Abstract
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.
References
Adamo SA (1998) The specificity of behavioral fever in the cricket Acheta domesticus. J Parasitol 84:529–533
Adamo SA, Lovett MME (2011) Some like it hot: the effects of climate change on reproduction, immune function and disease resistance in the cricket Gryllus texensis. J Exp Biol 214:1997–2004
Adamo SA, Baker JL, Lovett MME, Wilson G (2012) Climate change and temperate zone insects: the tyranny of thermodynamics meets the world of limited resources. Environ Entomol 41:1644–1652
Angilletta MJ (2009) Thermal adaptation: a theoretical and empirical synthesis. Oxford University Press, Oxford
Ardia DR, Gantz JE, Schneider BC, Strebel S (2012) Costs of immunity in insects: an induced immune response increases metabolic rate and decreases antimicrobial activity. Funct Ecol 26:732–739
Ballabeni P, Benway H, Jaenike J (1995) Lack of behavioral fever in nematode-parasitized drosophila. J Parasitol 81(5):670–674
Blanford S, Thomas MB, Langewald J (1998) Behavioural fever in the Senegalese grasshopper, Oedaleus senegalensis, and its implications for biological control using pathogens. Ecol Entomol 23:9–14
Blanford S, Thomas MB, Langewald (2000) Thermal ecology of Zonocerus variegatus and its effects on biocontrol using pathogens. Agric For Entomol 2(1):3–10
Blanford S, Read AF, Thomas MB (2009) Thermal behaviour of Anopheles stephensi in response to infection with malaria and fungal entomopathogens. Malaria J 8:72
Boorstein SM, Ewald PW (1987) Costs and benefits of behavioral fever in melanoplus-sanguinipes infected by nosema-acridophagus. Physiol Zool 60(5):586–595
Bundey S, Raymond S, Dean P, Roberts SK, Dillon RJ, Charnley AK (2003) Eicosanoid involvement in the regulation of behavioral fever in the desert locust, Schistocerca gregaria. Arch Insect Biochem Physiol 52:183–192
Campbell J, Kessler B, Mayack C, Naug D (2010) Behavioural fever in infected honeybees: parasitic manipulation or coincidental benefit? Parasitology 137(10):1487–1491
Catalan TP, Niemeyer HM, Kalergis AM, Bozinovic F (2012) Interplay between behavioural thermoregulation and immune response in mealworms. J Insect Physiol 58(11):1450–1455
Dirnagl U, Lauritzen M (2010) Fighting publication bias: introducing the Negative Results section. J Cereb Blood Flow Metab 30:1263–1264
Elliot SL, Blanford S, Thomas MB (2002) Host-pathogen interactions in a varying environment: temperature, behavioural fever and fitness. Proc R Soc B 269(1500):1599–1607
Elliot SL, Horton CM, Blanford S, Thomas MB (2005) Impacts of fever on locust life-history traits: costs or benefits? Biol Lett 2:181–184
Frid L, Myers JH (2002) Thermal ecology of western tent caterpillars Malacosoma californicum pluviale and infection by nucleopolyhedrovirus. Ecol Entomol 27(6):665–673
Gillespie JP, Kanost MR, Trenczek T (1997) Biological mediators of insect immunity. Ann Rev Entomol 42:611–643
Hedrick AV, Perez D, Lichti N, Yew J (2002) Temperature preferences of male field crickets (Gryllus integer) alter their mating calls. J Comp Physiol A 188:799–805
Hunt VL, Charnley AK (2011) The inhibitory effect of the fungal toxin, destruxin A, on behavioural fever in the desert locust. J Insect Physiol 57(10):1341–1346
Hunt VL, Lock GD, Pickering SG, Charnley AK (2011) Application of infrared thermography to the study of behavioural fever in the desert locust. J Therm Biol 36:443–451
Inglis GD, Johnson DL, Goettel MS (1996) Effects of temperature and thermoregulation on mycosis by Beauveria bassiana in grasshoppers. Biol Control 7(2):131–139
Kluger MJ (1990) The febrile response. In: Morimoto R, Tissieres A, Georgopoulos C (eds) Stress proteins in biology and medicine. Cold Spring Harbor Laboratory, Cold Spring Harbor, pp 61–78
Kluger MJ, Kozak W, Conn CA, Leon LR, Soszynski D (1998) Role of fever in disease. Ann N Y Acad Sci 856:224–233
Louis C, Jourdan M, Cabanac M (1986) Behavioral fever and therapy in a rickettsia-infected orthoptera. Am J Physiol 250(6):R991–R995
McClain E, Magnuson P, Warner SJ (1988) Behavioral fever in a namib desert tenebrionid beetle, onymacris-plana. J Insect Physiol 34(4):279–284
Moore J (2002) Parasites and behavior of animals. Oxford University Press, Oxford
Moore J, Freehling M (2002) Cockroach hosts in thermal gradients suppress parasite development. Oecologia 133(2):261–266
Müller CB, Schmidt-Hempel P (1993) Exploitation of cold temperature as defence against parasitoids in bumblebees. Nature 363:65–67
Nespolo RF, Lardies MA, Bozinovic F (2003) Intrapopulational variation in the standard metabolic rate of insects: repeatability, thermal dependence and sensitivity (Q10) of oxygen consumption in a cricket. J Exp Biol 206:4309–4315
Otti O, Gantenbein-Ritter I, Jacot A, Brinkhof MWG (2012) Immune response increases predation risk. Evolution 66:732–739
Springate S, Thomas MB (2005) Thermal biology of the meadow grasshopper, Chorthippus parallelus, and the implications for resistance to disease. Ecol Entomol 30(6):724–732
Stahlschmidt ZR, Rollinson NJ, Acker M, Adamo SA (2013) Are all eggs created equal? Food availability and the fitness tradeoff between reproduction and immune function. Funct Ecol, in press
Starks PT, Blackie CA, Seeley TD (2000) Fever in honeybee colonies. Naturwissenschaften 87(5):229–231
Acknowledgments
We appreciate the funding support by the Killam Trusts Foundation (to Z.R.S. and S.A.A.) and the National Science and Engineering Research Council of Canada (to S.A.A.), and Madison Acker, Jillian Baker, and Robbin McKee for the assistance. We thank three anonymous reviewers for the helpful feedback on the paper.
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Communicated by: Sven Thatje
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Stahlschmidt, Z.R., Adamo, S.A. Context dependency and generality of fever in insects. Naturwissenschaften 100, 691–696 (2013). https://doi.org/10.1007/s00114-013-1057-y
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DOI: https://doi.org/10.1007/s00114-013-1057-y