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Warming winters will change patterns of behaviour in temperate and polar arthropods, but we know little about the drivers of winter activity in animals such as ticks. Any changes in behaviour are likely to arise from a combination of both abiotic (e.g. temperature) and biotic (e.g. infection) drivers, and will have important consequences for survival and species interactions. Blacklegged ticks, Ixodes scapularis, have invaded Atlantic Canada and high proportions (30-50%) are infected with the bacteria causing Lyme disease, Borrelia burgdorferi. Infection is correlated with increased overwintering survival of adult females, and ticks are increasingly active in the winter, but it is unclear if infection is associated with activity. Further, we know little about how temperature drives the frequency of winter activity. Here, we exposed wild-caught, adult, female Ixodes scapularis ticks to three different winter temperature regimes (constant low temperatures, increased warming, and increased warming + variability) to determine the thermal and infection conditions that promote or suppress activity. We used automated behaviour monitors to track daily activity in individual ticks and repeated the study with fresh ticks over three years. Following exposure to winter conditions we determined whether ticks were infected with the bacteria B. burgdorferi and if infection was responsible for any patterns in winter activity. Warming conditions promoted increased activity throughout the overwintering period but infection with B. burgdorferi had no impact on the frequency or overall number of ticks active throughout the winter. Individual ticks varied in their levels of activity throughout the winter, such that some were largely dormant for several weeks, while others were active almost daily; however, we do not yet know the drivers behind this individual variation in behaviour. Overall, warming winters will heighten the risk of tick-host encounters., Competing Interests: Declaration of competing interest The authors declare no competing interests., (Copyright © 2024 The Authors. Published by Elsevier Ltd.. All rights reserved.)

The tick, Ixodes scapularis, vectors pathogens such as Borrelia burgdorferi, the bacterium that causes Lyme disease. Over the last few decades I. scapularis has expanded its range, introducing a novel health threat into these areas. Warming temperatures appear to be one cause of its range expansion to the north. However, other factors are also involved. We show that unfed adult female ticks infected with B. burgdorferi have greater overwintering survival than uninfected female ticks. Locally collected adult female ticks were placed in individual microcosms and allowed to overwinter in both forest and dune grass environments. In the spring we collected the ticks and tested both dead and living ticks for B. burgdorferi DNA. Infected ticks had greater overwintering survival compared with uninfected ticks every winter for three consecutive winters in both forest and dune grass environments. We discuss the most plausible explanations for this result. The increased winter survival of adult female ticks could enhance tick population growth. Our results suggest that, in addition to climate change, B. burgdorferi infection itself may be promoting the northern range expansion of I. scapularis. Our study highlights how pathogens could work synergistically with climate change to promote host range expansion., (© 2023 The Authors. Insect Science published by John Wiley & Sons Australia, Ltd on behalf of Institute of Zoology, Chinese Academy of Sciences.)

The parasitic wasp Cotesia congregata suppresses feeding in its host, the caterpillar Manduca sexta, during specific periods of wasp development. We examined both feeding behaviour and the neurophysiology of the mandibular closer muscle in parasitized and unparasitized control M. sexta to determine how the wasp may accomplish this. To test whether the wasps activated a pre-existing host mechanism for feeding cessation, we examined the microstructure of feeding behaviour in caterpillars that stopped feeding due to illness-induced anorexia or an impending moult. These microstructures were compared with that shown by parasitized caterpillars. While there were overall differences between parasitized and unparasitized caterpillars, the groups showed similar progression in feeding microstructure as feeding ended, suggesting a common pattern for terminating a meal. Parasitized caterpillars also consumed less leaf area in 100 bites than control caterpillars at around the same time their feeding microstructure changed. The decline in food consumption was accompanied by fewer spikes per burst and shorter burst durations in chewing muscle electromyograms. Similar extracellular results were obtained from the motorneuron of the mandibular closer muscle. However, chewing was dramatically re-activated in non-feeding parasitized caterpillars if the connectives posterior to the suboesophageal ganglion were severed. The same result was observed in unparasitized caterpillars given the same treatment. Our results suggest that the reduced feeding in parasitized caterpillars is not due to damage to the central pattern generator (CPG) for chewing, motor nerves or chewing muscles, but is more likely to be due to a suppression of chewing CPG activity by ascending or descending inputs., Competing Interests: Competing interests The authors declare no competing or financial interests., (© 2023. Published by The Company of Biologists Ltd.)

Although skeletal muscle is a specialized tissue that provides the motor for movement, it also participates in other functions, including the immune response. However, little is known about the effects of this multitasking on muscle. We show that muscle loses some of its capacity while it is participating in the immune response. Caterpillars (Manduca sexta) were exposed to an immune challenge, predator stress or a combination of immune challenge and predator stress. The expression of immune genes (toll-1, domeless, cactus, tube and attacin) increased in body wall muscle after exposure to an immune challenge. Muscle also showed a reduction in the amount of the energy storage molecule glycogen. During an immune challenge, the force of the defensive strike, an important anti-predator behaviour in M. sexta, was reduced. Caterpillars were also less able to defend themselves against a common enemy, the wasp Cotesia congregata, suggesting that the effect on muscle is biologically significant. Our results support the concept of an integrated defence system in which life-threatening events activate organism-wide responses. We suggest that increased mortality from predation is a non-immunological cost of infection in M. sexta. Our study also suggests that one reason non-immunological costs of infection exist is because of the participation of diverse organs, such as muscle, in immunity., Competing Interests: Competing interests The authors declare no competing or financial interests., (© 2023. Published by The Company of Biologists Ltd.)

Insects are critical to our ecosystems, but we do not fully understand their future in our warming world. Rising temperatures are affecting insect physiology in myriad ways, including changes to their immune systems and the ability to fight infection. Whether predicted changes in temperature will contribute to insect mortality or success, and the role of disease in their future survival, remains unclear. Although heat can enhance immunity by activating the integrated defense system (e.g. via the production of protective molecules such as heat-shock proteins) and accelerating enzyme activity, heat can also compromise the immune system through energetic-resource trade-offs and damage. The responses to heat are highly variable among species. The reasons for this variability are poorly known, and we are lagging in our understanding of how and why the immune system responds to changes in temperature. In this Commentary, we highlight the variation in insect immune responses to heat and the likely underlying mechanisms. We suggest that we are currently limited in our ability to predict the effects of rising temperatures on insect immunity and disease susceptibility, largely owing to incomplete information, coupled with a lack of tools for data integration. Moreover, existing data are concentrated on a relatively small number of insect Orders. We provide suggestions for a path towards making more accurate predictions, which will require studies with realistic temperature exposures and housing design, and a greater understanding of both the thermal biology of the immune system and connections between immunity and the physiological responses to heat., Competing Interests: Competing interests The authors declare no competing or financial interests., (© 2023. Published by The Company of Biologists Ltd.)

The blacklegged tick, Ixodes scapularis, vectors Borrelia burgdorferi, a bacterium that causes Lyme Disease. Although synthetic pesticides can reduce tick numbers, there are concerns about their potential effects on beneficial insects, such as pollinators. Plant-based pest control agents such as essential oils could provide an alternative because they have low environmental persistency; however, these products struggle to provide effective control. We found a new natural acaricide, balsam fir (Abies balsamea) needles, that kill overwintering I. scapularis ticks. We extracted the essential oil from the needles, analyzed its chemical composition, and tested it for acaricidal activity. We placed ticks in tubes with substrate and positioned the tubes either in the field or in incubators simulating winter temperatures. We added balsam fir essential oil, or one of the main components of balsam fir essential oil (i.e., ß-pinene), to each tube. We found that both the oil and ß-pinene kill overwintering ticks. Whole balsam fir needles require several weeks to kill overwintering ticks, while the essential oil is lethal within days at low temperatures (≤ 4 °C). Further, low temperatures increased the efficacy of this volatile essential oil. Higher temperatures (i.e., 20 °C) reduce the acaricidal effectiveness of the essential oil by 50% at 0.1% v/v. Low temperatures may promote the effectiveness of other natural control products. Winter is an overlooked season for tick control and should be explored as a possible time for the application of low toxicity products for successful tick management., (© 2022. The Author(s).)

An explosion of data has provided detailed information about organisms at the molecular level. For some traits, this information can accurately predict phenotype. However, knowledge of the underlying molecular networks often cannot be used to accurately predict higher order phenomena, such as the response to multiple stressors. This failure raises the question of whether methodological reductionism is sufficient to uncover predictable connections between molecules and phenotype. This question is explored in this paper by examining whether our understanding of the molecular responses to food limitation and pathogens in insects can be used to predict their combined effects. The molecular pathways underlying the response to starvation and pathogen attack in insects demonstrates the complexity of real-world physiological networks. Although known intracellular signaling pathways suggest that food restriction should enhance immune function, a reduction in food availability leads to an increase in some immune components, a decrease in others, and a complex effect on disease resistance in insects such as the caterpillar Manduca sexta. However, our inability to predict the effects of food restriction on disease resistance is likely due to our incomplete knowledge of the intra- and extracellular signaling pathways mediating the response to single or multiple stressors. Moving from molecules to organisms will require novel quantitative, integrative and experimental approaches (e.g. single cell RNAseq). Physiological networks are non-linear, dynamic, highly interconnected and replete with alternative pathways. However, that does not make them impossible to predict, given the appropriate experimental and analytical tools. Such tools are still under development. Therefore, given that molecular data sets are incomplete and analytical tools are still under development, it is premature to conclude that methodological reductionism cannot be used to predict phenotype., (Copyright © 2021. Published by Elsevier Inc.)

AbstractResource-intensive traits, such as dispersal and reproduction, can be difficult to express simultaneously because of resource limitations. One solution is to switch between resource-intensive behaviors. Such phenotypic plasticity is one strategy that organisms use to funnel resources from one expensive trait to another. In crickets ( Gryllus texensis ), the development and maintenance of flight muscles reduce resource availability for reproduction, leading to physiological trade-offs between the two traits. Long-winged female G. texensis can histolyze their wing muscles, resulting in increased egg production, but they can then no longer fly. Using a diet that mimics food availability in the field, we found that long-winged females adopted one of the three following strategies: early reproduction, intermediate reproduction, and late reproduction. Some late reproducers maintained their flight capability until the end of their natural life span and laid few eggs. If females lost the ability to fly (i.e., their hind wings are removed), they laid eggs earlier, leading to increased reproductive output. However, other environmental cues (e.g., an increased number of mates, increased oviposition substrate quality, or a bout of dispersal flight) had no effect. Late-reproducing females laid 96% fewer eggs than early reproducers, suggesting that late reproduction exacts a huge fitness cost. Nevertheless, some females maintain their flight muscles to the end of their natural life span in both the lab and the field. We suggest that the ability to fly allows for bet hedging against an environmental catastrophe (e.g., drought or flood). This benefit may help explain the persistence of late-reproducing long-winged females, despite the cost of this choice. As climate change increases drought and flood in Texas, late dispersal may be one factor that helps this species survive in the future. An increased understanding of factors that maintain seemingly low fitness strategies can help us predict the resilience of species under climate change.

For many animals, the gut microbiome plays an essential role in immunity and digestion. However, certain animals, such as the caterpillar Manduca sexta , do not have a resident gut microbiome. Although these animals do have bacteria that pass through their gut from their natural environment, the absence of such bacteria does not reduce growth or survival. We hypothesized that M. sexta would sterilize their gut as a protective measure against secondary infection when faced with a gut infection or exposure to heat-killed bacteria in the blood (haemolymph). However, we found that gut sterilization did not occur during either type of immune challenge, i.e. bacterial numbers did not decrease. By examining the pattern of immune-related gene expression, gut pH, live bacterial counts and mass change (as a measure of sickness behaviour), we found evidence for physiological trade-offs between regulating the microbiome and defending against systemic infections. Caterpillars exposed to both gut pathogens and a systemic immune challenge had higher numbers of bacteria in their gut than caterpillars exposed to a single challenge. Following a multivariate analysis of variance, we found that the response patterns following an oral challenge, systemic challenge or dual challenge were unique. Our results suggest that the immune response for each challenge resulted in a different configuration of the immunophysiological network. We hypothesize that these different configurations represent different resolutions of physiological trade-offs based on the immune responses needed to best protect the animal against the present immune challenges., Competing Interests: Competing interestsThe authors declare no competing or financial interests., (© 2020. Published by The Company of Biologists Ltd.)

When animals are faced with a life-threatening challenge, they mount an organism-wide response (i.e. Plan A). For example, both the stress response (i.e. fight-or-flight) and the immune response recruit molecular resources from other body tissues, and induce physiological changes that optimize the body for defense. However, pathogens and predators often co-occur. Animals that can optimize responses for a dual challenge, i.e. simultaneous predator and pathogen attacks, will have a selective advantage. Responses to a combined predator and pathogen attack have not been well studied, but this paper summarizes the existing literature in insects. The response to dual challenges (i.e. Plan B) results in a suite of physiological changes that are different from either the stress response or the immune response, and is not a simple summation of the two. It is also not a straight-forward trade-off of one response against the other. The response to a dual challenge (i.e. Plan B) appears to resolve physiological trade-offs between the stress and immune responses, and reconfigures both responses to provide the best overall defense. However, the dual response appears to be more costly than either response occurring singly, resulting in greater damage from oxidative stress, reduced growth rate, and increased mortality.

Immune-nociceptor connections are found in animals across phyla. Local inflammation and/or damage results in increased nociceptive sensitivity of the affected area. However, in mammals, immune responses far from peripheral nociceptors, such as immune responses in the gut, produce a general increase in peripheral nociceptive sensitivity. This phenomenon has not, to our knowledge, been found in other animal groups. We found that consuming heat-killed pathogens reduced the tactile force needed to induce a defensive strike in the caterpillar Manduca sexta . This increase in the nociceptive sensitivity of the body wall is probably part of the reconfiguration of behaviour and physiology that occurs during an immune response (e.g. sickness behaviour). This increase may help enhance anti-predator behaviour as molecular resources are shifted towards the immune system. This article is part of the Theo Murphy meeting issue 'Evolution of mechanisms and behaviour important for pain'.

Some parasites manipulate host behavior by exploiting the host's behavioral control networks. This review explores two examples of this approach using parasites from opposite ends of the size spectrum, that is, viruses and parasitic insects. The first example explores the use of the gene (egt) by some baculoviruses to deactivate the hormone 20-hydroxyecdysone. Suppressing this chemical signal prevents the expression of behaviors that could reduce viral transmission. The second example explores how a parasitic wasp uses the host's immune/neural communication system to control host behavior. When a host's manipulated behavior requires complex neural coordination, exploitation of host behavioral control systems is likely to be involved. Simpler host behaviors can be induced by damage to host tissues., (Copyright © 2019 Elsevier Inc. All rights reserved.)

Should females alter their reproductive strategy when attacked by pathogens? Two hypotheses provide opposite predictions. Terminal reproductive investment theory predicts that reproduction should increase when the risk of death increases. However, physiological trade-offs between reproduction and immune function might be expected to produce a decrease in reproduction during a robust immune response. There is evidence for both hypotheses. We examine whether age determines the effect of an immune challenge on reproductive strategy in long-winged females of the Texas field cricket, Gryllus texensis, when fed an ecologically valid (i.e. limited) diet. The limited diet reduced reproductive output. However, even under resource-limited conditions, immune challenge had no effect on the reproductive output of young or middle-aged females. Both reproductive output and immune function (lysozyme-like activity and phenoloxidase (PO) activity) increased with age, which is contrary to both hypotheses. We hypothesize that PO activity is pleiotropic and represents an investment in both reproduction and immune function. Three proPO genes (identified in a published RNA-seq dataset (transcriptome)) were expressed either in the fat body or the ovaries (supporting the hypothesis that PO is bifunctional). The possible bifunctionality of PO suggests that it may not be an appropriate immune measure for studies on immune/reproductive trade-offs. This study also suggests that the threshold for terminal reproductive investment may not decrease prior to senescence in some species., Competing Interests: The authors have declared that no competing interests exist.

Mounting an immune response consumes resources, which should lead to increased feeding. However, activating the immune system reduces feeding (i.e. illness-induced anorexia) in both vertebrates and invertebrates, suggesting that it may be beneficial. We suggest that illness-induced anorexia may be an adaptive response to conflicts between immune defense and food detoxification. We found that activating an immune response in the caterpillar Manduca sexta increased its susceptibility to the toxin permethrin. Conversely, a sublethal dose of permethrin reduced resistance to the bacterium Serratia marcescens , demonstrating a negative interaction between detoxification and immune defense. Immune system activation and toxin challenge each depleted the amount of glutathione in the hemolymph. Increasing glutathione concentration in the hemolymph increased survival for both toxin- and immune+toxin-challenged groups. The results of this rescue experiment suggest that decreased glutathione availability, such as occurs during an immune response, impairs detoxification. We also found that the expression of some detoxification genes were not upregulated during a combined immune-toxin challenge, although they were when animals received a toxin challenge alone. These results suggest that immune defense reduces food detoxification capacity. Illness-induced anorexia may protect animals by decreasing exposure to food toxins when detoxification is impaired., Competing Interests: Competing interestsThe authors declare no competing or financial interests., (© 2018. Published by The Company of Biologists Ltd.)

Although predator exposure increases the risk of wound infections, it typically induces immunosuppression. A number of non-mutually exclusive hypotheses have been put forward to explain this immunosuppression, including: trade-offs between the immune system and other systems required for anti-predator behaviour, redistribution of immune resources towards mechanisms needed to defend against wound infections, and reconfiguration of the immune system to optimize defence under the physiological state of fight-or-flight readiness. We tested the ability of each hypothesis to explain the effects of chronic predator stress on the immune system of the caterpillar Manduca sexta Predator exposure induced defensive behaviours, reduced mass gain, increased development time and increased the concentration of the stress neurohormone octopamine. It had no significant effect on haemocyte number, melanization rate, phenoloxidase activity, lysozyme-like activity or nodule production. Predator stress reduced haemolymph glutathione concentrations. It also increased constitutive expression of the antimicrobial peptide attacin-1 but reduced attacin-1 expression in response to an immune challenge. These results best fit the immune reconfiguration hypothesis, although the other hypotheses are also consistent with some results. Interpreting stress-related changes in immune function may require an examination at the level of the whole organism., (© 2017. Published by The Company of Biologists Ltd.)

The classic biomedical view is that stress hormone effects on the immune system are largely pathological, especially if the stress is chronic. However, more recent interpretations have focused on the potential adaptive function of these effects. This paper examines stress response-immune system interactions from a physiological network perspective, using insects because of their simpler physiology. For example, stress hormones can reduce disease resistance, yet activating an immune response results in the release of stress hormones in both vertebrates and invertebrates. From a network perspective, this phenomenon is consistent with the 'sharing' of the energy-releasing ability of stress hormones by both the stress response and the immune system. Stress-induced immunosuppression is consistent with the stress response 'borrowing' molecular components from the immune system to increase the capacity of stress-relevant physiological processes (i.e. a trade off). The insect stress hormones octopamine and adipokinetic hormone can also 'reconfigure' the immune system to help compensate for the loss of some of the immune system's molecular resources (e.g. apolipophorin III). This view helps explain seemingly maladaptive interactions between the stress response and immune system. The adaptiveness of stress hormone effects on individual immune components may be apparent only from the perspective of the whole organism. These broad principles will apply to both vertebrates and invertebrates., (Copyright © 2016 Elsevier Inc. All rights reserved.)

A whole organism, network approach can help explain the adaptive purpose of stress-induced changes in immune function. In insects, mediators of the stress response (e.g. stress hormones) divert molecular resources away from immune function and towards tissues necessary for fight-or-flight behaviours. For example, molecules such as lipid transport proteins are involved in both the stress and immune responses, leading to a reduction in disease resistance when these proteins are shifted towards being part of the stress response system. Stress responses also alter immune system strategies (i.e. reconfiguration) to compensate for resource losses that occur during fight-or flight events. In addition, stress responses optimize immune function for different physiological conditions. In insects, the stress response induces a pro-inflammatory state that probably enhances early immune responses., (Copyright © 2016 Elsevier Ltd. All rights reserved.)

Some parasites alter the behaviour of their hosts. The larvae of the parasitic wasp Cotesia congregata develop within the body of the caterpillar Manduca sexta During the initial phase of wasp development, the host's behaviour remains unchanged. However, once the wasps begin to scrape their way out of the caterpillar, the caterpillar host stops feeding and moving spontaneously. We found that the caterpillar also temporarily lost sensation around the exit hole created by each emerging wasp. However, the caterpillars regained responsiveness to nociception in those areas within 1 day. The temporary reduction in skin sensitivity is probably important for wasp survival because it prevents the caterpillar from attacking the emerging wasp larvae with a defensive strike. We also found that expression of plasmatocyte spreading peptide (PSP) and spätzle genes increased in the fat body of the host during wasp emergence. This result supports the hypothesis that the exiting wasps induce a cytokine storm in their host. Injections of PSP suppressed feeding, suggesting that an augmented immune response may play a role in the suppression of host feeding. Injection of wasp larvae culture media into non-parasitized caterpillars reduced feeding, suggesting that substances secreted by the wasp larvae may help alter host behaviour., (© 2016. Published by The Company of Biologists Ltd.)

Immune activation alters behaviour (i.e. sickness behaviour) in animals across phyla and is thought to aid recovery from infection. Hypotheses regarding the adaptive function of different sickness behaviours (e.g. decreased movement and appetite) include the energy conservation and predator avoidance hypotheses. These hypotheses were originally developed for mammals (e.g. Hart, 1988), however similar sickness behaviours are also observed in insects (e.g., crickets). We predicted that immune-challenged crickets (Gryllus texensis) would reduce feeding, grooming, and locomotion as well as increase shelter use, consistent with the energy conservation and predator avoidance hypotheses. We found evidence of illness-induced anorexia in adult and juvenile crickets, consistent with previous research (Adamo et al., 2010), but contrary to expectations, we found an increase in grooming, and no evidence that crickets decreased locomotion or increased shelter use in response to immune challenge. Therefore, our results do not support the energy conservation or predator avoidance hypotheses. The difference in sickness behaviour between insects and mammals is probably due, in part, to the lack of physiological fever in insects. We hypothesize that the lack of physiological fever reduces the need for energy conservation, decreasing the benefits of some sickness behaviours such as increased shelter use. These results, taken together with others in the literature, suggest that ectotherms and endotherms may differ significantly in the selective forces leading to the evolution of most sickness behaviours., (Copyright © 2016 Elsevier B.V. All rights reserved.)

Dwindling resources might be expected to induce a gradual decline in immune function. However, food limitation has complex and seemingly paradoxical effects on the immune system. Examining these changes from an immune system network perspective may help illuminate the purpose of these fluctuations. We found that food limitation lowered long-term (i.e. lipid) and short-term (i.e. sugars) energy stores in the caterpillar Manduca sexta. Food limitation also: altered immune gene expression, changed the activity of key immune enzymes, depressed the concentration of a major antioxidant (glutathione), reduced resistance to oxidative stress, reduced resistance to bacteria (Gram-positive and -negative bacteria) but appeared to have less effect on resistance to a fungus. These results provide evidence that food limitation led to a restructuring of the immune system network. In severely food-limited caterpillars, some immune functions were enhanced. As resources dwindled within the caterpillar, the immune response shifted its emphasis away from inducible immune defenses (i.e. those responses that are activated during an immune challenge) and increased emphasis on constitutive defenses (i.e. immune components that are produced consistently). We also found changes suggesting that the activation threshold for some immune responses (e.g. phenoloxidase) was lowered. Changes in the configuration of the immune system network will lead to different immunological strengths and vulnerabilities for the organism., (© 2016. Published by The Company of Biologists Ltd.)

Intense, short-term stress (i.e., robust activation of the fight-or-flight response) typically produces a transient decline in resistance to disease in animals across phyla. Chemical mediators of the stress response (e.g., stress hormones) help induce this decline, suggesting that this transient immunosuppression is an evolved response. However, determining the function of stress hormones on immune function is difficult because of their complexity. Nevertheless, evidence suggests that stress hormones help maintain maximal resistance to disease during the physiological changes needed to optimize the body for intense physical activity. Work on insects demonstrates that stress hormones both shunt resources away from the immune system during fight-or-flight responses as well as reconfigure the immune system. Reconfiguring the immune system minimizes the impact of the loss of these resources and reduces the increased costs of some immune functions due to the physiological changes demanded by the fight-or-flight response. For example, during the stress response of the cricket Gryllus texensis, some molecular resources are shunted away from the immune system and toward lipid transport, resulting in a reduction in resistance to disease. However, insects' immune cells (hemocytes) have receptors for octopamine (the insect stress neurohormone). Octopamine increases many hemocyte functions, such as phagocytosis, and these changes would tend to mitigate the decline in immunity due to the loss of molecular resources. Moreover, because the stress response generates oxidative stress, some immune responses are probably more costly when activated during a stress response (e.g., those that produce reactive molecules). Some of these immune responses are depressed during stress in crickets, while others, whose costs are probably not increased during a stress response, are enhanced. Some effects of stress hormones on immune systems may be better understood as examples of reconfiguration rather than as mediating a trade-off., (© The Author 2014. Published by Oxford University Press on behalf of the Society for Integrative and Comparative Biology. All rights reserved. For permissions please email: journals.permissions@oup.com.)

Animals have a number of behavioral defenses against infection. For example, they typically avoid sick conspecifics, especially during mating. Most animals also alter their behavior after infection and thereby promote recovery (i.e., sickness behavior). For example, sick animals typically reduce the performance of energetically demanding behaviors, such as sexual behavior. Finally, some animals can increase their reproductive output when they face a life-threatening immune challenge (i.e., terminal reproductive investment). All of these behavioral responses probably rely on immune/neural communication signals for their initiation. Unfortunately, this communication channel is prone to manipulation by parasites. In the case of sexually transmitted infections (STIs), these parasites/pathogens must subvert some of these behavioral defenses for successful transmission. There is evidence that STIs suppress systemic signals of immune activation (e.g., pro-inflammatory cytokines). This manipulation is probably important for the suppression of sickness behavior and other behavioral defenses, as well as for the prevention of attack by the host's immune system. For example, the cricket, Gryllus texensis, is infected with an STI, the iridovirus IIV-6/CrIV. The virus attacks the immune system, which suffers a dramatic decline in its ability to make proteins important for immune function. This attack also hampers the ability of the immune system to activate sickness behavior. Infected crickets cannot express sickness behavior, even when challenged with heat-killed bacteria. Understanding how STIs suppress sickness behavior in humans and other animals will significantly advance the field of psychoneuroimmunology and could also provide practical benefits., (© The Author 2014. Published by Oxford University Press on behalf of the Society for Integrative and Comparative Biology. All rights reserved. For permissions please email: journals.permissions@oup.com.)

We identified the insect iridovirus IIV-6/CrIV as a pathogen of the cricket Gryllus texensis using electron microscopy (EM) and polymerase chain reaction (PCR) analysis. EM showed that the virus attacks the fat body, an organ important for protein production, immune function and lipid storage. During infection the fat body hypertrophied, but egg production withered, leaving the lateral oviducts empty of eggs; the females were effectively sterile. EM of the testis of infected males suggests that the testis was not invaded by the virus, although sperm taken from the spermatophores of infected males showed little or no motility. Nevertheless, males and females continued to mate when infected. In fact, infected males were quicker to court females than uninfected controls. The virus benefits from the continued sexual behaviour of its host; transmission studies show that the virus can be spread through sexual contact. Sickness behaviour, the adaptive reduction of feeding and sexual behaviour that is induced by an activated immune system, was absent in infected crickets. Total haemolymph protein was reduced, as was phenoloxidase activity, suggesting a reduction in immune protein production by the fat body. The evidence suggests that during IIV-6/CrIV infection, the immune signal(s) that induces sickness behaviour is absent. Curtailment of a host's sickness behaviour may be necessary for any pathogen that is spread by host sexual behaviour., (© 2014. Published by The Company of Biologists Ltd.)

Predator-induced stress responses are thought to reduce an animal's risk of being eaten. Therefore, these stress responses should enhance anti-predator behaviour. We found that individual insects (the cricket Gryllus texensis) show reliable behavioural responses (i.e. behavioural types) in a plus-shaped maze. An individual's behaviour in the plus maze remained consistent for at least 1/2 of its adult life. However, after exposure to a model predator, both male and female crickets showed a reduced period of immobility and an increased amount of time spent under shelter compared with controls. These changes could be mimicked by injections of the insect stress neurohormone octopamine. These behavioural changes probably aid crickets in evading predators. Exposure to a model predator increased the ability of crickets to escape a live predator (a bearded dragon, Pogona vitticeps). An injection of octopamine had the same effect, showing that stress hormones can reduce predation. Using crickets to study the fitness consequences of predator-induced stress responses will help integrate ecological and biomedical concepts of 'stress'.

Fever can reduce mortality in infected animals. Yet, despite its fitness-enhancing qualities, fever often varies among animals. We used several approaches to examine this variation in insects. Texas field crickets (Gryllus texensis) exhibited a modest fever (1 °C increase in preferred body temperature, T pref) after injection of prostaglandin, which putatively mediates fever in both vertebrates and invertebrates, but they did not exhibit fever during chronic exposure to heat-killed bacteria. Further, chronic food limitation and mating status did not affect T pref or the expression of behavioural fever, suggesting limited context dependency of fever in G. texensis. Our meta-analysis of behavioural fever studies indicated that behavioural fever occurs in many insects, but it is not ubiquitous. Thus, both empirical and meta-analytical results suggest that the fever response in insects 'is widespread, although certainly not inevitable' (Moore 2002). We highlight the need for future work focusing on standardizing an experimental protocol to measure behavioural fever, understanding the specific mechanism(s) underlying fever in insects, and examining whether ecological or physiological costs often outweigh the benefits of fever and can explain the sporadic nature of fever in insects.

For millions of years, parasites have altered the behaviour of their hosts. Parasites can affect host behaviour by: (1) interfering with the host's normal immune-neural communication, (2) secreting substances that directly alter neuronal activity via non-genomic mechanisms and (3) inducing genomic- and/or proteomic-based changes in the brain of the host. Changes in host behaviour are often restricted to particular behaviours, with many other behaviours remaining unaffected. Neuroscientists can produce this degree of selectivity by targeting specific brain areas. Parasites, however, do not selectively attack discrete brain areas. Parasites typically induce a variety of effects in several parts of the brain. Parasitic manipulation of host behaviour evolved within the context of the manipulation of other host physiological systems (especially the immune system) that was required for a parasite's survival. This starting point, coupled with the fortuitous nature of evolutionary innovation and evolutionary pressures to minimize the costs of parasitic manipulation, likely contributed to the complex and indirect nature of the mechanisms involved in host behavioural control. Because parasites and neuroscientists use different tactics to control behaviour, studying the methods used by parasites can provide novel insights into how nervous systems generate and regulate behaviour. Studying how parasites influence host behaviour will also help us integrate genomic, proteomic and neurophysiological perspectives on behaviour.

Climate change will result in warmer temperatures and an increase in the frequency and severity of extreme weather events. Given that higher temperatures increase the reproductive rate of temperate zone insects, insect population growth rates are predicted to increase in the temperate zone in response to climate. This consensus, however, rests on the assumption that food is freely available. However, under conditions of limited food, the reproductive output of the Texan cricket Gryllus texensis (Cade and Otte) was highest at its current normal average temperature and declined with increasing temperature. Moreover, low food availability decreased survival during a simulated heat wave. Therefore, the effects of climate change on this species, and possibly on many others, are likely to hinge on food availability. Extrapolation from our data suggests that G. texensis will show larger yearly fluctuations in population size as climate change continues, and this will also have ecological repercussions. Only those temperate zone insects with a ready supply of food (e.g., agricultural pests) are likely to experience the predicted increase in population growth in response to climate change; food-limited species are likely to experience a population decline.

Stress-induced changes in immune function occur in animals across phyla, and these effects are usually immunosuppressive. The function of this immunomodulation remains elusive; however, the existence of specialized receptors on immune cells suggests that it is adaptive. A comparative approach may provide a useful perspective. Although invertebrates have simpler endocrine/neuroendocrine systems and immune systems than vertebrates, they have robust stress responses that include the release of stress hormones/neurohormones. Stress hormones modify immune function in mollusks, insects, and crustaceans. As in vertebrates, the effects of stress hormones/neurohormones on invertebrate immune function are complex, and are not always immunosuppressive. They are context-, stressor-, time- and concentration-dependent. Stress hormone effects on invertebrate immune function may help to re-align resources during fight-or-flight behavior. The data are consistent with the hypothesis that stress hormones induce a reconfiguration of networks at molecular, cellular and physiological levels that allow the animal to maintain optimal immunity as the internal environment changes. This reconfiguration enhances some immune functions while suppressing others. Knowing the molecular details of these shifts will be critical for understanding the adaptive function of stress hormones on immune function., (Copyright © 2012 Elsevier Inc. All rights reserved.)

Octopamine (OA), the insect equivalent of norepinephrine, links the nervous system and immune system in insects. This study examines the underlying molecular mechanisms (i.e. second messenger systems) mediating OA effects on insect immune cells. At low concentrations (<1μM), OA stimulatedhemocyte spreading and phagocytosis in the larval Lepidopteran (caterpillar) Chilo suppressalis, whereas at high concentrations (>10 μM), OA inhibited hemocyte spreading and phagocytosis. Similarly, OA concentration had differential effects on two intracellular signaling pathways, Ca(2+) and cAMP. Low concentrations of OA increased intracellular Ca(2+), but only high concentrations of OA (>1 μM) led to an increase in both Ca(2+) and cAMP. We identified an α-adrenergic-like octopamine receptor in this species (CsOA1) and confirmed that it is expressed in hemocytes. After heterologous expression in HEK-293 cells, the CsOA1 receptor produced the same OA concentration-dependent responses on intracellular Ca(2+) and cAMP as had been observed in hemocytes. These findings support earlier work showing that OA has both stimulatory and suppressive effects on immune responses, depending on the OA concentration. Our evidence suggests that these biphasic effects are mediated by an octopamine receptor signaling through intracellular Ca(2+) and cAMP second messenger pathways. Stress hormones/neuromodulators have complex effects on immune function in animals across phyla. This complexity may be mediated, in part, by conserved connections between adrenergic-like G-coupled protein receptors and second messenger systems., (Copyright © 2012 Elsevier Inc. All rights reserved.)

Many of the deleterious effects of chronic stress in vertebrates are caused by the long-term elevation of stress hormones. These negative effects are thought to be unavoidable by-products of sustained activation of the stress response, but the details remain unclear. A comparative perspective may help in understanding chronic stress. We exposed crickets (Gryllus texensis) to a mock predator. A single exposure to a mock predator induced a transient increase in the hemolymph (blood) concentration of the insect stress neurohormone, octopamine. Repeated exposure to the mock predator increased basal levels of octopamine, similar to the effects of chronic stress on the basal levels of vertebrate stress hormones. This study is the first to report an increase in the basal levels of an invertebrate stress hormone in response to repeated flight-or-fight stress. Chronic stress reduced weight gain, and decreased feeding and enhanced weight loss after food deprivation in adult female crickets. However, chronic stress also increased the tendency of crickets to produce sustained flight. Therefore, this study supports the hypothesis that increasing basal levels of stress hormones may be a phylogenetically common response to chronically stressful conditions. It also demonstrates that chronic stress has both positive and negative effects in insects., (Copyright © 2011 Elsevier Inc. All rights reserved.)

In many parts of the world, climate change is increasing the frequency and severity of heat waves. How do heat waves impact short-lived poikilotherms such as insects? In the cricket, Gryllus texensis, 6 days of elevated temperatures (i.e. 7°C above the average field temperature and 5°C above their preferred temperature) resulted in increased egg laying, faster egg development and greater mass gain. The increased temperature also increased activity of phenoloxidase and lysozyme-like enzymes, two immune-related enzymes, and enhanced resistance to the Gram-negative bacterium Serratia marcescens. When given a sublethal S. marcescens infection, G. texensis maintained increased reproductive output at the elevated temperature (33°C). These data suggest that heat waves could result in more numerous, disease resistant, crickets. However, resistance to the Gram-positive bacterium, Bacillus cereus was lower at temperatures above or below the average field temperature (26°C). A sublethal infection with B. cereus reduced egg laying at all temperatures and suppressed the increase in egg laying induced by higher temperatures. These results suggest that for some species-pathogen interactions, increased temperatures can induce trade-offs between reproduction and disease resistance. This result may partly explain why G. texensis prefers temperatures lower than those that produce maximal reproductive output and enhanced immune function.

Mediators of the stress response (e.g. glucocorticoids and norepinephrine) can be immunosuppressive. Nevertheless, immune challenge leads to the release of these compounds in vertebrates. To resolve this paradox, it has been suggested that stress hormones help restore immune homeostasis, preventing self-damage. A comparative approach may provide additional hypotheses as to why an immune challenge induces the release of stress hormones/neurohormones. Octopamine, a neurohormonal mediator of the stress response in the cricket Gryllus texensis, increased in concentration in the hemolymph during an immune challenge. Therefore, the release of stress hormones during an immune response occurs in animals across phyla. Octopamine induced an increase in lipid concentration in the hemolymph. After an acute stress (flying or running) the total number of hemocytes in the hemolymph increased. Injections of octopamine had the same effect, suggesting that it may enhance hemocyte-dependent immune functions. On the other hand, octopamine decreased lysozyme-like activity in vitro, suggesting that it inhibits some immune functions. However, lysozyme-like activity was increased by the presence of heat-killed bacteria in vitro and this increase was significantly augmented by the presence of octopamine. Therefore, the effect of octopamine on immune function differed depending on the presence of pathogens. Stress hormones may help shift immune function into the most optimal configuration depending on the physiological context., (Copyright 2009 Elsevier Inc. All rights reserved.)

Parasite-induced alteration of host behaviour is a widespread transmission strategy among pathogens. Understanding how it works is an exciting challenge from both a mechanistic and an evolutionary perspective. In this review, we use key examples to examine the proximate mechanisms by which parasites are known to control the behaviour of their hosts. Special attention is given to the recent developments of post-genomic tools, such as proteomics, for determining the genetic basis of parasitic manipulation. We then discuss two novel perspectives on host manipulation (mafia-like strategy and exploitation of host compensatory responses), arguing that parasite-manipulated behaviours could be the result of compromises between host and parasite strategies. Such compromises may occur when collaborating with the parasite is less costly for the host in terms of fitness than is resisting parasite-induced changes. Therefore, even when changes in host behaviour benefit the parasite, the host may still play some role in the switch in host behaviour. In other words, the host does not always become part of the parasite's extended phenotype. For example, parasites that alter host behaviour appear to induce widely disseminated changes in the hosts' central nervous system, as opposed to targeted attacks on specific neural circuits. In some host-parasite systems, the change in host behaviour appears to require the active participation of the host (e.g., via host immune-neural connections). Even when the change in host behaviour results in clear fitness benefits for the parasite, these behavioural changes may sometimes be produced by the host. Changes in host behaviour that decrease the fitness costs of infection could be selected for, even if these changes also benefit the parasite.

Objective: The aim of this study was to prospectively assess the diagnostic capabilities of transabdominal sonography performed with newer sonography machines for showing focal bladder wall abnormalities (FBWAs) detected on cystoscopy., Methods: One hundred twelve consecutive patients (97 male and 15 female; mean age, 68 years) underwent cystoscopy. Reasons for referral were macroscopic hematuria (44 cases [39%]), surveillance after transurethral resection (56 cases [49.5%]), and incidental sonographic findings (12 cases [11.5%]). One to 2 days before cystoscopy, sonography was carried out by a single operator who was blinded to clinical and recent sonographic findings. The presence, size, number, and location of FBWAs (eg, polypoid vegetations and asymmetric bladder wall thickening) were recorded and compared with cystoscopic and histologic findings., Results: One hundred ten patients with a histologic diagnosis were available for the study. Benign conditions, nontransitional tumors, and transitional tumors were found in 26.3%, 3.7% and 70% of the patients, respectively. The sensitivity, specificity, positive predictive value, negative predictive value, and overall accuracy of sonography of cystoscopic lesions were 91.4%, 79.3%, 91.4%, 79.3%, and 88.2%. Cancers of 15 mm or smaller and flat tumors were often missed by sonography, whereas chronic cystitis accounted for most of the false-positive sonographic findings; however, sonography had poor capability of characterizing FBWAs, with specificity of 62%. In this respect, color Doppler findings proved of little aid as well., Conclusions: In patients selected for cystoscopy, transabdominal sonography with newer sonography machines showed good diagnostic accuracy for focal alterations of the bladder wall found on cystoscopy.

Intense physical activity results in transient immunosuppression in a wide range of animals. We tested the hypothesis that competition between immune function and lipid transport for the protein apolipophorin III (apoLpIII) can cause transient immunosuppression in crickets. Both flying, an energetically demanding behavior, and an immune challenge reduced the amount of monomeric (free) apoLpIII in the hemolymph of crickets. Because both immune function and flying depleted free apoLpIII, these two phenomena could be in competition for this protein. We showed that immune function was sensitive to the amount of free apoLpIII in the hemolymph. Reducing the amount of free apoLpIII in the hemolymph using adipokinetic hormone produced immunosuppression. Increasing apoLpIII levels after flight by pre-loading animals with trehalose reduced immunosuppression. Increasing post-flight apoLpIII levels by injecting purified apoLpIII also reduced flight-induced immunosuppression. These results show that competition between lipid transport and immune function for the same protein can produce transient immunosuppression after flight-or-fight behavior. Intertwined physiological systems can produce unexpected trade-offs.

Although many animals exhibit illness-induced anorexia when immune-challenged, the adaptive significance of this behavior remains unclear. Injecting Manduca sexta larvae (caterpillars) with live bacteria (Serratia marcescens), heat-killed bacteria or bacterial lipopolysaccharides resulted in a decline in feeding, demonstrating illness-induced anorexia in this species. We used M. sexta to test four commonly suggested adaptive functions for illness-induced anorexia. (1) Food deprivation did not reduce the iron content of the hemolymph. (2) Immune-challenged M. sexta were not more likely to move to a different part of the plant. Therefore, the decline in feeding is unlikely to be an adaptive response allowing the animal to move away from a patch of contaminated food. (3) M. sexta force-fed S. marcescens bacteria were not more susceptible to a S. marcescens systemic infection than were M. sexta force-fed nutrient broth. (4) Force-feeding infected M. sexta during illness-induced anorexia did not increase mortality and short-term food deprivation did not enhance survival. However, force-feeding M. sexta with a high lipid diet (linseed oil and water) resulted in an increase in mortality when challenged with S. marcescens. Force-feeding sucrose or water did not reduce resistance. Force-feeding a high lipid diet into healthy animals did not reduce weight gain, suggesting that it was not toxic. We hypothesize that there is a conflict between lipid metabolism and immune function, although whether this conflict has played a role in the evolution of illness-induced anorexia remains unknown. The adaptive function of illness-induced anorexia requires further study in both vertebrates and invertebrates.

Interactions between immune systems, nervous systems, and behavior are well established in vertebrates. A comparative examination of these interactions in other animals will help us understand their evolution and present adaptive functions. Insects show immune-behavioral interactions similar to those seen in vertebrates, suggesting that many of them may have a highly conserved function. Activation of an immune response in insects results in illness-induced anorexia, behavioral fever, changes in reproductive behavior, and decreased learning ability in a broad range of species. Flight-or-fight behaviors result in a decline in disease resistance. In insects, illness-induced anorexia may enhance immunity. Stress-induced immunosuppression is probably due to physiological conflicts between the immune response and those of other physiological processes. Because insects occupy a wide range of ecological niches, they will be useful in examining how some immune-behavioral interactions are sculpted by an animal's behavioral ecology.

Cuttlefish can rapidly alter their appearance by using neurally controlled chromatophore organs. This ability may provide a window into their cognitive capacity. We test whether the changes in body pattern that occur during hunting depend on context. If they do, then it may be possible to use these changes to study cephalopod cognition while the animal is engaged in ecologically relevant tasks. We found consistent individual differences in the tendency of cuttlefish to hunt with the first two arms raised. We also found that cuttlefish usually darken their skin after they seize a prey item. This darkening is observed regardless of the identity of the prey (fish, crab, or shrimp), prey context (buried in sand, in a bare tank, or on top of a rock pile), or the presence of a sudden stimulus. The sudden stimulus was created by presenting an overhead model bird to the cuttlefish. The model induced components of the Deimatic Display, which is a form of antipredator behavior, suggesting that the model was perceived as a potential threat. Passing Cloud displays and the Darkening of the arms were significantly reduced after exposure to the model bird. The effect of a potential predator on body pattern expression during hunting suggests it may be possible to use these changes as a sensitive indicator of ecologically relevant learning.

Cuttlefish have a large repertoire of body patterns that are used for camouflage and interspecific signaling. Intraspecific signaling by male cuttlefish has been well documented but studies on signaling by females are lacking. We found that females displayed a newly described body pattern termed Splotch toward their mirror image and female conspecifics, but not to males, prey or inanimate objects. Female cuttlefish may use the Splotch body pattern as an intraspecific signal, possibly to reduce agonistic interactions. The ability of females to produce a consistent body pattern in response to conspecifics and mirrors suggests that they can recognize same-sex conspecifics using visual cues, despite the lack of sexual dimorphism visible to human observers.

When startled, some animals reduce ventilation rate and heart rate, and become motionless. The function of this response, if any, remains unknown. We used non-invasive ultrasound imaging to monitor the ventilatory, cardiac and postural responses of cuttlefish exposed to sudden visual stimuli. Simultaneously, we recorded cuttlefish behaviour using an overhead video camera. Upon presentation of the sudden visual stimulus (rapidly approaching bird cut-out), cuttlefish rapidly changed the colour and the texture of their skin, taking on characteristics of the Deimatic Display. Cuttlefish also became motionless (behavioural freezing), hyperinflated their mantles, and decreased their ventilation rate and heart rate. We found no evidence of a relationship between the intensity of the Deimatic Display and the intensity of any other measured parameter. Ventilation rate decreased during behavioural freezing. Hyperinflation of the mantle was most intense in preparation for and during behavioural freezing. Heart rate decreases occurred during mantle hyperinflation and were greatest in animals showing the most hyperinflation. Decreased heart rate may not be adaptive per se. Instead, it might be a product of the unusual arrangement of the cuttlefish peripheral vasculature, which could be compressed during mantle hyperinflation. By filling the mantle with water (hyperinflation), this response to sudden stimuli may help cuttlefish prepare for possible flight by jet propulsion, which often follows the Deimatic Display.

The parasitic wasp, Cotesia congregata, suppresses feeding in its host Manduca sexta. Feeding suppression in the host coincides with the emergence of the wasps through the host's cuticle. During wasp emergence, host hemocyte number declined, suggesting that the host mounts a wound/immune response against the exiting parasitoids and/or resulting tissue damage. Eliciting a different type of immune response by injecting heat-killed Serratia marcescens also resulted in a decline in feeding and a reduction in hemocyte number. Both the emerging wasps and the bacteria induced an increase in hemolymph octopamine concentration and a decrease in foregut peristalsis in M. sexta. The emerging parasitoids produced the largest changes. The source of the additional octopamine appeared to be the host in both cases. S. marcescens was found to contain no detectable amounts of octopamine. The parasitoids had insufficient octopamine to account for the amount found in host hemolymph and they did not secrete octopamine in vitro. One cause for the high concentration of octopamine in parasitized M. sexta was that octopamine was removed from the hemolymph approximately 23 times more slowly after the wasps emerged than prior to wasp emergence. The striking similarity between the effects of parasitoids and bacteria on M. sexta feeding, hemocyte number, hemolymph octopamine concentration, and foregut peristalsis supports the possibility that the immune/wound reaction induced by the emerging wasps could play a role in the suppression of host feeding. These results also support the hypothesis that M. sexta exhibit an immune-activated anorexia., (Copyright 2005 Wiley-Liss, Inc.)

Using ultrasound imaging, we investigated the roles of the potentially contractile veins and of the mantle (the powerful body wall that moves water over the gills, and also encloses the large veins and the hearts) in returning the blood of cuttlefish to its hearts. Ultrasound provided the first non-invasive observations of vascular function in an unanaesthetized, free-moving cephalopod. The large veins (anterior vena cava, lateral venae cavae and efferent branchial vessels) contracted in live, intact cuttlefish (Sepia officinalis L.). The anterior vena cava contracted at the same rate as the mantle, but it often expanded during mantle contraction. Furthermore, the anterior vena cava contracted peristaltically in vivo, suggesting that it actively aids venous return. The lateral venae cavae and efferent branchial vessels contracted at the same rate as the branchial and systemic hearts, but at a different rate from the mantle. A peristaltic wave appeared to travel along the lateral venae cavae to the branchial hearts, potentially aiding venous return. We found a muscular valve between the anterior and lateral venae cavae, which ensured that blood flowed only one way between these unsynchronized vessels. The mantle appears to have an unclear connection with cardiovascular function. We conclude that, when cuttlefish are at rest, the mantle does not compress any of the large veins that we imaged (including the anterior vena cava), and that peristaltic contractions of the large veins might be important in returning cephalopod blood to the hearts.

Because most learning studies in cephalopods have been performed on octopods, it remains unclear whether such abilities are specific to octopus, or whether they correlate with having a larger and more centrally organized brain. To investigate associative learning in a different cephalopod, six sexually mature cuttlefish (Sepia officinalis) participated in a counterbalanced, within-subjects, appetitive, classical conditioning procedure. Two plastic spheres (conditioned stimuli, CSs), differing in brightness, were presented sequentially. Presentation of the CS+ was followed 5 s later by a live feeder fish (unconditioned stimulus, US). Cuttlefish began to attack the CS+ with the same type of food-acquisition seizures used to capture the feeder fish. After seven blocks of training (42 presentations of each CS) the difference in seizure probability between CS+ and CS- trials more than doubled; and was found to be significantly higher in late versus early blocks. These results indicate that cuttlefish exhibit autoshaping under some conditions. The possible ecological significance of this type of learning is briefly discussed.

An animal's ability to resist disease is usually estimated by measuring one or more components of the immune system. There is an assumption that these assays of immunity measure an animal's ability to mount an effective immune response. This paper tests this assumption by examining the relationship between two common estimates of insect immunocompetence, phenoloxidase and lysozyme-like enzyme activity, and resistance to three common insect bacterial pathogens: Serratia marcescens, Serratia liquefaciens, and Bacillus cereus. There was a correlation (Spearman's rs=0.33, p<0.001, n=190 pairs) between total phenoloxidase and baseline lysozyme-like activity within individuals. However, total phenoloxidase and baseline lysozyme-like activity levels did not predict which male crickets would survive any of the three bacterial challenges. Lysozyme-like activity increased after an immune challenge (Friedman, 33.72, p<0.001), and the greater the increase, the greater the chance that the cricket would survive S. marcescens (slope=0.15, chi 2=8.2, p=0.005) or B. cereus (slope=0.8, chi 2=6.4, p=0.01). The crickets with a greater total hemolymph protein concentration were also more likely to survive a challenge with any of the three bacterial pathogens than the crickets with lower total hemolymph protein concentrations (S. liquefaciens: slope=0.02, chi 2=9.2, p=0.002; B. cereus: slope=0.02, chi 2=6.5, p=0.01; S. marcescens: slope=0.03, chi 2=7.8, p=0.005). Because of the complexity of the immune system, empirical tests of the relationship between assays of immunity and resistance to a range of actual pathogens are important for correctly interpreting these measures.

Neuromodulators can resculpt neural circuits, giving an animal the behavioral flexibility it needs to survive in a complex changing world. This ability, however, provides parasites with a potential mechanism for manipulating host behavior. This paper reviews three invertebrate host-parasite systems to examine whether parasites can change host behavior by secreting neuromodulators. The parasitic wasp, Cotesia congregata, suppresses host feeding partly by inducing the host (Manduca sexta) to increase the octopamine concentration in its hemolymph. The increased octopamine concentration disrupts the motor pattern produced by the frontal ganglion, preventing the ingestion of food. Polymorphus paradoxus (Acanthocephalan) alters the escape behavior of its host, Gammarus lacustris (Crustacea), possibly through an effect on the host's serotonergic system. The trematode Trichobilharzia ocellata inhibits egg-laying in its snail host (Lymnaea stagnalis), partly by inducing the host to secrete schistosomin. Schistosomin decreases electrical excitability of the caudodorsal cells. The parasite also alters gene expression for some neuromodulators within the host's central nervous system. In at least two of these three examples, it appears that the host, not the parasite, produces the neuromodulators that alter host behavior. Producing physiologically potent concentrations of neuromodulators may be energetically expensive for many parasites. Parasites may exploit indirect less energetically expensive methods of altering host behavior. For example, parasites may induce the host's immune system to produce the appropriate neuromodulators. In many parasites, the ability to manipulate host behavior may have evolved from adaptations designed to circumvent the host's immune system. Immune-neural-behavioral connections may be pre-adapted for parasitic manipulation., (Copyright 2003 S. Karger AG, Basel)

Animals should increase their present reproductive output if their chances for future reproduction are low. However, an animal's ability to make this adjustment may be constrained by the physiological mechanisms mediating the response. To examine this hypothesis, I infected 2- and 5-week-old female crickets, Acheta domesticus, with either a pathogen (the bacterium Serratia marcescens) that induces antimicrobial immune responses, or a parasite (larvae of the parasitoid fly, Ormia ochracea) that induces an encapsulation immune response. Females of both age groups infected with bacteria laid more eggs the day after injection than did saline-injected crickets. A similar increase was elicited by injecting components of the bacterial cell wall (lipopolysaccharides). The bacteria-induced increase in egg laying (1) was not the result of physical stress, (2) did not appear to be a nonspecific response to the infection, and (3) was probably not mediated by octopamine. Females did not increase egg laying when infested with O. ochracea, even though this parasitoid invariably kills its host. Injections of Sephadex beads, which induced an immune response similar to that created by the parasitoids, also had no effect on egg laying. These results are consistent with the hypotheses that crickets can increase egg laying in response to infection and that increased egg output correlates with the activation of some, but not all, immune responses. Copyright 1999 The Association for the Study of Animal Behaviour.