Stage-related variation in rapid cold hardening as a test of the environmental predictability hypothesis

The environmental predictability (EP) hypothesis proposes that rapid cold hardening (RCH) might be common in temperate species incapable of surviving freezing events and which also dwell in unpredictable environments. The kelp fly Paractora dreuxi serves as a useful model organism to test this prediction at an intra-specific level because larvae and adults show different responses to low temperature despite occupying a similar unpredictable thermal environment. Here, using acclimation temperatures, which simulated seasonal temperature variation, we find little evidence for RCH in the freeze-intolerant adults but a limited RCH response in freeze-tolerant larvae. In the relatively short-lived adults, survival of -11 degrees C generally did not improve after 2h pre-treatments at -4, -2, 0, 10, 20 or 25 degrees C either in summer- (10 degrees C) or winter (0 degrees C)-acclimated individuals. By contrast, survival of summer-acclimated larvae to -7.6 degrees C was significantly improved by approximately 37% and 30% with -2 and 0 degrees C pre-treatments, respectively. The finding that summer-acclimated larvae showed RCH whereas this was not the case in the winter-acclimated larvae partially supports the predictions of the EP hypothesis. However, the EP hypothesis also predicts that the adults should have demonstrated an RCH response, yet they did not do so. Rather, it seems likely that they avoid stressful environments by behavioural thermoregulation. Differences in responses among the adults and larvae are therefore to some extent predictable from differences in their feeding requirements and behaviour. These results show that further studies of RCH should take into account the way in which differences among life stages influence the interaction between phenotypic plasticity and environmental variability and predictability.     

Life stage-related differences in hardening and acclimation of thermal tolerance traits in the kelp fly, Paractora dreuxi (Diptera, Helcomyzidae)

It is widely appreciated that physiological tolerances differ between life stages. However, few studies have examined stage-related differences in acclimation and hardening. In addition, the behavioural responses involved in determining the form and extent of the short-term phenotypic response are rarely considered. Here, we investigate life stage differences in the acclimation and hardening responses of the survival of a standard heat shock (SHS) and standard low temperature (or cold) shock (SCS), and the crystallization temperature (or supercooling point, SCP) of adults and larvae of the sub-Antarctic kelp fly, Paractora dreuxi. These stages live in the same habitat, but differ substantially in their mobility and thus environmental temperatures experienced. Results showed that neither acclimation nor hardening affected the lower lethal limits in larvae or adults. Adults showed an increase in survival of upper lethal limits after low temperature acclimation, whilst larvae showed a consistent lack of response. The acclimation × hardening interaction significantly affected the SCP in adults, but no response to either acclimation or hardening was found in the larvae. This study further demonstrates the complexities of thermal tolerance responses in P. dreuxi.     

Thermal behaviour of crustaceans

Specific thermoreceptors or putative multimodal thermoreceptors are not known in Crustacea. However, behavioural studies on thermal avoidance and preference and on the effects of temperature on motor activity indicate that the thermosensitivity of crustaceans may be in the range 0.2-2 degrees C. Work on planktonic crustaceans suggests that they respond particularly to changes in temperature by klinokinesis and orthokinesis. The thermal behaviour of crustaceans is modified by thermal acclimation among other factors. The acclimation of the critical maximum temperature is an example of resistance acclimation, while the acclimation of preference behaviour may be classified as capacity acclimation of some other function. In crustaceans, the use of the concepts stenothermy and eurythermy at the species level is questionable, and it is not possible to divide crustacean species into thermal guilds as suggested for fishes. Thermal preference behaviour contributes to fitness in different ways in different species, often by maximising the aerobic metabolic scope for activity. In crustaceans the peripheral nervous system seems to have retained the capacity for thermosensitivity and thermal acclimation independently of the central nervous system control of behaviour.     

Thermal plasticity in the invasive south American tomato pinworm Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae)

South American tomato pinworm, Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae) is a devastating invasive global insect pest of tomato, Solanum lycopersicum (Solanaceae). In nature, pests face multiple overlapping environmental stressors, which may significantly influence survival. To cope with rapidly changing environments, insects often employ a suite of mechanisms at both acute and chronic time-scales, thereby improving fitness at sub-optimal thermal environments. For T. absoluta, physiological responses to transient thermal variability remain under explored. Moreso, environmental effects and physiological responses may differ across insect life stages and this can have implications for population dynamics. Against this background, we investigated short and long term plastic responses to temperature of T. absoluta larvae (4th instar) and adults (24–48 h old) from field populations. We measured traits of temperature tolerance vis critical thermal limits [critical thermal minima (CT_min) and maxima (CT_max)], heat knockdown time (HKDT), chill coma recovery time (CCRT) and supercooling points (SCP). Our results showed that at the larval stage, Rapid Cold Hardening (RCH) significantly improved CT_min and HKDT but impaired SCP and CCRT. Heat hardening in larvae impaired CT_min, CCRT, SCP, CT_max but not HKDT. In adults, both heat and cold hardening generally impaired CT_min and CT_max, but had no effects on HKDT, SCP and CCRT. Low temperature acclimation significantly improved CT_min and HKDT while marginally compromising CCRT and CT_max, whereas high temperature acclimation had no significant effects on any traits except for HKDT in larvae. Similarly, low and high temperature acclimation had no effects on CT_min, SCPs and CT_max, while high temperature acclimation significantly compromised adult CCRT. Our results show that larvae are more thermally plastic than adults and can shift their thermal tolerance in short and long timescales. The larval plasticity reported here could be advantageous in new envirnments, suggesting an asymmetrical ecological role of larva relative to adults in facilitating T. absoluta invasion.     

Consequences of thermal acclimation for the mating behaviour and swimming performance of female mosquito fish

The mating system of eastern mosquito fish (Gambusia holbrooki) is dominated by male sexual coercion, where all matings are forced and females never appear to cooperate and actively avoid all attempts. Previous research has shown that male G. holbrooki offer a model system for examining the benefits of reversible thermal acclimation for reproductive success, but examining the benefits to female avoidance behaviour has been difficult. In this study, we examined the ability of non-male-deprived female G. holbrooki to avoid forced-coercive matings following acclimation to either 18 or 30 degrees C for six weeks (12h light:12h dark photoperiod). Thermal acclimation of burst and sustained swimming performance was also assessed, as these traits are likely to underlie their ability to avoid forced matings. There was no influence of thermal acclimation on the burst swimming performance of female G. holbrooki over the range 18-30 degrees C; however, sustained swimming performance was significantly lower in the warm- than the cool-acclimation group. For mating behaviour, we tested the hypothesis that acclimation would enhance the ability of female G. holbrooki to avoid forced matings at their host acclimation temperature relative to females acclimated to another environment. However, our hypothesis was not supported. The rate of copulations was almost three times greater for females acclimated to 30 degrees C than 18 degrees C when tested at 30 degrees C, indicating that they possess the ability to alter their avoidance behaviour to 'allow' more copulations in some environments. Coupled with previous studies, female G. holbrooki appear to have greater control on the outcome of coercive mating attempts than previously considered and can alter their propensity to receive forced matings following thermal acclimation. The significance of this change in female mating-avoidance behaviours with thermal acclimation remains to be explored.     

The behavioural thermal preference of the common triplefin (Forsterygion lapillum) tracks aerobic scope optima at the upper thermal limit of its distribution

Ocean temperatures are rising and fish are redistributing themselves poleward and into deeper waters to retain a favourable thermal environment (11 and 30). To investigate whether biogeographical shifts might occur through behavioural redistribution into optimal environments, we examined whether a common triplefin species (Forsterygion lapillum) would behaviourally select (i.e. track) a temperature that matches its physiological optimum under laboratory conditions. F. lapillum were acclimated to 15, 18 or 21 °C for at least 4 weeks, after which various rates of oxygen consumption (MO₂) were measured using automated respirometry and their behavioural thermal preferenda assessed using an electronic shuttle choice tank. Aerobic metabolic scope (resolved as the difference between maximal and maintenance MO₂) did not differ across all thermal treatments (i.e. specimens acclimated to 15, 18 or 21 °C) revealing that F. lapillum is a eurythermal species with a range of optimal physiological performance that closely matches the environmental conditions they are exposed to. A comparably wide range of behavioural preference would perhaps be expected but all three acclimation groups showed a surprisingly narrow behavioural preference range of 20–21 °C. The results therefore suggest that, irrespective of acclimation, eurythermal species may have a tendency to select optimal temperatures at the upper limit of their thermal distribution range. The results are discussed in the context of the ecology and the expected response of F. lapillum to future thermal change.     

Heat resistance throughout ontogeny: body size constrains thermal tolerance

Heat tolerance is a trait of paramount ecological importance and may determine a species' ability to cope with ongoing climate change. Although critical thermal limits have consequently received substantial attention in recent years, their potential variation throughout ontogeny remained largely neglected. We investigate whether such neglect may bias conclusions regarding a species' sensitivity to climate change. Using a tropical butterfly, we found that developmental stages clearly differed in heat tolerance. It was highest in pupae followed by larvae, adults and finally eggs and hatchlings. Strikingly, most of the variation found in thermal tolerance was explained by differences in body mass, which may thus impose a severe constraint on adaptive variation in stress tolerance. Furthermore, temperature acclimation was beneficial by increasing heat knock‐down time and therefore immediate survival under heat stress, but it affected reproduction negatively. Extreme temperatures strongly reduced survival and subsequent reproductive success even in our highly plastic model organism, exemplifying the potentially dramatic impact of extreme weather events on biodiversity. We argue that predictions regarding a species' fate under changing environmental conditions should consider variation in thermal tolerance throughout ontogeny, variation in body mass and acclimation responses as important predictors of stress tolerance.     

Thermal acclimation of swimming performance in newt larvae: the influence of diel temperature fluctuations during embryogenesis

1.  Thermal acclimation is one of the basic strategies by which organisms cope with thermal heterogeneity of the environment. Under predictable variation in environmental temperatures, theory predicts that selection favours acclimation of thermal performance curves over fixed phenotypes.
2.  We examined the influence of diel fluctuations in developmental temperatures on the thermal sensitivity of the maximal swimming capacity in larvae of the alpine newt, Triturus alpestris .
3.  We incubated newt eggs under three thermal regimes with varying daily amplitudes (1, 5 and 9 °C) and similar means (17·6–17·9 °C), and accordingly we measured the swimming speed of hatched larvae at three experimental temperatures (12, 17 and 22 °C), which they would normally experience in their natural habitat.
4.  Embryonic development under low and middle temperature fluctuations produced larvae with similar swimming speeds across experimental temperatures. In contrast, the most fluctuating regime induced development of phenotypes, which at 12 °C swam faster than larvae developed under moderate diel fluctuations.
5.  Our results provide evidence that diel temperature fluctuations induce acclimation of thermal dependence of locomotor performance. In ectotherms experiencing diel cycles in environmental temperatures, this plastic response may act as an important pacemaker in the evolution of thermal sensitivity.     

Does developmental acclimatization reduce the susceptibility to predation in newt larvae?

Many organisms respond to the heterogeneity of abiotic environmental conditions by plastic modifications of their phenotypes (acclimation or acclimatization). Despite considerable research efforts in this area, the beneficial (adaptive) effect of acclimation or acclimatization is still debated. We examined whether the development of newt larvae (Ichthyosaura alpestris) under different natural light and thermal conditions subsequently altered their susceptibility to predation in sun‐exposed versus shaded tanks in nature. During predation trials in various light and temperature conditions, newt larvae that developed in sun‐exposed warmer tanks consistently suffered from higher predation by dragonfly nymphs (Aeshna cyanea) compared to larvae from shaded or colder tanks. We conclude that higher sun exposure during embryonic and larval development negatively affects antipredator performance even in sun‐exposed tanks: this result is inconsistent with the beneficial acclimation hypothesis. © 2012 The Linnean Society of London, Biological Journal of the Linnean Society, 2012, ●● , ●●–●●.     

Microgeographical variation in thermal preference by an amphibian

Ectotherms use behaviour to buffer effects of temperature on growth, development and survival. While behavioural thermoregulation is widely reported, localized adaptation of thermal preference is poorly documented. Larval amphibians live in wetlands ranging from entirely open to heavily shaded by vegetation. We hypothesized that populations undergo localized selection leading to countergradient patterns of thermal preference behaviour. Specifically, we predicted that wood frog (Rana sylvatica) larvae from closed canopy ponds would be more strongly temperature selective and would prefer higher temperatures than conspecifics from populations found in open canopy ponds. In a study of six breeding ponds in north‐eastern Connecticut, USA, these predictions were upheld. The countergradient, microgeographical variation in thermal preference documented here implies that wood frog populations may have diverged rapidly in the face of contrasting selection pressures. Rapid, behaviourally mediated responses to changing thermal environments have important implications for understanding population responses to climate change.     

Thermal limits of wild and laboratory strains of two African malaria vector species, <Emphasis Type="Italic">Anopheles arabiensis</Emphasis> and <Emphasis Type="Italic">Anopheles funestus</Emphasis>

ABSTRACT: Malaria affects large parts of the developing world and is responsible for almost 800,000 deaths annually. As climates change, concerns have arisen as to how this vector-borne disease will be impacted by changing rainfall patterns and warming temperatures. Despite the importance and controversy surrounding the impact of climate change on the potential spread of this disease, little information exists on the tolerances of several of the vector species themselves. METHODS: Using a ramping protocol (to assess critical thermal limits - CT) and plunge protocol (to assess lethal temperature limits - LT) information on the thermal tolerance of two of Africa's important malaria vectors, Anopheles arabiensis and Anopheles funestus was collected. The effects of age, thermal acclimation treatment, sex and strain (laboratory versus wild adults) were investigated for CT determinations for each species. The effects of age and sex for adults and life stage (larvae, pupae, adults) were investigated for LT determinations. RESULTS: In both species, females are more tolerant to low and high temperatures than males; larvae and pupae have higher upper lethal limits than do adults. Thermal acclimation of adults has large effects in some instances but small effects in others. Younger adults tend to be more tolerant of temperature changes than older age groups. Long-standing laboratory colonies are sufficiently similar in thermal tolerance to field-collected animals to provide reasonable surrogates when making inferences about wild population responses. Differences between these two vectors in their thermal tolerances, especially in larvae and pupae, are plausibly a consequence of different habitat utilization. CONCLUSIONS: Limited plasticity is characteristic of the adults of these vector species relative to others examined to date, suggesting limited scope for within-generation change in thermal tolerance. These findings and the greater tolerance of females to thermal extremes may have significant implications for future malaria transmission, especially in areas of current seasonal transmission and in areas on the boundaries of current vector distribution.     

Thermoregulatory behaviour explains countergradient variation in the upper thermal limit of a rainforest skink

The vulnerability of a terrestrial ectotherm to high environmental temperatures depends on the animal's thermal physiology and thermoregulatory behaviour. These variables – environment, physiology, and behaviour – interact with each other, complicating assessment of species vulnerability to global warming. We previously uncovered a counterintuitive pattern in rainforest sunskinks Lampropholis coggeri: a negative relationship between their critical thermal maximum (CT_max) and the temperature of their environment. Could this result be explained by a three‐way interaction between environment, physiology, and behaviour? Here we find that sunskink thermal preference is correlated positively with CT_max, but, importantly, skinks from hotter environments prefer lower temperatures than conspecifics from cooler environments. In an acclimation experiment, we find that CT_max is plastic and shifts in alignment with acclimation temperature. We also found heritable variation in this trait in a common garden study, but this variation was small relative to the plastic shifts observed in CT_max. Thus, our previous observation of a negative correlation between field CT_max and temperature is explained, at least in part, by the lizard's thermoregulatory behaviour: lizards from hot environments preferentially choose cool microenvironments, and their physiology acclimates to these cooler experienced temperatures. Our results suggest that behavioural adjustments to the environment can produce countergradient variation in physiological traits. More broadly, our work underscores the importance of interactions between environment, behaviour, and physiology in ectotherms. Understanding these interactions will be crucial in assessing vulnerability to climate change.     

Thermal acclimation in the microcrustacean Daphnia: a survey of behavioural, physiological and biochemical mechanisms

Thermal acclimation in Daphnia magna was studied on various levels to test the recent “oxygen-limited thermal tolerance” hypothesis. Preference behaviour in a thermal gradient was determined by both, ambient temperature and corresponding oxygen concentration. Swimming activity depended on aerobic energy provision and reflected the match or mismatch of oxygen supply and energy demand at different ambient temperatures. Thermal acclimation modified both types of behaviour and more slightly heat tolerance. Perfusion and haemoglobin properties turned out to be central control variables to adapt oxygen transport to varying energy demands at different ambient temperatures. Exceptional advantages of Daphnia as an experimental model organism allowed to confirm on a behavioural, physiological and biochemical level that thermal acclimation is strongly based on the adaptation of oxygen transport allowing unidirectional shifts of the thermal tolerance range to warmer or colder temperatures.     

Effects of inbreeding on behavioural plasticity of parent–offspring interactions in a burying beetle

Inbreeding depression is defined as a fitness decline in progeny resulting from mating between related individuals, the severity of which may vary across environmental conditions. Such inbreeding‐by‐environment interactions might reflect that inbred individuals have a lower capacity for adjusting their phenotype to match different environmental conditions better, as shown in prior studies on developmental plasticity. Behavioural plasticity is more flexible than developmental plasticity because it is reversible and relatively quick, but little is known about its sensitivity to inbreeding. Here, we investigate effects of inbreeding on behavioural plasticity in the context of parent–offspring interactions in the burying beetle Nicrophorus vespilloides. Larvae increase begging with the level of hunger, and parents increase their level of care when brood sizes increase. Here, we find that inbreeding increased behavioural plasticity in larvae: inbred larvae reduced their time spent associating with a parent in response to the length of food deprivation more than outbred larvae. However, inbreeding had no effect on the behavioural plasticity of offspring begging or any parental behaviour. Overall, our results show that inbreeding can increase behavioural plasticity. We suggest that inbreeding‐by‐environment interactions might arise when inbreeding is associated with too little or too much plasticity in response to changing environmental conditions.     

Poor Nutritional Conditions During the Early Larval Stage Reduce Risk‐Taking Activities of Fire Salamander Larvae (Salamandra salamandra)

Environmental conditions experienced early in life have been shown to significantly affect growth trajectories at later stages in many vertebrate species. Amphibians typically have a biphasic life history, with an aquatic larval phase during early development and a subsequent terrestrial adult phase after completed metamorphosis. Thus, the early conditions have an especially strong impact on the future survival and fitness of amphibians. We studied whether early nutritional conditions affect the behavioural reaction of fire salamander larvae (Salamandra salamandra) before completion of metamorphosis. Fire salamander larvae reared under rich nutritional conditions were heavier and larger, displayed better body condition overall throughout the first three month of life and metamorphosed earlier compared with larvae raised under poor nutritional conditions. Specifically, we tested whether larvae reared under these different conditions differed with respect to their risk‐taking behaviour and activity. We found no differences in the activity of larvae with respect to their experienced early food conditions. However, larvae reared under poor nutritional conditions hid significantly more often in a risk‐taking test than larvae reared under rich food conditions. This increase in shelter‐seeking behaviour might be an adaptation to reduce the risk of larval drift or an adaptation to compensate for physiological deficits in part by appropriate behavioural reactions. Our results indicate that environmental conditions, such as food availability, may lead to different behavioural strategies.     

Thermal acclimation in a complex life cycle: The effects of larval and adult thermal conditions on metabolic rate and heat resistance in Culex pipiens (Diptera: Culicidae)

It has now been well established that insects can respond to variation in their environment via acclimation, yet the extent of the response varies among populations and environmental characteristics. One under-investigated theme which may contribute to this variation concerns acclimation effects across the life cycle. The present study explores how acclimation in the larval stage of Culex pipiens affects thermal relations in the adult stage. Mosquitoes were reared in a full factorial design at 18 or 26 °C as larvae and adults, then critical thermal maxima (CT_max) and metabolic rate–temperature relationships (MR–T) were determined for all 4 treatments. CT_max was positively affected by both larval and adult acclimation treatments. MR–T slope was significantly affected only by adult treatment: warm acclimated adults had on average shallower slopes and higher y-intercepts than cool acclimated ones. These results demonstrate that larval acclimation effects can alter adult phenotypes in a species whose life cycle includes two drastically different environments, an aquatic and a terrestrial stage. Studying insects with complex life cycles, especially those with aquatic or subterranean larval stages, can provide valuable information on the effects of thermal variability and predictability on phenotypic plasticity.     

Physiological and behavioural responses to seasonal changes in environmental temperature in the Australian spiny crayfish Euastacus sulcatus

The strategies used by ectotherms to minimise the detrimental effects of suboptimal thermal environments on physiological performance are often related to whether they inhabit a terrestrial or aquatic environment. Most terrestrial ectotherms use thermoregulatory strategies to maintain body temperature within an optimal range, while many aquatic ectotherms utilise thermal acclimation to maintain performance over varying seasonal temperatures. This study aimed to elucidate the relative contributions of acclimation and behavioural thermoregulation to maintaining whole-animal performance over varying seasonal temperatures in the semi-terrestrial Lamington spiny crayfish (Euastacus sulcatus). Crayfish activity and surface temperatures were determined by means of radio tracking and behavioural observations. Field studies demonstrated that E. sulcatus is exposed to stable daily temperatures, varying only between seasons from 10°C in late winter to over 20°C in summer. Also, terrestrial behaviour corresponded to a small portion of crayfish time (1.13%), much lower than predicted, indicating that E. sulcatus has limited opportunity for behavioural thermoregulation. We also tested the effect of acclimation to either 10 or 20°C on chela strength and stamina. We found acclimation had a more marked effect on chela stamina than maximum strength measures; however, overall acclimatory capacity was limited in E. sulcatus. Thus, we found that the semi-terrestrial crayfish E. sulcatus used neither thermoregulatory behaviours nor physiological strategies to deal with seasonal changes in environmental temperature.     

Differential responses of thermal tolerance to acclimation in the sub-Antarctic rove beetle Halmaeusa atriceps

Abstract. Investigations of the responses to acclimation of upper and lower lethal limits and limits to activity in insects have focused primarily on Drosophila. In the present study, Halmaeusa atriceps (Staphylinidae) is examined for thermal tolerance responses to acclimation, and seasonal acclimatization. In summer and winter, lower lethal temperatures of adults and larvae are approximately −7.6 ± 0.03 and −11.1 ± 0.06 °C, respectively. Supercooling points (SCPs) are more variable, with winter SCPs of −5.4 ± 0.4 °C in larvae and −6.3 ± 0.8 °C in adults. The species appears to be chill susceptible in summer and moderately freeze tolerant in winter, thus showing seasonal acclimatization. Similar changes cannot be induced solely by acclimation to low temperatures in the laboratory. Upper lethal temperatures show a weaker response to acclimation. There are also significant responses to acclimation of critical thermal limits. Critical thermal minima vary between −3.6 ± 0.2 and −0.6 ± 0.2 °C in larvae, and from −4.1 ± 0.1 to −0.8 ± 0.2 °C in adults. By contrast, critical thermal maxima vary much less within adults and larvae. These findings are in keeping with the general pattern found in insects, although this species differs in several respects from others found on Marion Island.     

Differences in the reproductive behaviour and larval development of two Canthon rutilans subspecies reinforce their thermal regional segregation

Two dung beetle subspecies of Canthon rutilans Castelnau (Coleoptera: Scarabaeidae, Scarabaeinae), C. rutilans rutilans and C. rutilans cyanescens, inhabit different environmental temperature conditions in southern Brazil. We developed a laboratory breeding experiment with 60 pairs of individuals of the two subspecies at five temperature conditions (from 15 to 35 °C) to compare the influence of temperature on the behaviour of adults and the development of larvae. The behavioural patterns of the adults in both subspecies differ according to temperature. The size of food balls was smaller and lighter in C. rutilans cyanescens. Although temperature did not influence the feeding behaviour (measured as the number of food balls made), reproductive behaviour (measured as the number of brood balls made by pair) was significantly lower at 15 °C for both subspecies. Besides that, brood balls from C. rutilans rutilans were bigger and heavier at lower temperatures. The number of offspring and the time of emergence depend on temperature too. However, the weight of the offspring and the longevity of adults depend on the subspecies and temperature treatment. These results demonstrate that the subspecies have different thermal adaptations: C. rutilans rutilans has reproductive behaviour adapted to living under colder and broader conditions than C. rutilans cyanescens.