no change) and SOD increased in every organ except intestine (no change) and brain (decrease, probably due to enzyme denaturation). Muscle showed the greatest stress response with a massive increase in GST. Hepatic CYP1A decreased upon warming suggesting that temperature influences detoxifying mechanisms and may affect fish health. These results are significant in the context of climate change and associated impacts on fisheries and aquaculture because over-induction of oxidative stress due to warming can induce health problems, mortality and shortened lifespan.     

The effects of changing climate on faunal depth distributions determine winners and losers

Changing climate is predicted to impact all depths of the global oceans, yet projections of range shifts in marine faunal distributions in response to changing climate seldom evaluate potential shifts in depth distribution. Marine ectotherms' thermal tolerance is limited by their ability to maintain aerobic metabolism (oxygen‐ and capacity‐limited tolerance), and is functionally associated with their hypoxia tolerance. Shallow‐water (<200 m depth) marine invertebrates and fishes demonstrate limited tolerance of increasing hydrostatic pressure (pressure exerted by the overlying mass of water), and hyperbaric (increased pressure) tolerance is proposed to depend on the ability to maintain aerobic metabolism, too. Here, we report significant correlation between the hypoxia thresholds and the hyperbaric thresholds of taxonomic groups of shallow‐water fauna, suggesting that pressure tolerance is indeed oxygen limited. Consequently, it appears that the combined effects of temperature, pressure and oxygen concentration constrain the fundamental ecological niches (FENs) of marine invertebrates and fishes. Including depth in a conceptual model of oxygen‐ and capacity‐limited FENs' responses to ocean warming and deoxygenation confirms previous predictions made based solely on consideration of the latitudinal effects of ocean warming (e.g. Cheung et al., 2009), that polar taxa are most vulnerable to the effects of climate change, with Arctic fauna experiencing the greatest FEN contraction. In contrast, the inclusion of depth in the conceptual model reveals for the first time that temperate fauna as well as tropical fauna may experience substantial FEN expansion with ocean warming and deoxygenation, rather than FEN maintenance or contraction suggested by solely considering latitudinal range shifts.     

Macro-zooplankter responses to simulated climate warming in experimental freshwater microcosms

1. We report data collected from 48 replicated microcosm communities created to mimic plant‐dominated shallow lake and pond environments. Over a 2‐year period, the microcosms were subjected to warming treatments (continuous 3 °C above ambient and 3 °C above ambient during summer only), a nutrient addition treatment and the presence or absence of fish. We tracked macro‐zooplankter dynamics, censusing cladoceran populations at the species level, copepods at the order level and ostracods as a class. 2. Responses to warming were subtle. Cladoceran diversity and overall abundance were not significantly affected by warming, although measures of community evenness increased. Warming effects on patterns of population trajectories tended to be strongly seasonal and most apparent during periods of pronounced increase. Populations of the prevalent cladocerans, Chydorus sphaericus and Simocephalus vetulus, displayed idiosyncratic patterns, with evidence in the case of S. vetulus for a negative relationship between warming and body‐size at maturity. Copepod populations were reduced in size by warming, but those of ostracods increased. 3. The effects of the nutrient addition and fish treatments were strong and consistent, interacting little with warming effects in statistical models. Zooplankter abundance tended to be the highest in the fish‐free microcosms receiving additional nutrient inputs and lowest when fish were present and no nutrients were added. Both treatments reduced cladoceran diversity and community evenness. 4. We suggest that warming, independently, is unlikely to supplant the effects of changing nutrient loading and fish predation as the major driver of zooplankter dynamics in shallow lakes and ponds. Moreover, in the situations where warming was of significant influence in our experiment, the distinction between summer‐only warming and year‐around warming was blurred. This suggests that warming effects were most pervasive during the summer, at the upper end of the temperature spectrum.