Climate change and the evolution of reef fishes: past and future

Predicting the impacts of ocean warming and acidification on marine ecosystems requires an evolutionary perspective because, for most marine species, these environmental changes will occur over a number of generations. Acclimation through phenotypic plasticity and adaptation through genetic selection could help populations of some species cope with future warmer and more acidic oceans. Coral reef species are predicted to be some of the most vulnerable to climate change because they live close to their thermal limits. Yet, their evolutionary history may indicate that they possess adaptations that enable them to cope with a high CO₂ environment. Here, we first explore the evolutionary history of reef fishes and how their history has shaped their physiological adaptations to environmental temperatures and pCO₂. We examine current‐day thermal and CO₂ environments experienced by coral reef fishes and summarize experimental studies that have tested how they respond to elevated temperatures and pCO₂ levels. We then examine evidence for acclimation and adaptation to projected ocean warming and acidification. Indeed, new studies have demonstrated the potential for transgenerational plasticity and heritable genetic variation that would allow some fishes to maintain performance as the oceans warm and become more acidic. We conclude by outlining management approaches – specifically those that can help preserve genetic variation by maintaining population size – to enhance the potential for genetic adaptation to climate change.     

Latitudinal variation in growth and otolith‐inferred field metabolic rates of Canadian young‐of‐the‐year Arctic charr

Countergradient variation (CGV) is defined as genetic variation that counteracts the negative influences of the physical environment, minimising phenotypic variability along an environmental gradient. CGV is thought to have relevance in predicting the response of organisms to climate variability and change. To test the hypothesis that growth rate increased with latitude, consistent with CGV, young‐of‐the‐year (YOY) Arctic charr, Salvelinus alpinus, were examined along a ~27° latitudinal gradient in central and eastern Canada. Growth rates were estimated from fork lengths standardised by the thermal opportunity for growth based on experienced water temperatures derived using otolith oxygen stable isotopes. Results demonstrated patterns consistent with CGV, where northern populations demonstrated faster growth rates. A secondary aim was to test for similar geographical patterns in otolith‐inferred metabolic rates, which reflect the energetic costs of standard metabolic rate (SMR) and other processes such as feeding, locomotion, thermoregulation, reproduction and growth. Results demonstrated a significant, positive relationship between otolith‐inferred metabolic rate and latitude, which may reflect an increase in one, or a combination, of the above‐noted physiological processes. The similar latitudinal pattern in growth and otolith‐inferred metabolic rates suggests greater intake of food per unit of time by northern fish. The phenotypic variation in physiological traits observed here demonstrates the significant adaptability of Arctic charr to different thermal regimes with different growing season lengths. Determining the relative contributions of phenotypic plasticity and genetic variation to the observed latitudinal variation will be critical to predicting the responses of Arctic charr to climate change more accurately.     

Subpolar gyre and temperature drive boreal fish abundance in Greenland waters

As result of ocean warming, marine boreal species have shifted their distribution poleward, with increases in abundance at higher latitudes, and declines in abundance at lower latitudes. A key to predict future changes in fish communities is to understand how fish stocks respond to climate variability. Scattered field observations in the first half of the 20th century suggested that boreal fish may coherently invade Greenland waters when temperatures rise, but this hypothesis has remained untested. Therefore, we studied how local temperature variability and the dynamics of the subpolar gyre, a large‐scale driver of oceanic conditions in the North Atlantic, affect abundance of boreal fishes in a region that sharply defines their lower thermal boundary. We analysed information from demersal trawl surveys from 1981 to 2017, for species distributed from shallow shelf to depths of 1,500 m, collected at over 10,000 stations along ~3,000 km of Greenland. Our results show that local temperature and variability of Labrador and Irminger Sea water in the subpolar gyre region drive interdecadal variability of boreal fish abundance in Greenland waters. Although temperature fluctuations were higher in shallow than deep regions, fish abundance changed as quickly in great depths as in shallow depths. This link between physics and biology provides an opportunity for prediction of future trends, which is of utility in Greenland, where fisheries constitute more than 90% of the national export value.     

Contrasting climate velocity impacts in warm and cool locations show that effects of marine warming are worse in already warmer temperate waters

Species responses to climate change are often measured at broad spatiotemporal scales, which can miss the fine-scale changes that are most relevant to conservation and fisheries management. We develop a scaleable geostatistical approach to assess how juvenile and adult fish distributions have been shaped by changes in bottom temperature and dissolved oxygen over a recent decade of warming in the northeast Pacific. Across 38 demersal fishes, biomass trends were associated negatively with warming and positively with dissolved oxygen, but when trends in both biomass and climate were converted to velocities—the speed and direction a population would have to move to maintain consistent conditions—the effect of temperature change differed depending on local conditions. In the warmest locations, warming velocities were associated with negative biotic velocities for 19 of 69 species-maturity combinations, and yet were almost always associated with stable or positive biotic velocities in the coolest locations (64 of 69). These spatially consistent biomass declines (negative biotic velocities) in the warmest locations and increases in cooler locations suggest a redistribution of species with the potential for new ecological and fisheries interactions. After controlling for temperature, the more spatially consistent effects of dissolved oxygen were often negative, suggesting a mechanism other than hypoxia avoidance—potentially changes in primary production. Our approach identifies the species and locations that are most sensitive to observed changes in the environment at any scale, thus facilitating future vulnerability assessments.     

Downstream effects of hydroelectric dam operation on thermal habitat use by Brook Trout (Salvelinus fontinalis) and Slimy Sculpin (Cottus cognatus)

Hydroelectric dams can alter downstream water temperatures, impacting thermal habitat available for fishes. Decreases in river water temperatures resulting from hydroelectric dam operations may be beneficial to coldwater species and could potentially offset warming resulting from climatic trends. We used two coldwater fish species, Slimy Sculpin (Cottus cognatus) and Brook Trout (Salvelinus fontinalis) to assess the impact of a cool water draw below a 15 MW hydroelectric dam on fish thermal habitat use relative to a nearby naturally flowing river. Cooler water temperatures below the dam corresponded with significantly cooler mean growth season temperature use for Slimy Sculpin, but not Brook Trout, relative to the natural river. As well, mean growing season temperature use by Slimy Sculpin was significantly cooler relative to Brook Trout in both rivers, and significantly different amongst studied sites in the regulated river. Fish condition was significantly correlated with temperature use for Slimy Sculpin in the naturally flowing river only. Our results indicate that manipulating river water temperatures through hydroelectric dam operations to benefit multiple fish species will be difficult given the complexity of riverine thermal habitat and species‐specific differences in thermal preferences and behaviour.     

Behavioural thermoregulation in cold-water freshwater fish: Innate resilience to climate warming?

Behavioural thermoregulation enables ectotherms to access habitats providing conditions within their temperature optima, especially in periods of extreme thermal conditions, through adjustments to their behaviours that provide a “whole-body” response to temperature changes. Although freshwater fish have been detected as moving in response to temperature changes to access habitats that provide their thermal optima, there is a lack of integrative studies synthesising the extent to which this is driven by behaviour across different species and spatial scales. A quantitative global synthesis of behavioural thermoregulation in freshwater fish revealed that across 77 studies, behavioural thermoregulatory movements by fish were detected both vertically and horizontally, and from warm to cool waters and, occasionally, the converse. When fish moved from warm to cooler habitats, the extent of the temperature difference between these habitats decreased with increasing latitude, with juvenile and non-migratory fishes tolerating greater temperature differences than adult and anadromous individuals. With most studies focused on assessing movements of cold-water salmonids during summer periods, there remains an outstanding need for work on climatically vulnerable, non-salmonid fishes to understand how these innate thermoregulatory behaviours could facilitate population persistence in warming conditions.     

水温升高对水体性质及水生生物的影响研究进展

全球变暖导致水温升高,河流、湖泊普遍升温,而这种增温趋势还将加剧。水温升高,直接导致水体稳定度提高,垂向对流减少,分层现象加剧,冰河解冻提前,水体封冻期缩短;间接导致水体溶解氧含量降低,尤其底层水体缺氧现象更加严重,底层水体缺氧导致沉积物中营养盐向上覆水的释放量增加,两者均会诱导水体发生气候变化富营养化。水温升高影响水生有机体的生物过程、物种组成及食物网变化;水体分层及溶解氧含量降低均会增加水体营养物负荷,促进水体浮游藻类种群发生变化;水温变化还会改变水生植物生长条件、生物量及分布,影响水体中鱼类的生存、生长发育,以及栖息地发生变化,使水生无脊椎动物种群数量减少。因此,水温增加势必对水生生态系统产生重要影响。     

Coping with climate change: Phenotypic plasticity in an imperilled freshwater fish in response to elevated water temperature

1. Climate change has emerged as an increasingly important threat to freshwater systems. To cope with rapidly changing thermal regimes, freshwater fishes must either relocate or adjust through genetic adaptation and/or phenotypic plasticity. Short-term responses to elevated water temperature have been well studied in freshwater fishes; however, far less is understood about change induced by long-term exposure. Furthermore, few studies have investigated the effects of temperature on already imperilled species, which may be more sensitive to environmental change.
2. This study investigated the effects of rearing temperature on critical thermal maximum (CT_max), agitation temperature (T_ag, temperature at which fish show behavioural signs of thermal stress) and gill size in pugnose shiner, Notropis anogenus, a threatened species in Canada. Juvenile pugnose shiner were reared for 4 months across five different ecologically relevant temperatures. CT_max and T_ag were measured under normoxia and acute exposure to hypoxia to test for oxygen sensitivity of the upper thermal limits in this species.
3. CT_max increased with elevated water temperature. T_ag also increased with rearing temperature and occurred, on average, 4.3°C above acclimation temperatures. The CT_max and T_ag were lower when fish were exposed acutely to hypoxia. Interestingly, gill size (e.g. total gill filament length) increased with rearing temperature, which may increase oxygen uptake capacity and support increased metabolic demands of warmer waters.
4. Overall, pugnose shiner show plasticity in several traits in response to long-term exposure to elevated water temperature that may facilitate persistence in warmer waters. However, acute hypoxia exposure reduced thermal tolerance, stressing the importance of evaluating interactive effects of multiple stressors.
5. Identifying source populations of pugnose shiner with greater thermal tolerance or implementing captive breeding under higher temperature regimes may improve the success of re-introduction efforts in the face of climate change, but the consequences to fitness of increased thermal tolerance should be examined.

     

Fishes of southern South America: a story driven by temperature

The latitudinal extension of southern South America imposes a thermal gradient that affects the structure of marine and freshwater fish assemblages and the biology of the species through direct exposure to the temperature gradients or by means of a web of historical and ecological relationships. We have reviewed biological and ecological data of marine and freshwater fishes from the southern Neotropics, including Patagonia, and report several examples of dependence on temperature, from glacial times to today’s climate change. We were able to identify historic and present effects on the diversity of fish assemblages, isolation, southern limits for the distribution of species, and morphological variation among populations. There is a wide range of characteristics that exemplify an adaptation to low temperatures, including biochemical peculiarities, physiological adjustments, and alternative life history patterns, and these appear in both freshwater and marine, and native and exotic fishes. The consequences of stable temperature regimes in both the ocean and thermal streams deserve special mention as these shape specialists under conditions of low selective pressure. At present, habitat use and interactions among species are being subject to changes as consequences of water temperature, and some of these are already evident in the northern and southern hemispheres.     

The role of temperature in the capture and release of fish

We searched major electronic databases to identify peer‐reviewed literature investigating the role of temperature on the stress response and mortality of captured and released fish. We identified 83 studies that fit these criteria, the majority of which were conducted in North America (81%) on freshwater fish (76%) in the orders Perciformes (52%) and Salmoniformes (28%). We found that hook‐and‐line fisheries (65% of all studies) were more commonly studied than all net fisheries combined (24%). Despite the wide recognition for many species that high water temperatures exacerbate the effects of capture on released fish, this review is the first to quantitatively investigate this problem, finding that warming contributed to both mortality and indices of stress in 70% of articles that measured each of those endpoints. However, more than half (58%) of the articles failed to place the experimental temperatures into a biological context, therefore limiting their broad applicability to management. Integration of survival and sublethal effects to investigate mechanisms of fish mortality was relatively rare (28%). Collectively, the results suggest that capture–release mortality increases at temperatures within, rather than above, species‐specific thermal preferenda. We illustrate how knowledge of ecologically relevant high temperatures in the capture and release of fish can be incorporated into management, which will become increasingly important as climate change exerts additional pressure on fish and fisheries.     

Projecting future habitat quality of three midwestern reservoir fishes under warming conditions

Rising temperatures caused by climate change are likely to affect cool‐water and warm‐water fishes differently. Yet, forecasts of anticipated temperature effects on fishes of different thermal guilds are lacking, especially in freshwater ecosystems. Towards this end, we used spatially explicit, growth rate potential (GRP) models to project changes in seasonal habitat quality for a warm‐water piscivore (largemouth bass Micropterus salmoides), a cool‐water piscivore (walleye Sander vitreus) and a hybrid piscivore (saugeye S. vitreus × S. canadensis) in two Midwestern reservoirs. We assessed habitat quality for two periods (early and middle 21st century) under two realistic greenhouse gas emission scenarios (a mid‐century emissions peak and a rapid continuous increase in emissions). Largemouth bass were projected to experience enhanced or slightly reduced habitat during all seasons, and throughout the mid‐21st century. By contrast, walleye habitat was projected to decline with anticipated warming, except during the spring in the smaller of our two study reservoirs and during the fall in the larger of our two study reservoirs. Saugeye habitat was projected to either increase modestly or decline slightly during the spring and fall and declines in habitat quality and quantity that were smaller than those for walleye were identified during summer. Collectively, our findings indicate that climate warming will differentially alter habitat suitability for reservoir piscivores, favouring warm‐water species over cool‐water species. We expect these changes in habitat quality to impact the dynamics of reservoir fish populations to varying degrees necessitating the consideration of climate when making future management decisions.     

Predicting egg size across temperatures in marine teleost fishes

Marine teleost fish species in colder environments generally produce larger eggs than those in warmer environments. This pattern is thought to reflect changes in the optimal strategy of allocation to offspring size and number across temperatures, yet quantitative assessments of this hypothesis are lacking. Here, we model optimal offspring size across temperatures in marine teleost fishes based on the trade‐off between offspring survivorship and number. In doing so, we derive quantitative predictions for the relationship of optimal egg size to temperature based on the size and temperature dependences of the growth and mortality, and hence survivorship, of eggs and larvae. Our model shows that smaller eggs are favoured at warmer temperatures largely because egg survivorship declines with both egg size and temperature. The predictions of our model (egg mass in grams = 0.013*e^{?0.11*T ºC}) were comparable to the observed interspecific relationship (0.0029*e^{?0.09*T ºC}; N = 221 spp.). Thus, our results provide insights into how temperature shapes the evolution of egg size in marine teleost fishes.     

Potential impacts of climate change on growth and prey consumption of stream‐dwelling smallmouth bass in the central United States

Smallmouth bass (Micropterus dolomieu, SMB) is a broadly distributed, economically important species in the USA and Canada. Although previous research has suggested that projected climate warming may allow SMB to thrive beyond their current northern distribution, little research has been devoted to the population‐level effects of climate change on warm‐water fishes, including SMB. We modelled the impacts of projected climate change on growth of stream‐dwelling SMB along a north–south gradient in the central USA. Using downscaled regional projections from three global climate models, we generated scenarios for thermal habitat change for four populations (in Oklahoma, Missouri, Iowa and Minnesota) and used bioenergetics simulations to estimate prey consumption and growth under future projections. Bioenergetics simulations showed that prey consumption is expected to increase in all populations with moderate stream warming (2–3 °C). Growth potential is predicted to increase by 3–17% if not limited by food availability with stream warming by 2060 and was most pronounced for southern populations. For each 1 °C increase in stream temperature, SMB consumption would be expected to increase by about 27% and growth would increase by about 6%. Due to implications for species interactions, population performance and regulation of local fisheries, a better understanding of how SMB populations will respond to climate change is recommended for effective management and conservation.     

Temperature influence on the fish assemblage structure in a large lowland river, the lower Oder River, Germany

Abstract –  Water temperatures were expected to structure river fish assemblages by promoting: (i) offspring's growth and densities in warm years, (ii) spring spawning fish when temperatures increase early and (iii) improved growth and overwintering condition from elongated vegetation periods. Favourable temperature conditions in their first year should improve growth and survival in consecutive years. In the lower Oder River, Germany, fish have been sampled annually, 0+ in July since 1997, and older fish in November since 1998. This data set was analysed to test the hypotheses mentioned above. The water temperature ranged between −0.4 and 25.1 °C during the study period, resulting in substantial variations of the 29 temperature metrics derived from daily means. Cumulative degree-days until catch, in spring and during March, as well as minimum and mean temperatures in March and spring explained 63% of the variability observed. The mean total length of the most frequent 0+ fish differed significantly between years related to temperature. Increased length growth at higher temperatures was a general tendency. Total length and density of 0+ fish were significantly inversely correlated, but the potential influence of temperature on species densities was not significant. The mean fish densities varied not significantly between years. No indication was found that higher total length in the first year of life resulted in an improved growth in subsequent years.
For future research and management it has to be expected that temperature impacts become increasingly significant in regulated river systems. With decreasing hydrodynamics the significance of temperature effects will increase.     

Bonga shad (Ethmalosa fimbriata) spawning tactics in an upwelling environment

Successful recruitment in small pelagic fish populations inhabiting upwelling zones is subject to variation in fecundity and is driven by spatial and temporal fluctuations in environmental conditions, that is, mainly sea surface temperature, salinity and food availability. These fluctuations in abiotic factors have stimulated small pelagic fish populations to exhibit specifically adapted spawning tactics. To better understand to what extent a short‐lived exploited fish species such as bonga shad Ethmalosa fimbriata has adapted to an upwelling environment, we have investigated the interrelationship between upwelling intensity as a proxy for productivity and population fecundity by means of a virtual population analysis. We found that females of intermediate size contributed significantly more eggs to the population's fecundity than smaller or larger ones. Our model results further indicate that E. fimbriata exhibits a spawning preference at water temperatures of around 25°C and upwelling intensities of around 2.5 m³ s^?1 m^?1. Hence, we hypothesize that climate change‐driven increases in sea temperatures and modifications of upwelling‐favourable winds could significantly impact the species’ reproductive biology. To understand how climate change might impact fisheries, spawning tactics of small pelagic fishes are important to assess as well as their recruitment success. Such information is particularly relevant in countries where the fishery is critical at socio‐economic level, to better implement fisheries management addressing multiple stressors.     

The effect of lake morphometry on thermal habitat use and growth in Arctic charr populations: implications for understanding climate‐change impacts

Oxygen stable isotope temperature reconstruction methods were used to estimate mean experienced summer temperatures from growth zones within individual Arctic charr otoliths sampled from lakes with contrasting morphologies but proximate locations. For either lake, otolith‐estimated temperatures were not significantly related to back‐calculated growth. Fish in the smaller lake evidenced an increase in growth with age related to increasing use of cooler thermal habitats, with the use of thermal habitat possibly governed by predation risks. No relationships between age, growth or temperature were observed in the larger lake. Significant negative effects on back‐calculated growth were observed due to increasing air temperatures in the smaller and shallower lake, possibly owing to warmer surface and littoral waters and a limited amount of preferred cool‐water habitat. A similar relationship was not observed in the larger and deeper lake and indicated that resident Arctic charr were not as vulnerable to the impacts of temperature warming, possibly because of better behavioural thermoregulation opportunities in the cooler, deeper lake. Results provide evidence for differing climate‐influenced growth outcomes among proximately located populations, with outcomes likely to depend on the differences among habitats, including lake size and morphometry which may act to influence fish densities in available preferred thermal habitats.     

Anticipating climate change impacts on Mongolian salmonids: bioenergetics models for lenok and Baikal grayling

The Eg–Uur River ecosystem in north‐central Mongolia provides an opportunity to study salmonid species in a system that has already experienced significant climate change. These species are currently imperilled in Mongolian waters, with Baikal grayling (Thymallus arcticus baicalensis) listed as near‐threatened and lenok (Brachymystax lenok) listed as vulnerable on the Mongolian red list. Air temperature records demonstrate that in the last 40 years Northern Mongolia's rate of warming has been three times greater than the northern hemisphere average. Despite alarming trends in air temperatures, little is known of the thermal ecology of these species. Due to the threat of climate change to these species, the objective of our study was to quantify metabolic costs for these species from streamside routine metabolic measures and derive bioenergetics models that we used to assess potential climate change response. Streamside measurements of metabolism were remarkably consistent with expectations from measures of other salmonids gathered under more closely controlled laboratory conditions. Metabolism increased exponentially with temperature for both species. The resulting preliminary bioenergetics models suggest these species are already experiencing temperatures near their upper levels for growth during summer and conditions are expected to deteriorate with warming. Even a modest 2 °C increase in water temperatures during ice out would result in a 59% reduction in growth of lenok, and an inability of Baikal grayling to grow (if food levels remained unchanged) or a 14–23% increase in consumption in order to maintain current growth rates.     

Changes in albacore tuna habitat in the northeast Pacific Ocean under anthropogenic warming

Albacore tuna are widespread in the North Pacific Ocean and the basis of an important commercial fishery. These fish live mainly within a fairly narrow thermal niche range defined by sea surface temperature (SST) isotherms between 14 and 19°C. Because the fish's thermal range coincides with strong latitudinal temperature gradients off the northwest coast of North America, there is a great deal of seasonal and interannual variability in the distribution of these fish, and a significant potential for a new habitat in this region with anthropogenic climate change. We use historical catch and effort data from the Canadian troll fleet to define the fish's thermal niche, and document observed shifts in distribution associated with interannual climate variability. We then use an ensemble of climate model simulations from the Coupled Model Intercomparison Project to estimate northward extension of the potential habitat under anthropogenic warming scenarios. A potential new habitat is about half a million square kilometres even under a moderate mitigation scenario. Estimates are smaller for some months of the year in which the fishery is conducted, but as well as opening up new regions, the length of season in which the fishery is active may be extended in the northern part of the range. However, much of the potential new habitat will be in oceanic waters with relatively low productivity. Our estimated area of potential habitat is based on the fish's thermal niche and assumes that other biologically important factors such as food will not be limiting.     

Physical forcing on fish abundance in the southern California Current System

The California Current System (CCS) is an eastern boundary current system with strong biological productivity largely due to seasonal wind‐driven upwelling and transport of the California Current (CC). Two independent, yet complementary time series, CalCOFI ichthyoplankton surveys and sampling of southern California power plant cooling‐water intakes, have indicated that an assemblage of predominantly cool‐water affinity fishes spanning nearshore to oceanic environments in the southern CCS has declined dramatically from the 1970s to the 2000s. We examined potential oceanographic drivers behind this decline both within and north of the CalCOFI survey area in order to capture upstream processes as well. Empirical orthogonal function (EOF) analyses using output from a data‐assimilative regional ocean model revealed significant relationships between the fish time series and spatial patterns of upwelling, upper ocean heat content and eddy kinetic energy in the CCS. Correlation and linear regression analyses indicated that the declining trend in fish abundance was correlated with a suite of factors: reduced offshore and increased inshore upwelling; a long term warming trend combined with more recent interannual variability in ocean temperature; weaker eddy kinetic energy north of Point Conception (35°N), potentially indicating reduced transport of the California Current (CC); increased influence of the California Undercurrent (CUC); and a decline in zooplankton displacement volume across the southern CCS. Understanding how changes in oceanography affect fish populations will offer insights into managing fisheries in a changing climate.     

River modification reduces climate resilience of brown trout (Salmo trutta) populations in Ireland

This study investigated interactions between eco‐hydromorphological state, riparian vegetation cover, water temperature and fish community composition in lowland rivers in Ireland. Physical habitat modification of study sites corresponded with degraded eco‐hydromorphological state (degree of ecological and physical modification) and reduced thermal buffering capacity (greater temperature fluctuation and increased frequency of extreme temperature events). This impact was reflected in the fish community, with a shift from a brown trout‐dominated (Salmo trutta L.) fish assemblage to predominance of the more thermally plastic minnow, Phoxinus phoxinus (L.), and stone loach, Barbatula barbatula (L.). Eco‐hydromorphological state may be a central factor affecting the ability of temperate rivers to resist temperature change in a warming climate and to maintain suitable conditions for salmonids and other cold‐water biota. Strategies aimed at climate change proofing of temperate rivers should focus on preserving or re‐establishing the eco‐hydromorphological processes that create habitat complexity and buffer stream temperature.