The impacts of diel thermal variability on growth, development and performance of wild Atlantic salmon (Salmo salar) from two thermally distinct rivers.

Temperature in many natural aquatic environments follows a diel cycle, but to date, we know little on how diel thermal cycles affect fish biology. The current study investigates the growth, development and physiological performance of wild Atlantic salmon collected from the Miramichi and Restigouche rivers (NB, Canada). Fish were collected as parr and acclimated to either 16-21 or 19-24°C diel thermal cycles throughout the parr and smolt life stages. Both Miramichi and Restigouche Atlantic salmon parr grew at similar rates during 16-21 or 19-24°C acclimations. However, as smolts, the growth rates of the Miramichi (-8% body mass day-1) and Restigouche (-38% body mass day-1) fish were significantly slower at 19-24°C, and were in fact negative, indicating loss of mass in this group. Acclimation to 19-24°C also increased Atlantic salmon CTmax. Our findings suggest that both life stage and river origin impact Atlantic salmon growth and performance in the thermal range used herein. These findings provide evidence for local adaptation of Atlantic salmon, increased vulnerability to warming temperatures, and highlight the differential impacts of these ecologically relevant diel thermal cycles on the juvenile life stages in this species.

Thermal variability induces sex-specific morphometric changes in zebrafish (Danio rerio).

In nature, organisms are exposed to variable environmental conditions that impact their performance and fitness. Despite the ubiquity of environmental variability, substantial knowledge gaps in our understanding of organismal responses to nonconstant thermal regimes remain. In the present study, using zebrafish (Danio rerio) as a model organism, we applied geometric morphometric methods to examine how challenging but ecologically realistic diel thermal fluctuations experienced during different life stages influence adult body shape, size, and condition. Zebrafish were exposed to either thermal fluctuations (22-32°C) or a static optimal temperature (27°C) sharing the same thermal mean during an early period spanning embryonic and larval ontogeny (days 0-30), a later period spanning juvenile and adult ontogeny (days 31-210), or a combination of both. We found that body shape, size, and condition were affected by thermal variability, but these plasticity-mediated changes were dependent on the timing of ontogenetic exposure. Notably, after experiencing fluctuating temperatures during early ontogeny, females displayed a deeper abdomen while males displayed an elongated caudal peduncle region. Moreover, males displayed beneficial acclimation of body condition under lifelong fluctuating temperature exposure, whereas females did not. The present study, using ecologically realistic thermal regimes, provides insight into the timing of environmental experiences that generate phenotypic variation in zebrafish.

Phytoplankton competition and resilience under fluctuating temperature.

Environmental variability is an inherent feature of natural systems which complicates predictions of species interactions. Primarily, the complexity in predicting the response of organisms to environmental fluctuations is in part because species' responses to abiotic factors are non-linear, even in stable conditions. Temperature exerts a major control over phytoplankton growth and physiology, yet the influence of thermal fluctuations on growth and competition dynamics is largely unknown. To investigate the limits of coexistence in variable environments, stable mixed cultures with constant species abundance ratios of the marine diatoms, Phaeodactylum tricornutum and Thalassiosira pseudonana, were exposed to different temperature fluctuation regimes (n = 17) under high and low nitrogen (N) conditions. Here we demonstrate that phytoplankton exhibit substantial resilience to temperature variability. The time required to observe a shift in the species abundance ratio decreased with increasing fluctuations, but coexistence of the two model species under high N conditions was disrupted only when amplitudes of temperature fluctuation were high (±8.2°C). N limitation caused the thermal amplitude for disruption of species coexistence to become lower (±5.9°C). Furthermore, once stable conditions were reinstated, the two species differed in their ability to recover from temperature fluctuations. Our findings suggest that despite the expectation of unequal effect of fluctuations on different competitors, cycles in environmental conditions may reduce the rate of species replacement when amplitudes remain below a certain threshold. Beyond these thresholds, competitive exclusion could, however, be accelerated, suggesting that aquatic heatwaves and N availability status are likely to lead to abrupt and unpredictable restructuring of phytoplankton community composition.

Effects of thermal fluctuations on biological processes: a meta-analysis of experiments manipulating thermal variability.

Thermal variability is a key driver of ecological processes, affecting organisms and populations across multiple temporal scales. Despite the ubiquity of variation, biologists lack a quantitative synthesis of the observed ecological consequences of thermal variability across a wide range of taxa, phenotypic traits and experimental designs. Here, we conduct a meta-analysis to investigate how properties of organisms, their experienced thermal regime and whether thermal variability is experienced in either the past (prior to an assay) or present (during the assay) affect performance relative to the performance of organisms experiencing constant thermal environments. Our results-which draw upon 1712 effect sizes from 75 studies-indicate that the effects of thermal variability are not unidirectional and become more negative as mean temperature and fluctuation range increase. Exposure to variation in the past decreases performance to a greater extent than variation experienced in the present and increases the costs to performance more than diminishing benefits across a broad set of empirical studies. Further, we identify life-history attributes that predictably modify the ecological response to variation. Our findings demonstrate that effects of thermal variability on performance are context-dependent, yet negative outcomes may be heightened in warmer, more variable climates.

Differential reproductive plasticity under thermal variability in a freshwater fish (Danio rerio).

Human-driven increases in global mean temperatures are associated with concomitant increases in thermal variability. Yet, few studies have explored the impacts of thermal variability on fitness-related traits, limiting our ability to predict how organisms will respond to dynamic thermal changes. Among the myriad organismal responses to thermal variability, one of the most proximate to fitness-and, thus, a population's ability to persist-is reproduction. Here, we examine how a model freshwater fish (Danio rerio) responds to diel thermal fluctuations that span the species's viable developmental range of temperatures. We specifically investigate reproductive performance metrics including spawning success, fecundity, egg provisioning and sperm concentration. Notably, we apply thermal variability treatments during two ontogenetic timepoints to disentangle the relative effects of developmental plasticity and reversible acclimation. We found evidence of direct, negative effects of thermal variability during later ontogenetic stages on reproductive performance metrics. We also found complex interactive effects of early and late-life exposure to thermal variability, with evidence of beneficial acclimation of spawning success and modification of the relationship between fecundity and egg provisioning. Our findings illuminate the plastic life-history modifications that fish may undergo as their thermal environments become increasingly variable.

Acute, diel, and annual temperature variability and the thermal biology of ectotherms.

Global warming is increasing mean temperatures and altering temperature variability at multiple temporal scales. To better understand the consequences of changes in thermal variability for ectotherms it is necessary to consider thermal variation at different time scales (i.e., acute, diel, and annual) and the responses of organisms within and across generations. Thermodynamics constrain acute responses to temperature, but within these constraints and over longer time periods, organisms have the scope to adaptively acclimate or evolve. Yet, hypotheses and predictions about responses to future warming tend not to explicitly consider the temporal scale at which temperature varies. Here, focusing on multicellular ectothermic animals, we argue that consideration of multiple processes and constraints associated with various timescales is necessary to better understand how altered thermal variability because of climate change will affect ectotherms.

Thermal performance curves for aerobic scope in a tropical fish (Lates calcarifer): flexible in amplitude but not breadth.

Aerobic metabolic scope is a popular metric to estimate the capacity for temperature-dependent performance in aquatic animals. Despite this popularity, little is known of the role of temperature acclimation and variability in shaping the breadth and amplitude of the thermal performance curve for aerobic scope. If daily thermal experience can modify the characteristics of the thermal performance curve, interpretations of aerobic scope data from the literature may be misguided. Here, tropical barramundi (Lates calcarifer) were acclimated for ∼4 months to cold (23°C), optimal (29°C) or warm (35°C) conditions, or to a daily temperature cycle between 23 and 35°C (with a mean of 29°C). Measurements of aerobic scope were conducted every 3-4 weeks at three temperatures (23, 29 and 35°C), and growth rates were monitored. Acclimation to constant temperatures caused some changes in aerobic scope at the three measurement temperatures via adjustments in standard and maximum metabolic rates, and growth rates were lower in the 23°C-acclimated group than in all other groups. The metabolic parameters and growth rates of the thermally variable group remained similar to those of the 29°C-acclimated group. Thus, acclimation to a variable temperature regime did not broaden the thermal performance curve for aerobic scope. We propose that thermal performance curves for aerobic scope are more plastic in amplitude than in breadth, and that the metabolic phenotype of at least some fish may be more dependent on the mean daily temperature than on the daily temperature range.

The critical thermal maximum of diving beetles (Coleoptera: Dytiscidae): a comparison of subterranean and surface-dwelling species.

Thermal tolerance limits in animals are often thought to be related to temperature and thermal variation in their environment. Recently, there has been a focus on studying upper thermal limits due to the likelihood for climate change to expose more animals to higher temperatures and potentially extinction. Organisms living in underground environments experience reduced temperatures and thermal variation in comparison to species living in surface habitats, but how these impact their thermal tolerance limits are unclear. In this study, we compare the thermal critical maximum (CTmax) of two subterranean diving beetles (Dytiscidae) to that of three related surface-dwelling species. Our results show that subterranean species have a lower CTmax (38.3-39.0°C) than surface species (42.0-44.5°C). The CTmax of subterranean species is ∼10°C higher than the highest temperature recorded within the aquifer. Groundwater temperature varied between 18.4°C and 28.8°C, and changes with time, depth and distance across the aquifer. Seasonal temperature fluctuations were 0.5°C at a single point, with the maximum heating rate being ∼1000x lower (0.008°C/hour) than that recorded in surface habitats (7.98°C/hour). For surface species, CTmax was 7-10°C higher than the maximum temperature in their habitats, with daily fluctuations from ∼1°C to 16°C and extremes of 6.9°C and 34.9°C. These findings suggest that subterranean dytiscid beetles are unlikely to reach their CTmax with a predicted warming of 1.3-5.1°C in the region by 2090. However, the impacts of long-term elevated temperatures on fitness, different life stages and other species in the beetle's trophic food web are unknown.

Thermal variation near the thermal optimum does not affect the growth, metabolism or swimming performance in wild Atlantic salmon Salmo salar.

Typically, laboratory studies on the physiological effects of temperature are conducted using stable acclimation temperatures. Nonetheless, information extrapolated from these studies may not accurately represent wild populations living in thermally variable environments. The aim of this study was to compare the growth rate, metabolism and swimming performance of wild Atlantic salmon exposed to cycling temperatures, 16-21°C, and stable acclimation temperatures, 16, 18.5, 21°C. Growth rate, metabolic rate, swimming performance and anaerobic metabolites did not change among acclimation groups, suggesting that within Atlantic salmon's thermal optimum range, temperature variation has no effect on these physiological properties.

The physiological ups and downs of thermal variability in temperate freshwater ecosystems.

Freshwater fish face a variety of spatiotemporal thermal challenges throughout their life. On a broad scale, temperature is an important driver of physiological, behavioural and ecological patterns and ultimately affects populations and overall distribution. These broad patterns are partly underpinned by the small-scale local effects of temperature on individuals within the population. Climate change is increasing the range of daily thermal variation in most freshwater ecosystems, altering behaviour and performance of resident fishes. The aim of this review is understanding how daily thermal variation in temperate rivers affects individual fish physiology, behaviour and overall performance. The following are highlighted in this study: (a) the physical characteristics of rivers that can either buffer or exacerbate thermal variability, (b) the effects of thermal variability on growth and metabolism, (c) the approaches for quantifying thermal variation and thermal stress and (d) how fish may acclimatize or adapt to our changing climate.

Thermal variability during ectotherm egg incubation: A synthesis and framework.

Natural populations of ectothermic oviparous vertebrates typically experience thermal variability in their incubation environment. Yet an overwhelming number of laboratory studies incubate animals under constant thermal conditions that cannot capture natural thermal variability. Here, we systematically searched for studies that incubated eggs of ectothermic vertebrates, including both fishes and herpetofauna, under thermally variable regimes. We ultimately developed a compendium of 66 studies that used thermally variable conditions for egg incubation. In this review, we qualitatively discuss key findings from literature in the compendium, including the phenotypic effects resulting from different patterns of thermally variable incubation, as well as the ontogenetic persistence of these effects. We also describe a physiological framework for contextualizing some of these effects, based on thermal performance theory. Lastly, we highlight key gaps in our understanding of thermally variable incubation and offer suggestions for future studies.

Short communication: Domesticated and wild fathead minnows differ in growth and thermal tolerance.

Many populations have evolved in response to laboratory environments (lack of predators, continual food availability, etc.). Another potential agent of selection in the lab is exposure to constant thermal environments. Here, we examined changes in growth, critical thermal maximum (CTmax), and food consumption under constant (25 °C) and fluctuating (22-28 °C and 19-31 °C) conditions in two populations of fathead minnows, Pimephales promelas: one that has been kept in a laboratory setting for over 120 generations (~40 years) and a corresponding wild one. We found that under thermal fluctuations, domesticated fathead minnows grew faster than their wild counterparts, but also exhibited lower thermal tolerance. Food consumption was significantly higher in the lab population under the constant and large fluctuation thermal treatments. Our results suggest that the lab population has adjusted to the stable conditions in the laboratory and that we should carefully apply lessons learned in the lab to wild populations.

Rapid within- and transgenerational changes in thermal tolerance and fitness in variable thermal landscapes.

Phenotypic plasticity may increase the performance and fitness and allow organisms to cope with variable environmental conditions. We studied within-generation plasticity and transgenerational effects of thermal conditions on temperature tolerance and demographic parameters in Drosophila melanogaster. We employed a fully factorial design, in which both parental (P) and offspring generations (F1) were reared in a constant or a variable thermal environment. Thermal variability during ontogeny increased heat tolerance in P, but with demographic cost as this treatment resulted in substantially lower survival, fecundity, and net reproductive rate. The adverse effects of thermal variability (V) on demographic parameters were less drastic in flies from the F1, which exhibited higher net reproductive rates than their parents. These compensatory responses could not totally overcome the challenges of the thermally variable regime, contrasting with the offspring of flies raised in a constant temperature (C) that showed no reduction in fitness with thermal variation. Thus, the parental thermal environment had effects on thermal tolerance and demographic parameters in fruit fly. These results demonstrate how transgenerational effects of environmental conditions on heat tolerance, as well as their potential costs on other fitness components, can have a major impact on populations' resilience to warming temperatures and more frequent thermal extremes.

Rapid metabolic compensation in response to temperature change in the intertidal copepod, Tigriopus californicus.

Animals living in the intertidal zone must adapt to thermal variability, including adjustments in metabolism. We examined metabolic responses to temperature in the copepod, Tigriopus californicus, which inhabits supratidal splash pools along the Pacific coast of North America. We maintained three populations of T. californicus at 20 °C, one from southern California (San Diego, "SD") and two from Oregon (Fogarty Creek, "FCN", Boiler Bay, "BOB") and examined possible geographic patterns in metabolism. We measured oxygen consumption rate (V̇o2) at 20 °C and following 48 h (chronic) acclimation to 25, 27.5 and 30 °C. V̇o2 was temperature-independent, with temperature quotients (Q10) values ≤1 in all populations, indicative of metabolic compensation. We detected no variation in V̇o2 or survival between populations. To explore the time course of metabolic compensation, we performed an acute acclimation experiment in which V̇o2 was measured at 20 °C, following immediate exposure to 25 °C, and following 2 h, 4 h and 6 h exposure to 25 °C. This acute acclimation experiment revealed that V̇o2 increased immediately in SD and FCN, but was no longer different than 20 °C levels by 2 h and 4 h at 25 °C, respectively. BOB showed no significant change in V̇o2, which may indicate complete temperature-independent metabolism or different mechanisms of compensation between populations. This study demonstrates a time course of rapid metabolic compensation in response to temperature that occurs in a small intertidal animal, and suggests intertidal invertebrates can thermally acclimate within a few hours of a significant temperature change.

Nonlinear averaging of thermal experience predicts population growth rates in a thermally variable environment.

As thermal regimes change worldwide, projections of future population and species persistence often require estimates of how population growth rates depend on temperature. These projections rarely account for how temporal variation in temperature can systematically modify growth rates relative to projections based on constant temperatures. Here, we tested the hypothesis that time-averaged population growth rates in fluctuating thermal environments differ from growth rates in constant conditions as a consequence of Jensen's inequality, and that the thermal performance curves (TPCs) describing population growth in fluctuating environments can be predicted quantitatively based on TPCs generated in constant laboratory conditions. With experimental populations of the green alga Tetraselmis tetrahele, we show that nonlinear averaging techniques accurately predicted increased as well as decreased population growth rates in fluctuating thermal regimes relative to constant thermal regimes. We extrapolate from these results to project critical temperatures for population growth and persistence of 89 phytoplankton species in naturally variable thermal environments. These results advance our ability to predict population dynamics in the context of global change.

Plastic responses to diel thermal variation in juvenile green sturgeon, Acipenser medirostris.

Human-induced thermal variability can disrupt energy balance and performance in ectotherms; however, phenotypic plasticity may play a pivotal protective role. Ectotherm performance can be maintained in thermally heterogeneous habitats by reducing the thermal sensitivity of physiological processes and concomitant performance. We examined the capacity of juvenile green sturgeon (Acipenser medirostris) to respond to daily thermal variation. Juveniles (47 days post-hatch) were exposed to either stable (15 ±â€¯0.5 °C) or variable (narrowly variable: 13-17 °C day-1 or widely variable 11-21 °C day-1) thermoperiod treatments, with equivalent mean temperatures (15 ±â€¯0.5 °C), for 21 days. Growth (relative growth rate, % body mass gain), upper thermal tolerance (critical thermal maxima, CTMax) and the thermal sensitivity of swimming performance (critical swimming speed, Ucrit) were assessed in fish from all treatments. Accelerated growth was observed in fish maintained under widely variable temperatures compared to narrowly variable and stable temperatures. No significant variation in CTMax was observed among thermoperiod treatments, suggesting all treatment groups acclimated to the mean temperature rather than daily maximums. The widely variable treatment induced a plastic response in swimming performance, where Ucrit was insensitive to temperature and performance was maintained across a widened thermal breadth. Maximum Ucrit attained was similar among thermoperiod treatments, but performance was maximised at different test temperatures (stable: 4.62 ±â€¯0.44 BL s-1 at 15 °C; narrowly variable: 4.52 ±â€¯0.23 BL s-1 at 21 °C; widely variable: 3.90 ±â€¯0.24 BL s-1 at 11 °C, mean ±â€¯s.e.m.). In combination, these findings suggest juvenile A. medirostris are resilient to daily fluctuations in temperature, within the temperature range tested here.

Fluctuating thermal environments and time-dependent effects on fruit fly egg-hatching performance.

Organismal performance in a changing environment is dependent on temporal patterns and duration of exposure to thermal variability. We experimentally assessed the time-dependent effects of thermal variability (i.e., patterns of thermal exposure) on the hatching performance of Drosophila melanogaster. Flies were collected in central Chile and maintained for four generations in laboratory conditions. Fourth generation eggs were acclimated to different thermal fluctuation cycles until hatching occurred. Our results show that the frequency of extreme thermal events has a significant effect on hatching success. Eggs exposed to 24 hr cycles of thermal fluctuation had a higher proportion of eggs that hatched than those acclimated to shorter (6 and 12 hr) and longer cycles (48 hr). Furthermore, eggs subjected to frequent thermal fluctuations hatched earlier than those acclimated to less frequent thermal fluctuations. Overall, we show that, egg-to-adult viability is dependent on the pattern of thermal fluctuations experienced during ontogeny; thus, the pattern of thermal fluctuation experienced by flies has a significant and until now unappreciated impact on fitness.

Repeated freezing induces a trade-off between cryoprotection and egg production in the goldenrod gall fly, Eurosta solidaginis.

Internal ice formation leads to wholesale changes in ionic, osmotic and pH homeostasis, energy metabolism, and mechanical damage, across a small range of temperatures, and is thus an abiotic stressor that acts at a distinct, physiologically relevant, threshold. Insects that experience repeated freeze-thaw cycles over winter will cross this stressor threshold many times over their lifespan. Here, we examined the effect of repeatedly crossing the freezing threshold on short-term physiological parameters (metabolic reserves and cryoprotectant concentration) as well as long-term fitness-related performance (survival and egg production) in the freeze-tolerant goldenrod gall fly, Eurosta solidaginis We exposed overwintering prepupae to a series of low temperatures (-10, -15 or -20°C) with increasing numbers of freezing events (3, 6 or 10) with differing recovery periods between events (1, 5 or 10 days). Repeated freezing increased sorbitol concentration by about 50% relative to a single freezing episode, and prompted prepupae to modify long-chain triacylglycerols to acetylated triacylglycerols. Long-term, repeated freezing did not significantly reduce survival but did reduce egg production by 9.8% relative to a single freezing event. Exposure temperature did not affect any of these measures, suggesting that threshold crossing events may be more important to fitness than the intensity of stress in overwintering E. solidaginis.

Avian parental behavior and nest success influenced by temperature fluctuations.

Behavioral adjustments and parental decisions during reproduction can influence the thermal environment at nests, yet our understanding into how environmental factors (i.e., temperature and precipitation) constrain an adult's ability to balance self-maintenance and incubation demands is limited. To expand our understanding of how species respond to environmental factors, we investigated the reproductive ecology of two ground-nesting species (northern bobwhite [Colinus virginianus] and scaled quail [Callipepla squamata]) in a region (i.e., the Southern Great Plains) prone to thermal variability (i.e., extreme hot and cold temperatures). Specifically, our objective was to examine how temperature and precipitation directly influenced behavioral adjustments (i.e., off-bout duration, frequency, and nest attentiveness) and parental decisions (i.e., nest site selection), and indirectly influenced nest fate. Overall, we found that parents chose to nest in sites that were significantly cooler in temperature than randomly selected sites, and parents further altered the thermal environment experienced by embryos through incubation behavior. Daily precipitation and average ambient temperature and/or their interaction best predicted incubation behaviors, yet each species differed in the timing (i.e., morning vs. evening), frequency, and duration of off-bouts. Furthermore, successful nests were associated with cooler nest site temperatures for bobwhite and warmer nest site temperatures for scaled quail. Our finding of relatively stable (35.5 °C) incubation temperature for developing embryos of both species suggests that ground-nesting birds are able to regulate microclimate through behavioral adjustments and parental decisions even under extreme temperature fluctuations. Nevertheless, the ability for a ground-nesting species to effectively modify behavioral adjustments and decisions may be altered during long periods of enhanced physiological and environmental stress.

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.