Thermal biology in insect-parasite interactions

https://doi.org/10.1016/S0169-5347(03)00069-7Get rights and content

Abstract

Recently, several applied studies exploring the use of pathogens for insect biocontrol have demonstrated significant effects of environmental temperature on the outcome of infection. For example, host resistance, host recovery, pathogen virulence and replication can alter considerably with sometimes very small changes in temperature. Moreover, the effectiveness of certain insect parasitoids and the activity of endosymbionts can vary across the range of realistic temperatures experienced in the field. These responses are not necessarily linear or immediately predictable, because they derive from a complex ‘genotype-by-genotype-by-environment’ interaction. Given the importance of parameters such as virulence and resistance in determining the course of a host–parasite interaction, such effects of temperature could have profound implications for host–parasite dynamics and coevolution.

Section snippets

Effects of temperature on host–pathogen/parasite interactions

Driven by the desire to develop alternatives to chemical insecticides, there have been many studies exploring the potential of pathogens and parasites for use in biological pest control [1]. A common starting point for most of this work is the investigation of dose responses and host mortality rates under constant laboratory conditions. The resulting measures of ld50 and lt50 are then used to select the most promising (virulent) agents for further testing in the field. This approach is also

Beyond hosts and their parasites

The examples we have discussed concern insect hosts and their parasites. However, it is also possible to identify effects of temperature on associations that are not strictly parasitic. For instance, endosymbiotic rickettsia and other bacteria have been isolated from a diversity of host organisms and have a range of effects on host biology 30, 31, 32. Interestingly, although at least some of these endosymbionts are obligate partners, several studies illustrate a difference in thermal

Mechanisms: parasite growth and host defence

The effects of temperature on a host–parasite interaction depend on the thermal sensitivity profiles and the environmental variability (Box 1). When both host and parasite share the same thermal optima and are adapted to perform similarly across a temperature range, the effects of temperature can be simple. However, when host and parasite have more discrete thermal performance profiles and temperatures regularly fluctuate across the range of these reaction norms, the nonlinearities in the

Implications for population dynamics and the evolution of host–parasite interactions

Although there are very few published studies that examine the consequences of temperature-induced effects on host–parasite population dynamics, measures of host susceptibility, host recovery, latent period of infection, pathogen-induced mortality rate (virulence) and pathogen replication are included in some form in most host–parasite models. As previously discussed, temperature can impact on all of these parameters, either singly or in combination. It follows then that temperature must impact

Conclusions and recommendations

Our key message here is that, in studying host–parasite interactions, environment matters. More specifically, the course of an interaction is determined by host body temperature, which, depending on thermal behaviour, might not be close to ambient. Where some distinction exists between thermal sensitivity profiles of host and parasite, environmental temperature, via its influence on host body temperature, might have complex effects that are not necessarily immediately predictable.

Clearly,

Acknowledgements

We are grateful to three anonymous reviewers for helpful comments on the article. The paper forms a part contribution to the EU-funded ‘Environmentally Sustainable Locust Control Programme (ESLOCO - QLK5-CT-1999-01118)’ and the project ‘Development of biologically based strategies for sustainable control of red locust in Central and Southern Africa’ funded by United Kingdom Department for International Development (DFID) for the benefit of developing countries (R7818 Crop Protection Research

Glossary

Glossary

Acridid:
family of grasshoppers with short antennae. The acridids include the locusts that are a select group of grasshoppers able to pass into a swarming phase subject to the right environmental conditions.
Behavioural thermoregulation:
the use of behaviour, such as avoiding or seeking sources of heat, to regulate body temperature.
Cellular and humoral defense mechanisms:
refers to the two components of the insect immune system. The humoral response consists of soluble factors in the blood such as

References (83)

  • N.C. Franc et al.

    Innate recognition systems in insect immunity: new approaches in Drosophila

    Microbes Infect.

    (2000)
  • G. Dimopoulos

    Innate immune defence against malaria infection in mosquito

    Curr. Opin. Immunol.

    (2001)
  • P.M. Kelly et al.

    In vivo mass production in the cabbage moth (Mamestra brassicae) of a heterologous (Panolis) and homologous (Mamestra) nuclear polyhedrosis virus

    J. Virol. Methods

    (1988)
  • M. Bonsall

    Evolutionary and ecological aspects of disease and parasitism

    Trends Ecol. Evol.

    (2002)
  • R.B. Huey et al.

    Evolution of thermal sensitivity of ectotherm performance

    Trends Ecol. Evol.

    (1989)
  • R. Malakar

    Within-host interactions of Lymatria dispar (Lepidoptera: Lymantridae) nucleopolyhedrosis virus and Entomophaga maimaiga (Zygomycetes: Entomophthorales)

    J. Invertebr. Pathol.

    (1999)
  • D.W. Johnson

    A temperature-dependent development model for a nucleopolyhedrosis virus of the velvetbean caterpillar Anticarsia gemmatalis (Lepidoptera: Noctuidae)

    J. Invertebr. Pathol.

    (1982)
  • H. Dreisig

    Control of body temperature by shuttling ectotherms

    J. Therm. Biol.

    (1984)
  • S. Blanford et al.

    Host thermal biology: the key to understanding insect–pathogen interactions and microbial pest control?

    Agric. Forest Entomol.

    (1999)
  • S. Blanford et al.

    Role of thermal biology in disease dynamics

    Aspects Appl. Biol.

    (1999)
  • D.G. Inglis

    Effects of temperature and thermoregulation on mycosis by Beauveria bassiana in grasshoppers

    Biol. Contr.

    (1996)
  • D.G. Inglis

    Effects of temperature and sunlight on mycosis (Beauveria bassiana) (Hyphomycetes: Sympodulosporae) of grasshoppers under field conditions

    Environ. Entomol.

    (1997)
  • S. Arthurs et al.

    Effects of a mycoinsecticide on feeding and fecundity of the brown locust, Locustana pardalina

    Biocontr. Sci. Technol.

    (2000)
  • S. Blanford et al.

    Thermoregulation by two acridid species: effects of habitat and season on thermal behaviour and the potential impact on biocontrol with pathogens

    Environ. Entomol.

    (2000)
  • C.J. Lomer

    Biological control of locusts and grasshoppers

    Annu. Rev. Entomol.

    (2001)
  • R.F. Chapman et al.

    Factors affecting the mortality of the grasshopper, Zonocerus variegatus, in Southern Nigeria

    J. Anim. Ecol.

    (1979)
  • S. Blanford

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

    Agric. Forest Entomol.

    (2000)
  • R.I. Carruthers

    Influence of thermal ecology on the mycosis of a rangeland grasshopper

    Ecology

    (1992)
  • A.E. Hajek

    Modelling the dynamics of E. maimaiga (Zygomycetes: Entomophthorales) epizootics in gypsy moth (Lepidoptera: Lymantriidae) populations

    Environ. Entomol.

    (1993)
  • S. Blanford

    Temperature checks the Red Queen? Resistance and virulence in a variable environment

    Ecol. Lett.

    (2003)
  • Stacey, D.A. et al. Genotype and temperature influence pea aphid resistance to a fungal entomopathogen. Physiol....
  • R.L. Yadava

    Studien über den einfluß von temperatur und relativer luftfeuchtigkeit auf die entwicklung der kernpolyedrose der Nonne (Lymantria monacha L.) und des Schwammspinners (L. dispar L.)

    Z. Agnew Entomol.

    (1970)
  • M.A. Mohamed

    Temperature and crowding effects on virus manifestation in Neodiprion sertifer (Hymenoptera: Diprionidae) larvae

    Great Lakes Entomol.

    (1985)
  • S.A. Adamo

    The specificity of behavioural fever in the cricket Acheta domesticus

    J. Parasitol.

    (1998)
  • L. Frid et al.

    Thermal ecology of western tent caterpillars, Malacosoma californnicum pluviale, and infection by nucleopolyhedrovirus

    Ecol. Entomol.

    (2002)
  • H. Menti

    Infectivity of populations of the entomoptahogenic nematodes Steinernema feltiae and Heterorhabditis megidis in relation to temperature, age and lipid content

    Nematology

    (2000)
  • A.R. Kraaijeveld et al.

    Trade-off between parasitoid resistance and larval competitive ability in Drosophila melanogaster

    Nature

    (1997)
  • M.D.E. Fellowes

    Cross resistance following artificial selection for increased host defence against parasitoids in Drosophila melanogaster

    Evolution

    (1999)
  • D. Blumberg

    Seasonal variations in the encapsulation of eggs of the encyrtid parasitoid, Metaphycus stanleyi, by the pyriform scale, Protopulvinaria pyriformis

    Entomol. Exp. Appl.

    (1991)
  • L. Sigsgaard

    The temperature-dependent duration of development and parasitism of three cereal aphid parasitoids, Aphidius ervi, A. rhopalosiphi, and Praon volucre

    Entomol. Exp. Appl.

    (2000)
  • S.S. Liu

    The biology of Daidromus collaris (Hymenoptera: Ichneumonidae), a pupal parasitoid of Plutella xylostella (Lepidoptera: Plutellidae), and its interaction with Oomyzus sokolowskii (Hymenoptera: Eulophidae)

    Bull. Entomol. Res.

    (2001)
  • Cited by (389)

    • Sex dependent transcriptome responses of the diamondback moth, Plutella xylostella L. to cold stress

      2023, Comparative Biochemistry and Physiology - Part D: Genomics and Proteomics
    • Biopesticides: commercial opportunities and challenges

      2023, Development and Commercialization of Biopesticides: Costs and Benefits
    View all citing articles on Scopus
    View full text