The inhibitory effect of the fungal toxin, destruxin A, on behavioural fever in the desert locust

During an infection locusts behaviourally fever by seeking out higher environmental temperatures. This behaviour places the pathogen at sub-optimal growth temperatures while improving the efficiency of the immune system, thereby prolonging the lifespan of the host. It is therefore in the interest of the pathogen to either adapt to fever-like temperatures or to evolve mechanisms to interfere with, or inhibit fever. We investigated the behavioural fever response of desert locusts to two fungal pathogens. A prolonged fever was observed in locusts infected with Metarhizium acridum. However, fever was comparatively short-lived during infection with Metarhizium robertsii. In both cases restriction of thermoregulation reduced lifespan. Destruxin A (dtx A) produced by M. robertsii, but not M. acridum has previously been associated with the inhibition of the insect immune system. Injection of dtx A during infection with the fever-causing M. acridum inhibited fever and was particularly effective when administered early on in infection. Furthermore, locusts injected with dtx A were more susceptible to M. acridum infection. Therefore engineering M. acridum isolates currently used for locust biocontrol, to express dtx A may improve efficiency of control by interfering with fever.     

Impacts of fever on locust life-history traits: costs or benefits?

Fever, like other mechanisms for defence against pathogens, may have positive and negative consequences for host fitness. In ectotherms, fever can be attained through modified behavioural thermoregulation. Here we examine potential costs of behavioural fever by holding adult, gregarious desert locusts at elevated temperatures simulating a range of fever intensities. We found no effect of fever temperatures on primary fitness correlates of survival and fecundity. However, flight capacity and mate competition were reduced, although there was no relation between time spent at fever temperatures and magnitude of the response. While these effects could indicate a direct cost of fever, they are also consistent with a shift towards the solitaria phase state that, in a field context, could be considered an adaptive life-history response to limit the impact of disease. These conflicting interpretations highlight the importance of considering complex defence mechanisms and trade-offs in an appropriate ecological context.     

Behavioural fever in the Senegalese grasshopper, Oedaleus senegalensis, and its implications for biological control using pathogens

1. Thermoregulatory behaviour of the Senegalese grasshopper, Oedaleus senegalensis (Krauss), was investigated in the field following a spray application of an oil-based formulation of Metarhizium flavoviride Gams and Rozsypal in Niger, West Africa.
2. Measurements of environmental temperature, wind speed and solar radiation were made in conjunction with measurements of internal body temperatures of grasshoppers from a control (unsprayed) and treated plot using microthermocouples and hand-held thermometers. Grasshoppers were monitored for 4 days from the third day after application.
3. Oedaleus senegalensis utilized a range of thermoregulatory behaviours to maximize body temperatures during periods of low insolation and ambient temperature, and to minimize excessive heat loading during the hottest periods. Preferred body temperature of uninfected grasshoppers was 39 °C, with a range from 24 °C in the early morning to a high of 46 °C during periods of high insolation and ambient temperature.
4. Infected grasshoppers altered their thermoregulatory behaviour and showed a behavioural fever response to the pathogen. Preferred body temperatures of infected individuals were raised to a new set point of ≈ 42 °C. This is believed to be the first evidence for a behavioural fever in response to a microbial infection for any natural population. In the present study, its effects appeared to provide little therapeutic advantage to hosts infected following application. Preliminary evidence from other studies, however, indicates that modifications to host thermoregulation could be a significant constraint to the pathogen and may limit its impact under certain conditions.     

Inhibition of fungal growth in thermoregulating locusts,Locusta migratoria,infected by the fungus Metarhizium anisopliae var acridum

The locust, Locusta migratoria, has the capacity to develop a behavioural fever which reduces fungal infection by Metarhizium anisopliae var acridum. We investigated hemocyte and blastospore kinetics in infected insects under conditions that did or did not allow thermoregulation. Hemocyte concentrations were severely reduced in inoculated insects that did not thermoregulate but remained similar to those of controls in inoculated insects that were allowed to thermoregulate. Reductions in hemocyte counts were accompanied by an increase in the concentration of blastospores. In non-thermoregulating insects, circulating blastospores were first observed two days post-inoculation and had heavily colonized the hemolymph by day 5; in contrast, no blastospores were recovered from hemolymph of inoculated-thermoregulating insects. We used fluorescein isothiocyanate (FITC)-labelled silica beads to examine in vivo phagocytosis in thermoregulating and non-thermoregulating locusts. In the absence of fungus, a greater proportion of beads were engulfed by hemocytes in thermoregulating than in non-thermoregulating locusts early (4 and 24h) after bead injection, but the proportions were similar thereafter. In infected locusts, phagocytosis in non-thermoregulating insects was progressively impaired; such impairment, however, was not observed in challenged, thermoregulating insects. Our results suggest that thermoregulation helped keep fungal growth in check, apparently through the maintenance of hemocyte population levels and the direct inhibition of blastospore propagation by elevated temperatures.     

Behavioral thermoregulation in the migratory locust: a therapy to overcome fungal infection

We examined under laboratory conditions the thermopreference of the migratory locust, Locusta migratoria migratorioides, following infection by the entomopathogenic fungus Metarhizium anisopliae var. acridum and its influence on mycosis. Infected locusts raised their body temperature more frequently than healthy conspecifics through selection of high temperatures in a heat gradient. Thermoregulation did not, however, alter the frequency of feeding events nor the amount of food eaten by infected L. migratoria. A thermoregulation regime of a minimum of 4 h/day substantially increased survival of inoculated insects (by 85%). However, the therapeutic effect decreased when thermoregulation was delayed following inoculation of the pathogen. Thermoregulation reduced locust mortality but did not completely eliminate the fungus from infected hosts; the fungus grew and killed the insects when thermoregulation was interrupted. We suggest that periodic, short bouts of thermoregulation, when performed from the onset of infection and for an extended period of time, are sufficient to provide a therapeutic effect to infected hosts. Such thermoregulatory capacity of locusts may limit the potential of fungal pathogens as biological control agents under certain ecological conditions.     

House flies delay fungal infection by fevering: at a cost

1. Many ectothermic species have evolved the ability to invoke a ‘behavioural fever’ when infected with a pathogen. The relative costs and benefits of this response, however, have rarely been quantified. 2. The aim of this study was investigate the nature and consequences of behavioural fever in the house fly, Musca domestica L., in response to infection with a possible biocontrol agent, the fungal entomopathogen, Beauveria bassiana (Balsamo) Vuillemin. 3. It was found that infected flies preferred higher temperatures and allocated more effort to thermoregulation than uninfected flies. Flies could not overcome infection but the altered thermal behaviour allowed infected flies to extend their survival and to lay more eggs relative to infected flies maintained under constant conditions. However, flies allowed to fever had lower egg viability suggesting a possible cost. 4. Under the present experimental conditions, the putative costs and benefits fever balanced one another resulting in no net change in fitness. Fever did not, therefore, limit the control potential of the fungus. We discuss whether the costs and benefits of behavioural fever might differ in other ecological contexts.     

Fever and phenotype: transgenerational effect of disease on desert locust phase state

Natural enemy attack can cause transgenerational shifts in phenotype such that offspring are less vulnerable to future attack. Desert locusts (Schistocerca gregaria) show density‐dependent variation in their resistance to pathogens, such that they are less vulnerable to pathogens when in the high‐density gregarious phase state (when they would probably be more exposed to pathogens) than when in the solitarious phase state. We therefore hypothesized that infected gregarious parents would maintain this phenotype in their offspring. We infected gregarious desert locust nymphs with the fungal pathogen Metarhizium anisopliae var. acridum, and allowed them to survive to reproduction by means of behavioural fever. The phase state of the locust offspring was assessed by their colouration and behavioural assays. Contrary to our hypothesis, we found an increase in solitarization in the infected population (14.6% solitarious offspring from infected parents, vs. <2% from uninfected counterparts at equivalent density). In a second experiment, we simulated behavioural fever temperatures and obtained a similar result (13.6% solitarious offspring vs. 4.4% from controls), implying that the phenomenon is probably a side‐effect of the hosts’ fever response. Identification of this novel environmental factor affecting locust phase state could have important implications for the biological control of these major pests.     

Thermal biology of the meadow grasshopper, Chorthippus parallelus, and the implications for resistance to disease

Abstract.  1. The thermal biology of the meadow grasshopper, Chorthippus parallelus , a common, habitat generalist acridid species found in the U.K., was characterised and the influence of thermoregulatory behaviour for resistance against a temperate ( Beauveria bassiana ) and tropical ( Metarhizium anisopliae var. acridum ) fungal pathogen was determined.
2.  Chorthippus parallelus was found to be an active behavioural thermoregulator, with a preferred temperature range of 32–35 °C.
3. Both pathogens proved lethal to fifth instar and adult grasshoppers. No evidence of behavioural fever in response to infection by either pathogen was found, but normal thermoregulation was found to reduce virulence and spore production of B. bassiana. Normal thermoregulation did not appear to affect M. anisopliae var. acridum .
4. These results suggest that the effects of temperature on host resistance depend on the thermal sensitivity of the pathogen and, in this case, derive from direct effects of temperature on pathogen growth rather than indirect effects mediated by host immune response.
5. The implications for possible risks of exotic pathogens and influence of climate change are discussed.     

Plasticity of preferred body temperatures as means of coping with climate change?

Thermoregulatory behaviour represents an important component of ectotherm non-genetic adaptive capacity that mitigates the impact of ongoing climate change. The buffering role of behavioural thermoregulation has been attributed solely to the ability to maintain near optimal body temperature for sufficiently extended periods under altered thermal conditions. The widespread occurrence of plastic modification of target temperatures that an ectotherm aims to achieve (preferred body temperatures) has been largely overlooked. I argue that plasticity of target temperatures may significantly contribute to an ectotherm's adaptive capacity. Its contribution to population persistence depends on both the effectiveness of acute thermoregulatory adjustments (reactivity) in buffering selection pressures in a changing thermal environment, and the total costs of thermoregulation (i.e. reactivity and plasticity) in a given environment. The direction and magnitude of plastic shifts in preferred body temperatures can be incorporated into mechanistic models, to improve predictions of the impact of global climate change on ectotherm populations.     

Deposition of pathogenic Mycoplasma gallisepticum onto bird feeders: host pathology is more important than temperature-driven increases in food intake

Although ambient temperature has diverse effects on disease dynamics, few studies have examined how temperature alters pathogen transmission by changing host physiology or behaviour. Here, we test whether reducing ambient temperature alters host foraging, pathology and the potential for fomite transmission of the bacterial pathogen Mycoplasma gallisepticum (MG), which causes seasonal outbreaks of severe conjunctivitis in house finches (Haemorhous mexicanus). We housed finches at temperatures within or below the thermoneutral zone to manipulate food intake by altering energetic requirements of thermoregulation. We predicted that pathogen deposition on bird feeders would increase with temperature-driven increases in food intake and with conjunctival pathology. As expected, housing birds below the thermoneutral zone increased food consumption. Despite this difference, pathogen deposition on feeders did not vary across temperature treatments. However, pathogen deposition increased with conjunctival pathology, independently of temperature and pathogen load, suggesting that MG could enhance its transmission by increasing virulence. Our results suggest that in this system, host physiological responses are more important for transmission potential than temperature-dependent alterations in feeding. Understanding such behavioural and physiological contributions to disease transmission is critical to linking individual responses to climate with population-level disease dynamics.     

Microclimate limits thermal behaviour favourable to disease control in a nocturnal amphibian

While epizootics increasingly affect wildlife, it remains poorly understood how the environment shapes most host–pathogen systems. Here, we employ a three‐step framework to study microclimate influence on ectotherm host thermal behaviour, focusing on amphibian chytridiomycosis in fire salamanders (Salamandra salamandra) infected with the fungal pathogen Batrachochytrium salamandrivorans (Bsal). Laboratory trials reveal that innate variation in thermal preference, rather than behavioural fever, can inhibit infection and facilitate salamander recovery under humidity‐saturated conditions. Yet, a 3‐year field study and a mesocosm experiment close to the invasive Bsal range show that microclimate constraints suppress host thermal behaviour favourable to disease control. A final mechanistic model, that estimates range‐wide, year‐round host body temperature relative to microclimate, suggests that these constraints are rule rather than exception. Our results demonstrate how innate host defences against epizootics may remain constrained in the wild, which predisposes to range‐wide disease outbreaks and population declines.     

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.     

Eicosanoid involvement in the regulation of behavioral fever in the desert locust,Schistocerca gregaria

The desert locust Schistocerca gregaria behaviorally thermoregulates in order to try and maintain a favoured "set point" body temperature. Locusts infected with the deuteromycete fungal pathogen Metarhizium anisopliae var acridumchoose a significantly elevated temperature. This "behavioral fever" greatly delays the progress of mycosis. We have confirmed this phenomenon and shown that desert locusts also fever when infected with the bacterial pathogen Serratia marcescens. Elevation in the prefered environmental temperature occurs also upon injection with laminarin and lipopolysaccharide (microbial cell wall components). Since such treatments also stimulate the immune system it would appear that "behavioral fever" is probably a feature of the immune response. The eicosanoid biosynthesis inhibitor dexamethasone prevented laminarin invoked fever. This effect was reversable by arachidonic acid. Therefore in common with the febrile response in mammals behavioral fever in insects may be mediated locally by circulating eicosanoids.     

Physiology of temperature regulation: comparative aspects

Few environmental factors have a larger influence on animal energetics than temperature, a fact that makes thermoregulation a very important process for survival. In general, endothermic species, i.e., mammals and birds, maintain a constant body temperature (Tb) in fluctuating environmental temperatures using autonomic and behavioural mechanisms. Most of the knowledge on thermoregulatory physiology has emerged from studies using mammalian species, particularly rats. However, studies with all vertebrate groups are essential for a more complete understanding of the mechanisms involved in the regulation of Tb. Ectothermic vertebrates-fish, amphibians and reptiles-thermoregulate essentially by behavioural mechanisms. With few exceptions, both endotherms and ectotherms develop fever (a regulated increase in Tb) in response to exogenous pyrogens, and regulated hypothermia (anapyrexia) in response to hypoxia. This review focuses on the mechanisms, particularly neuromediators and regions in the central nervous system, involved in thermoregulation in vertebrates, in conditions of euthermia, fever and anapyrexia.     

Altitudinal variation in behavioural thermoregulation: local adaptation vs. plasticity in California grasshoppers

We investigated the adaptive significance of behavioural thermoregulation in univoltine populations of the grasshopper Melanoplus sanguinipes along an altitudinal gradient in California using laboratory tests of animals raised under different temperatures. Trials consisted of continuous body temperature measurements with semi-implanted microprobes in a test arena, and observation and simultaneous recording of behavioural responses. These responses included mobility, basking and orientation of the body axes (aspect angle) towards a radiation source. Mobility and basking are determined by the altitudinal origin of the parental generation and not by the temperature treatments. With increasing altitude, individuals tend increasingly to raise body temperatures via mobility and increased basking. In contrast, body orientation towards the radiation source is influenced by the temperature treatments but not by the altitude of origin. Individuals experiencing higher temperatures during rearing show a lower tendency to lateral flanking. We conclude that body orientation responses are not adapted locally. In contrast other components of the behavioural syndrome that increase body temperature, such as mobility and basking, are adaptive in response to local selection pressure. The thermoregulatory syndrome of these grasshoppers is an important contribution to life-history adaptations that appropriately match season lengths.     

Thermoregulatory behaviour in Tropidurus torquatus (Squamata, Tropiduridae) from Brazilian coastal populations: an estimate of passive and active thermoregulation in lizards

Geographical variation in the degree of thermoregulatory behaviour of the lizard Tropidurus torquatus was studied in 10 restinga populations along approximately 1500 km of Brazilian coast. An index of thermoregulation was estimated using the difference between body and environmental (air and substrate) temperatures and the percentage of negative values for these differences (proportion of body temperatures lower than environmental temperatures). In most populations, the lizards primarily used active thermoregulation, through behavioural means, and mainly in relation to substrate temperatures. Along the restingas, the degree of active thermoregulation increased as a function of the increase in the local environmental temperatures along the restingas. Behavioural thermoregulation of T. torquatus helps the lizards to maintain their body temperatures within an optimal range in which to perform their normal daily activities.     

爬行动物胚胎的行为热调节

行为热调节是外温动物体温调节的主要方式。传统观点认为行为热调节仅存在于胚后阶段,然而近年来研究表明爬行动物胚胎具备行为热调节能力。本文回顾了爬行动物胚胎行为热调节的发现和研究进展,探讨了胚胎行为热调节的生态适应意义,分析了胚胎如何感知温度以完成行为热调节,指出了该领域的未来研究方向。     

Emerging disease of amphibians cured by elevated body temperature

The emerging infectious disease chytridiomycosis is thought to have contributed to many of the recent alarming declines in amphibian populations. Mortalities associated with these declines have often occurred during cooler seasons and at high elevations, suggesting that environmental temperature may be an important factor in disease emergence. We found that thermal environment affects the progress of the disease, and that housing frogs Litoria chloris at an environmental temperature of 37 degrees C for less than 16 h can clear them of the chytrid pathogen Batrachochytrium dendrobatidis. Our experiment demonstrated that elevated body temperatures similar to those experienced in behavioral fever and during normal thermoregulation can clear frogs of chytrid infection; therefore, variation in thermoregulatory opportunities and behaviors are likely to contribute to the differences in disease incidence observed among host species, populations, and regions. Although further refinement of the technique is needed to encompass various host species, appropriately applied thermal manipulations of amphibians and their enclosures may prove to be a safe and effective way of eliminating the fungal pathogen from captive amphibian populations and: preventing accidental spread of the pathogen when animals are translocated or released from captivity.     

Behavioral models of hydrothermal regulation in anurans: A field study in the Atlantic Forest,Brazil

Anurans rely on different microhabitats and microclimates for hydro-thermoregulation, which is an important physiological property for locomotor performance, body temperature, water flux, and pathogen defense. We ask whether microhabitat scouting is related to physiological states, specifically if microhabitat choice benefits the production of behavioral fever (e.g., increasing body temperature by selecting warmer places) or sickness behavior (e.g., inactivity and anorexia). We investigated how thermoregulatory behaviors affect hydro-thermoregulation in anurans, using agar models as a sampling unit, simulating four behaviors related to behavioral fever and sickness behavior. We compared the models' hydro-thermal balance in two different environments (wet and transitional forests). We showed that the wet forest was warmer and more stable than transitional forest and the agar models in the wet forest were warmer. Still, the four behavioral simulations exhibited similar average temperatures during the five-day study period in both forests. However, the apathetic behavior models had the lowest daily temperatures. The percentage hydration across models was higher in the wet forest, and daily variation in water loss for each behavioral simulation was higher in the transitional forest. Nevertheless, when limiting the analysis to the warmest times (1000–1600 h), apathetic behavior models lost less water than the others in both forests. We showed that different forests provide microclimatic variation for understory anurans, but different thermoregulatory behaviors may lead to similar body temperatures. Therefore, the Atlantic Forest offers different microclimates and thermoregulation options for anurans, as some species could develop behavioral fever while others demonstrate sickness behavior. Abstract in Portuguese is available with online material.