Abstract
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.
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References
Adamo SA (1998) The specificity of behavioral fever in the cricket Acheta domesticus. J Parasitol 84:529–533
Arthurs S, Thomas MB (2000) Effect of a mycoinsecticide on feeding and fecundity of the brown locust Locustana pardalina. Biocontrol Sci Technol 10:321–329
Beckage NE (1997) Parasites and pathogens. Effects on host hormones and behavior. Chapman and Hall, New York
Blanford S, Thomas MB (1999) Host thermal biology: the key to understanding host-pathogen interactions and microbial pest control? Agric For Entomol 1:195–202
Blanford S, Thomas MB (2000) Thermal behavior of two acridid species: effects of habitat and season on body temperature and the potential impact on biocontrol with pathogens. Environ Entomol 29:1060–1069
Blanford S, Thomas MB (2001) Adult survival, maturation, and reproduction of the desert locust Schistocerca gregaria infected with the fungus Metarhizium anisopliae var acridum. J Invertebr Pathol 78:1-8
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
Boorstein SM, Ewald PW (1987) Costs and benefits of behavioral fever in Melanoplus sanguinipes infected by Nosema acridophagus. Physiol Zool 60:586–595
Brodeur J, McNeil JN (1989) Seasonal microhabitat selection by an endoparasitoid through adaptive modification of host behavior. Science 244:226–228
Brodeur J, McNeil JN (1992) Host behaviour modification by the endoparasitoid Aphidius nigripes: a strategy to reduce hyperparasitism. Ecol Entomol 17:97–104
Brodeur J, Rosenheim JA (2000) Intraguild interactions in aphid parasitoids. Entomol Exp Appl 97:93–108
Brooks WM (1993) Host-parasitoid-pathogen interactions. In: Beckage NE, Thompson SN, Federici BA (eds) Parasites and pathogens of insects. Pathogens, vol 2. Academic Press, San Diego, pp 231–272
Cabanac M (1990) Phylogeny of fever. In: Bligh J, Voight K (eds) Thermoreception and temperature regulation. Springer, Berlin Heidelberg New York, pp 284–296
Carruthers RI, Larkin TS, Firstencel H (1992) Influence of thermal ecology on the mycosis of a rangeland grasshopper. Ecology 73:190–204
Casey TM (1981) Behavioural mechanisms of thermoregulation. In: Heinrich B (ed) Insect thermoregulation. Wiley, New York, pp 79–114
Chappell MA, Whitman DW (1990) Grasshopper thermoregulation. In: Chapman RF (ed) Biology of grasshoppers. Wiley Interscience, New York, pp 143–172
Elliot SL, Blanford S, Thomas MB (2002) Host-pathogen interactions in a varying environment: temperature, behavioural fever and fitness. Proc R Soc Lond B Biol Sci 269:1599–1607
Fargues J, Ouedraogo A, Goettel MS, Lomer CJ (1997) Effects of temperature, humidity and inoculation method on susceptibility of Schistocerca gregaria to Metarhizium flavoviride. Biocontrol Sci Technol 7:345–356
Gardner SN, Thomas MB (2002) Costs and benefits of fighting infection in locusts. Evol Ecol Res 4:109–131
Gillespie JP, Kanost MR, Trenczek T (1997) Biological mediators of insect immunity. Annu Rev Entomol 42:611–643
Hajek AE, St-Leger RJ (1994) Interactions between fungal pathogens and insect hosts. Annu Rev Entomol 39:293–321
Hart BL (1988) Biological basis of the behavior of sick animals. Neurosci Behav Rev 12:123–137
Heinrich B (1981) Insect thermoregulation. Wiley, New York
Hoffmann JA, Reichart J-M, Hetru C (1996) Innate immunity in higher insects. Curr Opin Immunol 8:8–13
Holmes JC, Bethel WM (1972) Modification of intermediate host behaviour by parasites. Zool J Linn Soc 51 [Suppl 1]:123–149
Horton DR, Moore J (1993) Behavioral effects of parasites and pathogens in insect hosts. In: Beckage NE, Thompson SN, Federici BA (eds) Parasites and pathogens of insects. Parasites, vol 1. Academic Press, San Diego, pp 107–124
Inglis DG, Johnson DL, Goettel MS (1996) Effects of temperature and thermoregulation on mycosis by Beauveria bassiana in grasshoppers. Biol Control 7:131–139
Inglis DG, Duke GM, Kawchuk LM, Goettel MS (1999) Influence of oscillating temperatures on the competitive infection and colonization of the migratory grasshopper by Beauveria bassiana and Metarhizium flavoviride. Biol Control 14:111–120
Johnson DL, Pavlikova E (1986) Reduction of consumption by grasshoppers (Orthoptera: Acrididae) infected with Nosema locustae Canning (Microsporidia: Nosematidae). J Invertebr Pathol 48:232–238
Karban R (1998) Caterpillar basking behavior and nonlethal parasitism by tachinid flies. J Insect Behav 11:713–723
Kleespies RG, Zimmermann G (1992) Production of blastospores by three strains of Metarhizium anisopliae (Metch) Sorokin in submerged culture. Biocontrol Sci Technol 2:127–135
Kluger MJ (1979) Fever, its biology, evolution and function. Princeton University Press, Princeton
Kluger MJ (1991) The adaptive value of fever. In: Mackowiak PA (ed) Fever: basic mechanisms and management. Raven Press, New York, pp 105–124
Kluger MJ, Kozak JW, Conn CA, Leon LR, Sosynski D (1996) The adaptive value of fever. Infect Dis Clin North Am 10:1–20
Lactin DJ, Johnson DL (1995) Temperature-dependent feeding rates of Melanoplus sanguinipes nymphs (Orthoptera: Acrididae) in laboratory trials. Physiol Chem Ecol 24:1291–1296
Lomer CJ, Prior C, Kooyman C (1997) Development of Metarhizium spp. for the control of grasshoppers and locusts. In: Goettel MS, Johnson LD (eds) Microbial control of grasshoppers and locusts. Mem Entomol Soc Can 171:265–286
Louis C, Jourdan M, Cabanac M (1986) Behavioural fever and therapy in a rickettsia-infected Orthoptera. Am J Physiol 34:279–284
May M (1979) Insect thermoregulation. Annu Rev Entomol 24:313–349
Moore D, Reed M, Le Patourel G, Abraham YJ, Prior C (1992) Reduction of feeding by the desert locust, Schistocerca greagaria, after infection with Metarhizium flavoviride. J Invertebr Pathol 60:304–307
Moore J (2002) Parasites and the behavior of animals. Oxford University Press, New York
Moore J, Gotelli NJ (1996) Evolutionary patterns of altered behavior and susceptibility in parasitized hosts. Evolution 50:807–819
Muchlinski AE (1985) The energetic cost of the fever response in three species of ectothermic vertebrates. Comp Biochem Physiol 81A:577–579
Ouedraogo MR (2002) Fièvre comportementale des acridiens (Orthoptera: Acridoidae): rôle de la thermorégulation dans la défense immunitaire contre les mycoses induites par les champignons entomopathogènes (Hyphomycètes). PhD Thesis, University of Laval, Quebec, Canada
Ouedraogo A, Fargues J, Goettel MS, Lomer CJ (1997) Effect of temperature on vegetative growth among isolates of Metarhizium anisopliae and M. flavoviride. Mycopathology 137:37–43
Ouedraogo MR, Kamp A, Goettel MS, Brodeur J, Bidochka MJ (2002) Attenuation of fungal infection in thermoregulating Locusta migratoria is accompanied by changes in hemolymphal proteins. J Invertebr Pathol 81:19–24
Ouedraogo MR, Cusson M, Goettel MS, Brodeur J (2003) Inhibition of fungal growth in thermoregulating locusts, Locusta migratoria, infected by the fungus Metarhizium anisopliae var acridum. J Invertebr Pathol 82:103–109
Poulin R (1995) “Adaptive” changes in the behaviour of parasitized animals: a critical review. Int J Parasitol 25:1371–1383
Prior C, Greathead DJ (1989) Biological control of locusts: the potential for the exploitation of pathogens. FAO Plant Prot Bull 37:37–48
Roxburgh L, Pinshow B, Prange DH (1996) Temperature regulation by evaporative cooling in a desert grasshopper, Calliptamus barbarus (Ramme, 1951). J Therm Biol 21:331–337
Sambeek VJ, Weisner A (1999) Successful parasitation of locusts by entomopathogenic nematodes is correlated with inhibition of insect phagocytes. J Invertebr Pathol 73:154–161
SAS Institute (2000) SAS/STAT, Version 8. SAS Institute, Cary, N.C., USA
Sayeed O, Benzer S (1996) Behavioral genetics of thermosensation and hygrosensation in Drosophila. Proc Natl Acad Sci USA 93:6079–6084
Seyoum E, Moore D, Charnley AK (1994) Reduction in flight and food consumption by the desert locust, Schistocerca gregaria, Forskal (Orth., Cyrtacanthacrinae), after infection with Metarhizium flavoviride. J Appl Entomol 118:310–315
Sokal RR, Rohlf FJ (1981) Biometry, 2nd edn. Freeman, New York
Thomas MB, Jenkins NE (1997) Effects of temperature on growth of Metarhizium flavoviride and virulence to the variegated grasshopper, Zonocerus variegatus. Mycol Res 101:1460–1474
Thomas MB, Blanford S, Lomer CJ (1997) Reduction of feeding by the variegated grasshopper, Zonocerus variegatus, following infection by the fungal pathogen, Metarhizium flavoviride. Biocontrol Sci Technol 7:327–334.
Tyrrell D (1990) Pathogenesis of Entomophaga aulicae. I. Disease symptoms and effect of infection on weight gain of infected Choristoneura fumiferana and Malacosoma disstria larvae. J Invertebr Pathol 56:150–156
Uvarov B (1977) Grasshoppers and locusts. A handbook of general acridology, vol 2. Centre for Overseas Pest Research, London, UK
Watson DW, Mullens BA, Petersen JJ (1993) Behavioural response of Musca domestica (Diptera: Muscidae) to infection by Entomophthora muscae (Zygomycetes: Entomophtorales). J Invertebr Pathol 61:10–16
Zimmermann G (1982) Effect of high temperature and artificial sunlight on the viability of conidia of Metarhizium anisopliae. J Invertebr Pathol 40:36–40
Acknowledgements
We thank D. Auclair, M. Fournier, J. Blais, and N. Shallow for technical assistance; G. Daigle for his help in the statistical analyses; J. Langewald from the LUBILOSA program for providing locust eggs and fungal isolate IMI 330189; and C. Cloutier, C. Cusson, A. Hajek, and M. Thomas for useful comments on an earlier version of this manuscript. This work was supported by a scholarship from the Programme Canadien des Bourses de la Francophonie and the government of Burkina Faso to R.M.O., and a grant from the Natural Sciences and Engineering Research Council of Canada (NSERC) to J.B. This is LRC Contribution number 387-02026.
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Ouedraogo, R.M., Goettel, M.S. & Brodeur, J. Behavioral thermoregulation in the migratory locust: a therapy to overcome fungal infection. Oecologia 138, 312–319 (2004). https://doi.org/10.1007/s00442-003-1431-0
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DOI: https://doi.org/10.1007/s00442-003-1431-0