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.     

Sexual differences rather than flight performance underlie movement and exploration in a tropical butterfly

1. Individual movement behaviour governs several routine processes, and may scale up to important ecological processes, including dispersal. However, movement is affected by a wealth of factors, including abiotic conditions, flight performance, and behavioural traits. Although it has been historically assumed that insect flight is in the first place ruled by physiology and morphology, researchers have only recently begun to understand the potentially important role of behavioural traits. 2. This study aims to disentangle the relative importance of thermal conditions during development, and especially flight performance (capacity), versus behaviour (intrinsic motivation) in relation to movement attributes (i.e. time until take‐off, number of positions visited) under controlled laboratory conditions in the tropical butterfly Bicyclus anynana. 3. As predicted, links were found between flight performance (forced flight) and morphological traits (body size). However, this link was less pronounced for movement and exploratory behaviour, suggesting a more pronounced role of intrinsic motivation on the actual decision to move, or not. Thus, flight performance and movement may not be intimately associated. 4. Flight behaviour was mainly determined by sexual differences, with males showing better flight performance, higher mobility, and enhanced exploration than females. 5. Lower developmental temperatures increased thorax–abdomen ratio, thorax mass, and exploratory behaviour, and decreased wing loading. This may potentially aid flight capacity under thermally challenging conditions. 6. This study adds to the growing evidence that behavioural traits should not be neglected when investigating movement and dispersal, as they may well play a crucially important role.     

Cod in hot water: observations of behaviour in relation to temperature

Fish behaviour varies considerably in response to changes in environmental and biological conditions. Cod ( Gadus morhua ) is not a homeothermic species and recent research has suggested that the recruitment and distribution of cod stocks may be influenced by temperature. Concerns have therefore been raised about the potential effect of climate change on stocks that are already at the southern limits of their range. We used data storage tags (DSTs) to observe the behaviour of cod in relation to temperature between 1999 and 2002. Over 3500 days of data were collected from 17 individuals tagged in the North and Irish Seas. We describe how the patterns in the temperature experience of cod are related to behavioural mechanisms, such as horizontal and vertical migration, that match habitat choice to physiological preferences. The results are discussed in the context of this behavioural response to short‐ and long‐term shifts in thermal regime and the potential consequences on the overall behaviour and distribution of cod stocks.     

Thermal ecology of Zonocerus variegatus and its effects on biocontrol using pathogens

1 Thermal behaviour of the variegated grasshopper, Zonocerus variegatus, was investigated in the humid tropical zone of southern Benin, west Africa, in the dry seasons of 1996 and 1998. In 1998, investigations included studies of a population of grasshoppers sprayed with an oil‐based formulation of the entomopathogenic fungus Metarhizium anisopliae var acridum. 2 Body temperature measurements and observations of thermal behaviour both in the field and on thermal gradients in the laboratory, suggest that Z. variegatus was not an active behavioural thermoregulator. Although it did show shade‐seeking behaviour at high temperatures, no overt behavioural postures or microhabitat selection associated with heat gain and elevation of body temperatures was observed. Moreover, no alterations to thermal behaviour were found in response to infection by Metarhizium. 3 Body temperatures exhibited by Z. variegatus in the field will lengthen disease incubation of M. anisopliae var acridum compared with laboratory maintained, constant temperature conditions and may have a significant impact on pathogens with a lower thermal tolerance. 4 Habitat structure appeared to be an important factor determining the extent of body temperature elevation. The effect of habitat differences on infection and growth of M. anisopliae var acridum and other entomopathogenic fungi is discussed.     

Behavioural effects of temperature on ectothermic animals: unifying thermal physiology and behavioural plasticity

Temperature imposes significant constraints on ectothermic animals, and these organisms have evolved numerous adaptations to respond to these constraints. While the impacts of temperature on the physiology of ectotherms have been extensively studied, there are currently no frameworks available that outline the multiple and often simultaneous pathways by which temperature can affect behaviour. Drawing from the literature on insects, we propose a unified framework that should apply to all ectothermic animals, generalizing temperature's behavioural effects into: (1) kinetic effects, resulting from temperature's bottom‐up constraining influence on metabolism and neurophysiology over a range of timescales (from short to long term), and (2) integrated effects, where the top‐down integration of thermal information intentionally initiates or modifies a behaviour (behavioural thermoregulation, thermal orientation, thermosensory behavioural adjustments). We discuss the difficulty in distinguishing adaptive behavioural changes from constraints when observing animals' behavioural responses to temperature. We then propose two complementary approaches to distinguish adaptations from constraints, and categorize behaviours according to our framework: (i) ‘kinetic null modelling’ of temperature's effects on behaviour; and (ii) behavioural ecology experiments using temperature‐insensitive mutants. Our framework should help to guide future research on the complex relationship between temperature and behaviour in ectothermic animals.     

Temporal plasticity in thermal‐habitat selection of burbot Lota lota a diel‐migrating winter‐specialist

In this study, animal‐borne telemetry with temperature sensors was coupled with extensive habitat temperature monitoring in a dimictic reservoir, to test the following hypotheses: behavioural thermoregulation occurs throughout the year and temperature selection varies on a diel and seasonal basis, in a winter‐specialist diel‐migrating fish. Burbot Lota lota demonstrated nightly behavioural thermoregulation throughout the year, with a large seasonal shift between selection for very cold temperatures (<2° C) optimal for reproduction during the spawning period and selection for warmer temperatures (12–14° C) optimal for hunting and feeding during non‐reproductive periods. During daylight hours, while L. lota avoided habitats warmer than optimal for reproduction and feeding during the spawning and non‐reproductive periods, respectively, active selection was limited to selection for 4–6° C habitat during the prespawning period. Although behavioural thermoregulation explained the night‐time migration, behavioural thermoregulation only partially explained daytime behaviour, indicating that diel migration is best explained by a combination of factors. Thus, thermal‐habitat selection was a good predictor of night‐time habitat occupancy in a diel‐migrating species. Together, these results show that thermal‐habitat selection by fishes may be important throughout the year and a more seasonally plastic behaviour than previously recognized.     

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.     

Does body size influence thermal biology and diet of a python (Morelia spilota imbricata)?

Current theory predicts that larger‐bodied snakes not only consume larger prey (compared with smaller individuals), but may also have a different range of prey available to them due to their thermal biology. It has been argued that smaller individuals, with lower thermal inertia (i.e. faster cooling rates at nightfall when air temperature falls and basking opportunities are limited), may be thermally restricted to foraging and hunting during the day on diurnally active prey, and have reduced capacity to hunt crepuscular and nocturnal prey species. This predictive theory was investigated by way of dietary analysis, assessment of thermal biology and thermoregulation behaviour in an ambush forager, the south‐west carpet python (Morelia spilota imbricata, Pythonidae). Eighty‐seven scats were collected from 34 individual pythons over a 3‐year radiotelemetry monitoring study. As predicted by gape size limitation, larger pythons took larger prey; however, 65% of prey items of small pythons were represented by nocturnally active, small mammals, a larger proportion than present in larger snakes. Several measures of thermal biology (absolute body temperature, thermal differential of body temperature to air temperature, maximum hourly heating and cooling rates) were not strongly affected by python body mass. Additionally, body temperature was only influenced by the behavioural choice of microhabitat selection and was not affected by python body size or position, suggesting that these behavioural choices do not allow smaller pythons to vastly increase their temporal foraging window. By coupling dietary analysis, measures of body temperature and behavioural observations of free‐ranging animals, we conclude that, contrary to theoretical predictions, a small body size does not thermally restrict the temporal window for ambush foraging in M. s. imbricata. An ontogenetic or size‐determined switch from ambush feeding to actively foraging on slower prey would account for the differences in prey taken by these animals. The concept of altered foraging behaviour warrants further investigation in this species.     

Beneficial acclimation and the Bogert effect

Few studies have examined the extent to which phenotypic plasticity in a given trait might be influenced by behavioural responses to an environmental cue. Regulatory behaviour might eliminate environmental variation such that little selection for physiological change would take place. Here, to test this Bogert effect on acclimation, we use two life-stages of a kelp fly that inhabit the same habitat, but differ profoundly in their behaviour. We predicted that when denied opportunities for behavioural regulation, mobile, though brachypterous adults would show a performance advantage in most thermal environments following acclimation to their preferred temperature(s). By contrast, in the less mobile larvae, that have a broader thermal preference, beneficial acclimation would be more evident. Ordered factor anova with orthogonal polynomial contrasts revealed that adults recovered faster from chill coma following any one of six short-term temperature treatments if they had been acclimated at low temperature, whilst larvae showed beneficial acclimation.     

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.     

Behavioural syndromes in Merriam's kangaroo rats (Dipodomys merriami): a test of competing hypotheses

Behavioural syndromes, correlations of behaviours conceptually analogous to personalities, have been a topic of recent attention due to their potential to explain trade-offs in behavioural responses, apparently maladaptive behaviour and limits to plasticity. Using Merriam's kangaroo rats (Dipodomys merriami), we assessed the explanatory power and generality of hypothesized syndrome structures derived from the literature and the natural history of the species. Several aspects of functionally distinct behavioural responses of D. merriami were quantified. Syndrome structures were compared using structural equation modelling and model selection procedures. A domain-general behavioural syndrome incorporating cross-functional relationships between measures of boldness, agonistic behaviour, flexibility and food hoarding best explained the data. This pattern suggests that D. merriami behaviours should not be viewed as discrete elements but as components of a multivariate landscape. Our results support arguments that a lack of independence between behaviours may be a general aspect of behavioural phenotypes and suggest that the ability of D. merriami's behaviour to respond to selection may be constrained by underlying connections.     

Evolutionary stasis and lability in thermal physiology in a group of tropical lizards

Understanding how quickly physiological traits evolve is a topic of great interest, particularly in the context of how organisms can adapt in response to climate warming. Adjustment to novel thermal habitats may occur either through behavioural adjustments, physiological adaptation or both. Here, we test whether rates of evolution differ among physiological traits in the cybotoids, a clade of tropical Anolis lizards distributed in markedly different thermal environments on the Caribbean island of Hispaniola. We find that cold tolerance evolves considerably faster than heat tolerance, a difference that results because behavioural thermoregulation more effectively shields these organisms from selection on upper than lower temperature tolerances. Specifically, because lizards in very different environments behaviourally thermoregulate during the day to similar body temperatures, divergent selection on body temperature and heat tolerance is precluded, whereas night-time temperatures can only be partially buffered by behaviour, thereby exposing organisms to selection on cold tolerance. We discuss how exposure to selection on physiology influences divergence among tropical organisms and its implications for adaptive evolutionary response to climate warming.     

Comparing the strength of behavioural plasticity and consistency across situations: animal personalities in the hermit crab Pagurus bernhardus

Many phenotypic traits show plasticity but behaviour is often considered the 'most plastic' aspect of phenotype as it is likely to show the quickest response to temporal changes in conditions or 'situation'. However, it has also been noted that constraints on sensory acuity, cognitive structure and physiological capacities place limits on behavioural plasticity. Such limits to plasticity may generate consistent differences in behaviour between individuals from the same population. It has recently been suggested that these consistent differences in individual behaviour may be adaptive and the term 'animal personalities' has been used to describe them. In many cases, however, a degree of both behavioural plasticity and relative consistency is probable. To understand the possible functions of animal personalities, it is necessary to determine the relative strength of each tendency and this may be achieved by comparison of statistical effect sizes for tests of difference and concordance. Here, we describe a new statistical framework for making such comparisons and investigate cross-situational plasticity and consistency in the duration of startle responses in the European hermit crab Pagurus bernhardus, in the field and the laboratory. The effect sizes of tests for behavioural consistency were greater than for tests of behavioural plasticity, indicating for the first time the presence of animal personalities in a crustacean model.     

Behavioural and physiological stress responses to handling in wild guanacos

Both ethology and physiology can provide insights about stress conditions in wild animals during handling. Lama guanicoe (guanaco) is the major large herbivore inhabiting arid zones in Argentina. Since 2005, the Payún Matrú Cooperative, a business established and run by native people, has captured and handled guanacos for shearing at Payunia Reserve, Mendoza Province, Argentina, to market the species’ fibre for clothing and other products. The aim of our study was to evaluate the behavioural and physiological stress responses to handling of wild guanacos during these shearing activities. We evaluated stress conditions in guanacos by monitoring the frequency of agonistic behaviour in the holding corrals, following capture, the rate of vocalisation and agonistic behaviour during handling, and by estimating cortisol levels in handled animals. Crowding increased agonistic behaviour; this appeared to be related to dominance conflicts between males in the corrals. Time of corralling increased rate of agonistic behaviour and vocalisations during handling. The rate of behavioural stress responses was negatively related to cortisol levels in males; which may be due to animal fatigue or because behavioural stress responses may help mitigate physiological stress responses. Incorporating our results into animal welfare practices could help reduce stress conditions in wild guanacos. Our results suggest that both behavioural and physiological responses are important measures of stress in handled animals, and that behavioural stress responses cannot be used as a simple surrogate for glucocorticoid levels.     

Physiological and hormonal control of thermal depression in the tiger snake, Notechis scutatus

Plasma sodium concentrations in field-caught Western tiger snakes, Notechis scutatus, from semi-arid Carnac Island (CI) varied seasonally, with snakes exhibiting significant hypernatraemia during summer and normal concentrations following autumn rain. In contrast, field-caught tiger snakes from a perennial fresh-water swamp (Herdsman Lake, HL) exhibited no significant increase in plasma sodium concentrations during summer. Laboratory-induced hypernatraemia caused thermal depression in both populations; there was a weak negative relationship between plasma sodium concentration and temperature selection that was significant for CI snakes. Hypernatraemia significantly elevated circulating concentrations of the neuropeptide arginine vasotocin (AVT) in both CI and HL snakes. CI snakes injected with a physiological dosage of AVT also evidenced thermal depression. Despite the positive correlation between AVT and both plasma sodium concentration and osmolality for laboratory snakes, field samples from CI snakes indicate that circulating levels of AVT may be influenced more by plasma osmolality than sodium levels. The data suggest that, in CI snakes, chronic dehydration in the field leads to hypernatraemia which may lead to elevated levels of AVT if plasma osmolality also increases. This will in turn invoke a depression in thermal behaviour that may improve the water economy and survival of snakes on semi-arid CI. Although HL snakes do not experience seasonal dehydration, physiological changes away from the stable homeostatic state appear to prompt the same behavioural shifts, illustrating the intrinsic nature of the thermal behaviour in different populations of the same species of snake.     

Behavioural thermoregulatory tactics in lacustrine brook charr, Salvelinus fontinalis

The need to vary body temperature to optimize physiological processes can lead to thermoregulatory behaviours, particularly in ectotherms. Despite some evidence of within-population phenotypic variation in thermal behaviour, the occurrence of alternative tactics of this behaviour is rarely explicitly considered when studying natural populations. The main objective of this study was to determine whether different thermal tactics exist among individuals of the same population. We studied the behavioural thermoregulation of 33 adult brook charr in a stratified lake using thermo-sensitive radio transmitters that measured hourly individual temperature over one month. The observed behavioural thermoregulatory patterns were consistent between years and suggest the existence of four tactics: two "warm" tactics with both crepuscular and finer periodicities, with or without a diel periodicity, and two "cool" tactics, with or without a diel periodicity. Telemetry data support the above findings by showing that the different tactics are associated with different patterns of diel horizontal movements. Taken together, our results show a clear spatio-temporal segregation of individuals displaying different tactics, suggesting a reduction of niche overlap. To our knowledge, this is the first study showing the presence of behavioural thermoregulatory tactics in a vertebrate.     

Brain size predicts behavioural plasticity in guppies (Poecilia reticulata): An experiment

Understanding how animal personality (consistent between‐individual behavioural differences) arises has become a central topic in behavioural sciences. This endeavour is complicated by the fact that not only the mean behaviour of individuals (behavioural type) but also the strength of their reaction to environmental change (behavioural plasticity) varies consistently. Personality and cognitive abilities are linked, and we suggest that behavioural plasticity could also be explained by differences in brain size (a proxy for cognitive abilities), since accurate decisions are likely essential to make behavioural plasticity beneficial. We test this idea in guppies (Poecilia reticulata), artificially selected for large and small brain size, which show clear cognitive differences between selection lines. To test whether those lines differed in behavioural plasticity, we reared them in groups in structurally enriched environments and then placed adults individually into empty tanks, where we presented them daily with visual predator cues and monitored their behaviour for 20 days with video‐aided motion tracking. We found that individuals differed consistently in activity and risk‐taking, as well as in behavioural plasticity. In activity, only the large‐brained lines demonstrated habituation (increased activity) to the new environment, whereas in risk‐taking, we found sensitization (decreased risk‐taking) in both brain size lines. We conclude that brain size, potentially via increasing cognitive abilities, may increase behavioural plasticity, which in turn can improve habituation to novel environments. However, the effects seem to be behaviour‐specific. Our results suggest that brain size likely explains some of the variation in behavioural plasticity found at the intraspecific level.     

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.     

Not in their genes: Phenotypic flexibility, behavioural traditions and cultural evolution in wild bonnet macaques

Phenotypic flexibility, or the within-genotype, context-dependent, variation in behaviour expressed by single reproductively mature individuals during their lifetimes, often impart a selective advantage to organisms and profoundly influence their survival and reproduction. Another phenomenon apparently not under direct genetic control is behavioural inheritance whereby higher animals are able to acquire information from the behaviour of others by social learning, and, through their own modified behaviour, transmit such information between individuals and across generations. Behavioural information transfer of this nature thus represents another form of inheritance that operates in many animals in tandem with the more basic genetic system. This paper examines the impact that phenotypic flexibility, behavioural inheritance and socially transmitted cultural traditions may have in shaping the structure and dynamics of a primate society — that of the bonnet macaque (Macaca radiata), a primate species endemic to peninsular India. Three principal issues are considered: the role of phenotypic flexibility in shaping social behaviour, the occurrence of individual behavioural traits leading to the establishment of social traditions, and the appearance of cultural evolution amidst such social traditions. Although more prolonged observations are required, these initial findings suggest that phenotypic plasticity, behavioural inheritance and cultural traditions may be much more widespread among primates than have previously been assumed but may have escaped attention due to a preoccupation with genetic inheritance in zoological thinking. This paper is dedicated with admiration and gratitude to the late Dr Raja Ramanna, a man who held all primates in great esteem.