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Identifying environmental drivers of insect phenology across space and time: Culicoides in Scotland as a case study

Published online by Cambridge University Press:  30 July 2012

K.R. Searle ,
A. Blackwell ,
D. Falconer ,
M. Sullivan ,
A. Butler  and
B.V. Purse
K.R. Searle*
Affiliation:
Centre for Ecology and Hydrology, Bush Estate, Edinburgh, EH26 0QB
A. Blackwell
Affiliation:
Advanced Pest Solutions Ltd, Prospect Business Centre, Gemini Crescent, Dundee Technology Park, Dundee, DD2 1T
D. Falconer
Affiliation:
Advanced Pest Solutions Ltd, Prospect Business Centre, Gemini Crescent, Dundee Technology Park, Dundee, DD2 1T
M. Sullivan
Affiliation:
Advanced Pest Solutions Ltd, Prospect Business Centre, Gemini Crescent, Dundee Technology Park, Dundee, DD2 1T
A. Butler
Affiliation:
Biomathematics and Statistics Scotland, James Clerk Maxwell Building, The King's Buildings, Mayfield Road, Edinburgh, EH9 3JZ
B.V. Purse
Affiliation:
Centre for Ecology and Hydrology, Bush Estate, Edinburgh, EH26 0QB
*
*Author for correspondence Fax: +44 (0)131 4453943 E-mail: [email protected]
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Abstract

Interpreting spatial patterns in the abundance of species over time is a fundamental cornerstone of ecological research. For many species, this type of analysis is hampered by datasets that contain a large proportion of zeros, and data that are overdispersed and spatially autocorrelated. This is particularly true for insects, for which abundance data can fluctuate from zero to many thousands in the space of weeks. Increasingly, an understanding of the ways in which environmental variation drives spatial and temporal patterns in the distribution, abundance and phenology of insects is required for management of pests and vector-borne diseases. In this study, we combine the use of smoothing techniques and generalised linear mixed models to relate environmental drivers to key phenological patterns of two species of biting midges, Culicoides pulicaris and C. impunctatus, of which C. pulicaris has been implicated in transmission of bluetongue in Europe. In so doing, we demonstrate analytical tools for linking the phenology of species with key environmental drivers, despite using a relatively small dataset containing overdispersed and zero-inflated data. We demonstrate the importance of landcover and climatic variables in determining the seasonal abundance of these two vector species, and highlight the need for more empirical data on the effects of temperature and precipitation on the life history traits of palearctic Culicoides spp. in Europe.

Keywords

climateinsect phenologylandcoverspatio-temporal patternsvector-borne disease
Type
Research Paper
Information
Bulletin of Entomological Research , Volume 103 , Issue 2 , April 2013 , pp. 155 - 170
Copyright
Copyright © Cambridge University Press 2012

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References

Akey, D.H., Potter, H.W. & Jones, R.H. (1978) Effects of rearing temperature and larval density on longevity, size and fecundity in the biting gnat Culicoides viriipennis. Annals of the Entomological Society of America 71, 411–418.Google Scholar
Allingham, P. (1991) Effect of temperature on late immature stage of Culicoides brevitarsis (Diptera: Ceratopogonidae). Journal of Medical Entomology 28, 878–881.Google Scholar
Baylis, M., Mellor, P.S., Wittmann, E.J. & Rogers, D.J. (2001) Prediction of areas around the Mediterranean at risk of bluetongue by modelling the distribution of its vector using satellite imaging. Veterinary Record 149, 639–643.CrossRefGoogle ScholarPubMed
Birley, M.H. & Boorman, J.P.T. (1982) Estimating the survival and biting rates of haematophagus insects, with particular reference to the Culicoides obsoletus group (Diptera: Ceratopogonidae) in southern England. Journal of Animal Ecology 51, 135–148.CrossRefGoogle Scholar
Bishop, A.L., McKenzie, H.J., Barchia, I.M. & Harris, A.M. (1996) Effect of temperature regimes on the development, survival and emergence of Culicoides brevitarsis Kieffer (Diptera: Ceratopogonidae). Australian Journal of Entomology 35, 361–168.CrossRefGoogle Scholar
Blackwell, A. (1997) Diel flight periodicity of the biting midge Culicoides impunctatus and the effects of meteorological conditions. Medical and Veterinary Entomology 11, 361–367.CrossRefGoogle ScholarPubMed
Blackwell, A., Mordue, A.J., Young, M.R. & Mordue, W. (1992) Bivoltinism, survival rates and reproductive characteristics of the Scottish biting midge, Culicoides impunctatus, (Diptera: Ceratopogonidae) in Scotland. Bulletin of Entomological Research 82, 299–306.CrossRefGoogle Scholar
Boorman, J. (1986) British Culicoides Diptera Ceratopogonidae notes on distribution and biology. Entomologist's Gazette 37, 253–266.Google Scholar
Boorman, J. & Goddard, P. (1970) Observations on the biology of Culicoides impunctatus Goetgh. (Dipt., Ceratopogonidae) in southern England. Bulletin of Entomological Research 60, 189–198.CrossRefGoogle ScholarPubMed
Braverman, Y. & Mumcuoglu, K.Y. (2009) Newly emerged nulliparous Culicoides imicola Kieffer (Diptera: Ceratopogonidae) with pigmented abdomen. Medical and Veterinary Entomology 160, 356–358.Google ScholarPubMed
Campbell, J.A. & Pelham-Clinton, E.C. (1960) A taxonomic review of the British species of Culicoides Latreille (Diptera: Ceratopogonidae). Proceedings of the Royal Society of Edinburgh B, LXVII 21, 181–301.Google Scholar
Caracappa, S., Torina, A., Guerico, A., Vitale, F., Calabro, A., Ferrantelli, G., Vitale, M. & Mellor, P.S. (2003) Identification of a novel bluetongue virus vector species of Culicoides in Sicily. Veterinary Record 153, 71–74.CrossRefGoogle ScholarPubMed
Dyce, A.L. (1969) The recognition of nulliparous and parous Culicoides (Diptera: Ceratopoginidae) without dissection. Australia Journal of Entomology 8, 11–15.CrossRefGoogle Scholar
Eber, S. (2004) Bottom-up density regulation in the holly leaf-miner Phytomyza ilicis. Journal of Animal Ecology 73, 948–958.Google Scholar
Edwards, P.B. (1982) Laboratory observations on the biology and life cycle of the Australian biting midge Culicoides subimmaculatus (Diptera: Ceratopogonidae). Journal of Medical Entomology 19, 545–552.Google Scholar
EEA (European Environment Agency) (2000) Corine Landcover 2000: mapping a decade of change. Copenhagen, Denmark, European Environment Agency.Google Scholar
Gelman, A. & Hill, J. (2007) Data Analysis Using Regression and Multilevel/Hierarchical Models. New York, USA, Cambridge University Press.Google Scholar
Gelman, A. & Rubin, D.B. (1992) Inference from iterative simulation using multiple sequences. Statistical Science 7, 457–511.CrossRefGoogle Scholar
Gern, L., Cadenas, F.M. & Burri, C. (2008) Influence of some climatic factors on Ixodes ricinus ticks studied along altitudinal gradients in two geographic regions in Switzerland. International Journal of Medical Microbiology 298, 55–59.Google Scholar
Haylock, M.R., Hofstra, N., Klein Tank, A.M.G., Klok, E.J., Jones, P.D. & New, M. (2008) A European daily high-resolution gridded dataset of surface temperature and precipitation. Journal of Geophysical Research (Atmospheres) 113, 1–12.Google Scholar
Heffernan, J.M., Smith, R.J. & Wahl, L.M. (2005) Perspectives on the basic reproductive ratio. Journal of the Royal Society Interface 2, 281–293.Google Scholar
Hendry, G. & Goodwin, G. (1988) Biting midges in Scottish forestry: a costly irritant or a trivial nuisance? Scottish Forestry 42, 113–119.Google Scholar
Hill, M.A. (1947) The lifecycle and habits of Culicoides impunctatus Goetghebuer and Culicoides obsoletus Meigen, together with some observations on the lifecycle of Culicoides pallidicornis Kieffer, Culicoides cubitalis Edwards and Culicoides chiopterus Meigen. Annals of Tropical Medicine and Parasitology 41, 55–115.CrossRefGoogle Scholar
Hodgson, J.A., Thomas, C.D., Oliver, T.H., Anderson, B.J., Brereton, T.M. & Crones, E.E. (2010) Predicting insect phenology across space and time. Global Change Biology 17, 1289–1300.CrossRefGoogle Scholar
Hoeting, J.A. (2009) The importance of accounting for spatial and temporal correlation in analyses of ecological data. Ecological Applications 19, 574–577.CrossRefGoogle ScholarPubMed
Holmes, P.R. & Birley, M.H. (1987) An improved method for survival rate analysis from time series of haematophagus Dipteran populations. Journal of Animal Ecology 56, 427–440.Google Scholar
Holmes, P.R. & Boorman, P.T. (1987) Light suction trap catches of Culicoides midges in southern England. Medical and Veterinary Entomology 1, 349–359.Google Scholar
Hunt, G.J., Tabachnick, W.J. & McKinnon, C.N. (1989) Environmental factors affecting mortality of adult Culicoides variipennis (Diptera: Ceratopogonidae) in the laboratory. Journal of the American Mosquito Control Association 5, 387–391.Google Scholar
Institute for Animal Health (2011) Culicoides. NET: Incorporating the UK Culicoides reference laboratory. Available online at http://www.culicoides.net, (accessed 17 November 2011).Google Scholar
Kettle, D.S. (1950) The seasonal distribution of Culicoides impunctatus Goetghebuer (Diptera: Heleidae (Ceratopogonidae)) with a discussion on the possibility that it may be composed of two or more biological races. Transactions of the Royal Society of London 101, 125–145.Google Scholar
Kettle, D.S., Edwards, P.B. & Barnes, A. (1998) Factors affecting numbers of Culicoides in truck traps in Coastal Queensland. Medical and Veterinary Entomology 12, 367–377.Google Scholar
Kitoaka, S. (1982) Effects of rearing temperature on length of larval period and size in adults Culicoides arakawae and Culicoides maculates. National Institute for Animal Health Quarterly (Japan) 22, 159–162.Google Scholar
Kramer, W.L., Greiner, E.C. & Gibbs, E.P.J. (1985) Seasonal variations in population size, fecundity, and parity rates of Culicoides insignis (Diptera: Ceratopogonidae) in Florida, USA. Journal of Medical Entomology 22, 163–169.Google Scholar
Linley, J.R. (1966) The ovarian cycle in Culicoides barbosia Wirth and Blanton and C. furens (Poey) (Diptera: Ceratopogonidae). Bulletin of Entomological Research 57, 1–17.Google Scholar
Linley, J.R. & Hinds, M.J. (1976) Seasonal changes in size, female fecundity and male potency in Culicoides melleus (Diptera: Ceratopogonidae). Journal of Medical Entomology 13, 151–156.Google Scholar
Lord, C.C. & Baylis, M. (1999) Estimation of survival rates in haematophagus insects. Medical and Veterinary Entomology 13, 225–233.Google Scholar
Lunn, D., Spiegelhalter, D., Thomas, A. & Best, N. (2009) The BUGS project: evolution, critique and future directions. Statistics in Medicine 28, 3049–3067.Google Scholar
MacDonald, G. (1952) The objective of residual insecticide campaigns. Transactions of the Royal Society of Tropical Medicine and Hygiene 46, 227–235.CrossRefGoogle ScholarPubMed
MacDonald, G. (1957) Epidemiology and Control of Malaria. London, UK, Oxford University Press.Google Scholar
McCarthy, M.A. (2007) Bayesian Methods for Ecology. Cambridge, UK, Cambridge University Press.Google Scholar
Mellor, P.S., Boorman, J. & Baylis, M. (2000) Culicoides biting midges: their role as arbovirus vectors. Annual Review of Entomology 45, 307–340.Google Scholar
Mullens, B.A. & Holbrook, F.R. (1991) Temperature effects on the gonotrophic cycle of Culicoides variipennis (Diptera: Ceratopogonidae)). Journal of the American Mosquito Control Association 7, 588–591.Google Scholar
Mullens, B.A. & Rutz, D.A. (1983) Development of immature Culicoides variipennis (Diptera: Ceratopogonidae) at constant laboratory temperature. Annals of the Entomological Society of America 76, 71–76.Google Scholar
Mullens, B.A. & Rutz, D.A. (1984) Age structure and survivourship and Culicoides variipennis (Diptera: Cerapogonidae) in central New York State, USA. Journal of Medical Entomology 21, 194–203.Google Scholar
Parham, P.E. & Michael, E. (2010) Modelling climate change and malaria transmission. Modelling Parasite Transmission and Control 673, 184–199.Google Scholar
Parker, A.H. (1949) Observations on the seasonal and daily incidence of certain biting midges (Culicoides Latr.) in Scotland. Transactions of the Royal Entomological Society London 100, 170–190.Google Scholar
Purse, B.V., Tatem, A.J., Caracappa, S., Rogers, D.J., Mellor, P.S., Baylis, M. & Torina, A. (2004) Modelling the distributions of Culicoides bluetongue virus vectors in Sicily in relation to satellite-derived climate variables. Medical and Veterinary Entomology 18, 90–101.Google Scholar
R Development Core Team (2009) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. ISBN 3-900051-07-0.Google Scholar
Rawlings, P. (1996) A key, based on wing patterns of biting midges (genus Culicoides Latreille – Diptera: Ceratologonidae) in the Iberian penninsula, for use in epidemiological studies. Graellsia 52(11), 57–71.Google Scholar
Rodeghiero, M. & Battisti, A. (2000) Inter-tree distribution of the spruce web-spinning sawfly, Cephalcia abietis, at endemic density. Agricultural and Forest Entomology 2, 291–296.CrossRefGoogle Scholar
Saldaña, S., Lima, M. & Estay, S. (2007) Northern Atlantic Oscillation effects on the temporal and spatial dynamics of green spruce aphid populations in the UK. Journal of Animal Ecology 76, 782–789.Google Scholar
Service, M.W. (1968) Light-trap catches of Culicoides spp. (Dipt., Cerapogonoidae) from southern England. Bulletin of Entomological Research 59, 317–322.Google Scholar
Service, M.W. (1969) Studies on the biting habits of Culicoides impunctatus Goetghebuer, C. obsoletus (Meigen) and C. punctatus (Meigen) (Dipetera: Ceratopogonidae) in southern England. Proceedings of the Royal Entomological Society London, Series A 44, 1–10.CrossRefGoogle Scholar
Service, M.W. (1974) Further results of catches of Culicoides (Dipetra: Ceratopogonidae) and mosquitos from suction traps. Journal of Medical Entomology 11, 471–479.Google Scholar
Sileshi, G. (2006) Selecting the right statistical model for analysis of insect count data by using information theoretic measures. Bulletin of Entomological Research 96, 479–488.Google Scholar
Speigelhalter, D.J., Best, N.G., Carlin, B.P. & Van Der Linde, A. (2002) Bayesian measures of model complexity and fit. Journal of the Royal Statistical Society, Series B (Statistical Methodology) 64, 583–639.Google Scholar
Takken, W., Verhulst, N., Scholte, E.J., Jacobs, F., Jongema, Y. & van Lammeren, R. (2008) The phenology and population dynamics of Culicoides spp. in different ecosystems in the Netherlands. Preventative Veterinary Medicine 87, 41–54.Google Scholar
Tatem, A.J., Baylis, M., Mellor, P.S., Purse, B.V., Capela, R., Pena, I. & Rogers, D.J. (2003) Prediction of bluetongue vector distribution in Europe and north Africa using satellite imagery. Veterinary Microbiology 97, 13–29.CrossRefGoogle ScholarPubMed
Van Ark, H. & Meiswinkel, R. (1992) Subsampling of large light-trap catches of Culicoides (Diptera: Ceratopogonidae). Onderstepoort Journal of Veterinary Research 59, 183–189.Google Scholar
Vinatier, F., Tixier, P., Duyck, P. & Lescourret, F. (2011) Factors and mechanisms explaining spatial heterogeneity: a review of methods for insect populations. Methods in Ecology and Evolution 2, 11–22.Google Scholar
Wan, Z. & Li, Z.L. (1997) A physics-based algorithm for retrieving land-surface emissivity and temperature from EOS/MODIS data. IEEE Transactions on Geoscience and Remote Sensing 35, 980–996.Google Scholar
Wellby, M.P., Baylis, M., Rawlings, P. & Mellor, P.S. (1996) Effect of temperature on virogenesis of African horse sickness virus in Culicoides variipensis sonorensis (Diptera: Ceratopogonidae) and its significance in relation to the epidemiology of the disease. Bulletin of Entomological Research 86, 715–720.CrossRefGoogle Scholar
Wittmann, E.J. (2000) Temperature and transmission of arboviruses by Culicoides biting midges. PhD thesis, University of Bristol, Bristol, UK.Google Scholar
Wood, S.N. (2011) Fast stable restricted maximum likelihood and marginal likelihood estimation of semiparametric generalized linear models. Journal of the Royal Statistical Society, Series B 73, 3–36.Google Scholar
Work, T.M., Mullens, B.A. & Jessup, D.A. (1991) Estimation of survival and gonotrophic cycle length of Culicoides variipennis (Diptera: Cerapogonidae) in California. Journal of the American Mosquito Control Association 7, 242–249.Google Scholar
Yang, G., Brook, B.W., Whelan, P.I., Cleland, S. & Bradshaw, C.J.A. (2008) Endogenous and exogenous factors controlling temporal abundance patterns of tropical mosquitoes. Ecological Applications 18, 2028–2040.Google Scholar
Yang, G., Brook, B.W. & Bradshaw, C.J.A. (2009) Predicting the timing and magnitude of tropical mosquito population peaks for maximising control efficiency. PLOS Neglected Tropical Diseases 3, 1–9.CrossRefGoogle Scholar
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