Modelling the Abundances of Two Major Culicoides (Diptera: Ceratopogonidae) Species in the Niayes Area of Senegal.
- Journal Article
- Research Support
- Non-U.S. Gov't
- African Horse Sickness
- Animal Health
- Animal Models
- Animal Science
- Animal Study
- Climate
- Culicoides
- Disease control
- Disease Outbreaks
- Disease Surveillance
- Disease Transmission
- Environmental Stressors
- Epidemiology
- Epizootic
- Equine Diseases
- Equine Health
- Mosquito-borne Diseases
- Vector-borne disease
- Veterinary Research
- Veterinary Science
Summary
The research explores environmental and climate factors affecting the population dynamics of two major insect species (Culicoides oxystoma and Culicoides imicola) in the Niayes region of Senegal that are suspected vectors of African horse sickness and bluetongue viruses. These species have significant impact on local horse populations and thus, the area’s economy.
Research Methodology
The researchers carried out extensive data collection and analyses:
- They collected samples of Culicoides oxystoma and Culicoides imicola using OVI light traps at five different sites for three consecutive nights per month over a year.
- Cross Correlation Map analysis was applied to identify the time-lags at which environmental variables and abundance data had the strongest correlation.
Findings
The findings revealed high variability and overdispersion in the count data for both species. Overdispersion was a persistent phenomenon seen even when large counts were modeled using on-site climate measures. The researchers explored several models, but the only one successful in accounting for overdispersion was the Poisson regression mixed-effect model with nested random effects at the site and date of capture levels.
Environmental & Climatic Drivers
The researchers identified several environmental and climatic drivers that influence the abundance of these two species:
- For Culicoides oxystoma: mean temperature and relative humidity of the capture day, mean humidity between 21 and 19 days before a capture event, density of ruminants, percentage of water bodies covering within a 2 km radius, and interaction between temperature and humidity.
- For Culicoides imicola: mean rainfall and Normalized Difference Vegetation Index (NDVI) of the capture day, and percentage cover of water bodies.
Future Directions & Recommendations
The study suggested testing other variables such as soil moisture, wind speed, degree days, land cover, or landscape metrics to improve the models further. Additionally, the researchers proposed assessing other trapping methods, like host-baited traps, to help reduce overdispersion. This study is a foundational step in better understanding these specific species’ dynamics and how they can be better managed or controlled.
Cite This Article
Publication
Researcher Affiliations
- Institut Sénégalais de Recherches Agricoles, Laboratoire National de l'Elevage et de Recherches Vétérinaires, Dakar, Sénégal; Université Gaston Berger, Laboratoire d'Etudes et de Recherches en Statistiques et Développement, Saint-Louis, Sénégal.
- Institut Sénégalais de Recherches Agricoles, Laboratoire National de l'Elevage et de Recherches Vétérinaires, Dakar, Sénégal.
- Cirad, UMR15 CMAEE, F-34398 Montpellier, France; INRA, UMR1309 CMAEE, F-34398 Montpellier, France.
- Université Gaston Berger, Laboratoire d'Etudes et de Recherches en Statistiques et Développement, Saint-Louis, Sénégal.
- Institut Sénégalais de Recherches Agricoles, Laboratoire National de l'Elevage et de Recherches Vétérinaires, Dakar, Sénégal.
- Institut Sénégalais de Recherches Agricoles, Laboratoire National de l'Elevage et de Recherches Vétérinaires, Dakar, Sénégal.
- Institut Sénégalais de Recherches Agricoles, Laboratoire National de l'Elevage et de Recherches Vétérinaires, Dakar, Sénégal.
- Cirad, UMR15 CMAEE, F-34398 Montpellier, France; INRA, UMR1309 CMAEE, F-34398 Montpellier, France.
- Cirad, UMR15 CMAEE, F-34398 Montpellier, France; INRA, UMR1309 CMAEE, F-34398 Montpellier, France.
- Cirad, UMR15 CMAEE, F-34398 Montpellier, France; INRA, UMR1309 CMAEE, F-34398 Montpellier, France.
- Institut Sénégalais de Recherches Agricoles, Laboratoire National de l'Elevage et de Recherches Vétérinaires, Dakar, Sénégal.
- Institut Sénégalais de Recherches Agricoles, Laboratoire National de l'Elevage et de Recherches Vétérinaires, Dakar, Sénégal; Cirad, UMR15 CMAEE, F-34398 Montpellier, France; INRA, UMR1309 CMAEE, F-34398 Montpellier, France.
- Cirad, UMR15 CMAEE, F-34398 Montpellier, France; INRA, UMR1309 CMAEE, F-34398 Montpellier, France.
MeSH Terms
- Animals
- Ceratopogonidae / physiology
- Female
- Models, Biological
- Multivariate Analysis
- Reproducibility of Results
- Senegal
- Species Specificity
Conflict of Interest Statement
References
- Ostfeld RS, Glass GE, Keesing F. Spatial epidemiology: an emerging (or re-emerging) discipline.. Trends Ecol Evol 2005;20(6):328–36.
- Borkent A. World species biting midges (Diptera: Ceratopogonidae). Available: http://wwxinhsillinoisedu/files/9913/9144/3328/CeratopogonidaeCatalogpdf. 2014.
- Borkent A. The subgeneric classification of species of Culicoides—thoughts and a warning. Available: http://wwxinhsillinoisedu/files/9613/9136/7590/CulicoidesSubgenerapdf. 2014.
- Akakpo AJ, Wombou Toukam CM, Mankor A, Ly C. Impact économique de l’épizootie de peste équine de 2007 au Sénégal.. Bull Anim Hlth Prod Afr 2011;59:1–16.
- Diouf ND, Etter E, Lo MM, Lo M, Akakpo AJ. Outbreaks of African horse sickness in Senegal and methods of control of the 2007 epidemic.. Vet Rec 2013;172(6):152.
- Diarra M, Fall M, Fall AG, Diop A, Seck MT, Garros C. Seasonal dynamics of Culicoides (Diptera: Ceratopogonidae) biting midges, potential vectors of African horse sickness and bluetongue viruses in the Niayes area of Senegal.. Parasit Vectors 2014;7(1):147.
- Bakhoum MT, Fall M, Fall AG, Bellis GA, Gottlieb Y, Labuschagne K. First record of Culicoides oxystoma Kieffer and diversity of species within the Schultzei group of Culicoides Latreille (Diptera: Ceratopogonidae) biting midges in Senegal.. PLoS One 2013;8(12):e84316.
- Mellor P, Carpenter S, White DM. Bluetongue virus in the insect host. Bluetongue 2009. p. 295–320.
- Purse BV, Carpenter S, Venter GJ, Bellis G, Mullens BA. Bionomics of Temperate and Tropical Culicoides Midges: Knowledge Gaps and Consequences for Transmission of Culicoides-Borne Viruses.. Annu Rev Entomol 2015;60(1):373–92.
- Meiswinkel R, Gomulski LM, Delecolle JC, Goffredo M, Gasperi G. The taxonomy of Culicoides vector complexes—unfinished business.. Vet Ital 2004;40(3):151–9.
- Mellor PS, Boorman J, Baylis M. Culicoides biting midges: their role as arbovirus vectors.. Annu Rev Entomol 2000;45:307–40.
- Venter GJ, Paweska JT, Van Dijk AA, Mellor PS, Tabachnick WJ. Vector competence of Culicoides bolitinos and C. imicola for South African bluetongue virus serotypes 1, 3 and 4.. Med Vet Entomol 1998;12(4):378–85.
- Mellor PS, Hamblin C. African horse sickness.. Vet Res 2004;35(4):445–66.
- Venter GJ, Graham SD, Hamblin C. African horse sickness epidemiology: vector competence of south african Culicoides species for virus serotypes 3, 5 and 8.. Med Vet Entomol 2000;14(3):245–50.
- Purse BV, Falconer D, Sullivan MJ, Carpenter S, Mellor PS, Piertney SB. Impacts of climate, host and landscape factors on Culicoides species in Scotland.. Med Vet Entomol 2011.
- Baylis M, Meiswinkel R, Venter GJ. A preliminary attempt to use climate data and satellite imagery to model the abundance and distribution of Culicoides imicola (Diptera: Ceratopogonidae) in southern Africa.. J S Afr Vet Assoc 1999;70(2):80–9.
- Baylis M, Mellor PS, Wittmann EJ, Rogers DJ. Prediction of areas around the Mediterranean at risk of bluetongue by modelling the distribution of its vector using satellite imaging.. Vet Rec 2001;149(21):639–43.
- Conte A, Goffredo M, Ippoliti C, Meiswinkel R. Influence of biotic and abiotic factors on the distribution and abundance of Culicoides imicola and the Obsoletus Complex in Italy.. Vet Parasitol 2007;150(4):333–44.
- Ducheyne E, Chueca MAM, Lucientes J, Calvete C, Estrada R, Boender GJ. Abundance modelling of invasive and indigenous Culicoides species in Spain.. Geospatial Health 2013;8(1):241–54.
- Ippoliti C, Gilbert M, Vanhuysse S, Goffredo M, Satta G, Wolff E. Can landscape metrics help determine the Culicoides imicola distribution in Italy?. Geospatial Health 2013;8(1):267–77.
- Rigot T, Conte A, Goffredo M, Ducheyne E, Hendrickx G, Gilbert M. Predicting the spatio-temporal distribution of Culicoides imicola in Sardinia using a discrete-time population model.. Parasit Vectors 2012;5:270.
- Roger FL. Emergence of Bluetongue Disease in the Mediterranean basin: Modelling Locations at Risk for Potential Vectors (Culicoides spp.) using Satellite Imagery [MSc]. 2002.
- Tatem AJ, Baylis M, Mellor PS, Purse BV, Capela R, Pena I. Prediction of bluetongue vector distribution in Europe and north Africa using satellite imagery.. Vet Microbiol 2003;97(1–2):13–29.
- Baylis M, Bouayoune H, Touti J, El Hasnaoui H. Use of climatic data and satellite imagery to model the abundance of Culicoides imicola, the vector of African horse sickness virus, in Morocco.. Med Vet Entomol 1998;12(3):255–66.
- Conte A, Giovannini A, Savini L, Goffredo M, Calistri P, Meiswinkel R. The effect of climate on the presence of Culicoides imicola in Italy.. J Vet Med B Infect Dis Vet Public Health 2003;50(3):139–47.
- Conte A, Ippoliti C, Savini L, Goffredo M, Meiswinkel R. Novel environmental factors influencing the distribution and abundance of Culicoides imicola and the Obsoletus Complex in Italy.. Vet Ital 2007;43(3):571–80.
- Baylis M, Rawlings P. Modelling the distribution and abundance of Culicoides imicola in Morocco and Iberia using climatic data and satellite imagery.. Arch Virol Suppl 1998;14:137–53.
- Acevedo P, Ruiz-Fons F, Estrada R, Marquez AL, Miranda MA, Gortazar C. A broad assessment of factors determining Culicoides imicola abundance: modelling the present and forecasting its future in climate change scenarios.. PLoS One 2010;5(12):e14236.
- Allain E, Brenac T. Modèles linéaires généralisés appliqués à l'étude des nombres d'accidents sur des sites routiers: Le modèle de Poisson et ses extensions.. Recherche—Transports—Sécurité 2001;72(0):3–16.
- Bouche G, Lepage B, Migeot V, Ingrand P. Application of detecting and taking overdispersion into account in Poisson regression model.. Rev Epidemiol Sante Publique 2009;57:285–96.
- Gardner W, Mulvey E, Shaw E. Regression analyses of counts and rates: Poisson, overdispersed Poisson, and negative binomial models.. Psychol Bull 1995;118:392–404.
- Breslow N. Tests of Hypotheses in Overdispersed Poisson Regression and other Quasi-Likelihood Models.. J Amer Statist Assoc 1990;85(410):565–71.
- Dean C, Lawless JF. Tests for Detecting Overdispersion in Poisson Regression Models.. J Amer Statist Assoc 1989;84(406):467–72.
- Zuur AF, Ieno EN, Walker NJ, Saveliev AA, Smith GM. Mixed Effects Models and Extensions in Ecology with R. 2009. 549 p.
- Kirkeby C, Bodker R, Stockmarr A, Lind P. Spatial abundance and clustering of culicoides (diptera: ceratopogonidae) on a local scale.. Parasite Vector 2013;6(43):1–14.
- Fall M, Diarra M, Fall AG, Balenghien T, Seck MT, Bouyer J. Culicoides (Diptera: Ceratopogonidae) midges, the vectors of African horse sickness virus—a host/vector contact study in the Niayes area of Senegal.. Parasit Vectors 2015;8(1):39.
- Baylis M, el Hasnaoui H, Bouayoune H, Touti J, Mellor PS. The spatial and seasonal distribution of African horse sickness and its potential Culicoides vectors in Morocco.. Med Vet Entomol 1997;11(3):203–12.
- Meiswinkel R, Venter GJ, Nevill EM. Culicoides spp.. Infectious diseases of livestock, Volume One 2004. p 93–136.
- Braverman Y. Characteristics of Culicoides (Diptera, Ceratopogonidae) breeding places near Salisbury, Rhodesia.. Ecological Entomology 1978;3:163–70.
- Foxi C, Delrio G. Larval habitats and seasonal abundance of Culicoides biting midges found in association with sheep in northern Sardinia, Italy.. Med Vet Entomol 2010;24(2):199–209.
- Uslu U, Dik B. Description of breeding sites of Culicoides species (Diptera: Ceratopogonidae) in Turkey.. Parasite 2007;14(2):173–7.
- Poddar TK, Ray S, Choudhury A. Ecology of larval Culicoides oxystoma (Diptera: Ceratopogonidae) in the Hooghly estuary, Sagar Island, India.. Ann Entomol 1992;10(1):19–25.
- Wirth WW, Hubert AA. The Culicoides of southeast Asia (Diptera: Ceratopogonidae).. Mem Am Entomol Inst 1989;44:1–509.
- Ray S, Choudhury A. Vertical Distribution of a Biting Midge, Culicoides oxystoma (Diptera: Ceratopogonidae) During Different Seasons in the Hooghly Estuary, Sagar Island, India.. Int J Trop Insect Sci 1988;9(03):329–33.
- Yanase T, Matsumoto Y, Matsumori Y, Aizawa M, Hirata M, Kato T. Molecular identification of field-collected Culicoides larvae in the southern part of Japan.. J Med Entomol 2013;50(5):1105–10.
- Garcia-Saenz A, McCarter P, Baylis M. The influence of host number on the attraction of biting midges, Culicoides spp., to light traps.. Med Vet Entomol 2010;25(1):113–5.
- Calvete C, Estrada R, Miranda MA, Borras D, Calvo JH, Lucientes J. Ecological correlates of bluetongue virus in Spain: predicted spatial occurrence and its relationship with the observed abundance of the potential Culicoides spp. vector.. Vet J 2009;182(2):235–43.
- Golyandina N, Korobeynikov A, Shlemov A, Usevich K. Multivariate and 2D Extensions of Singular Spectrum Analysis with the Rssa Package.. arXiv 2013.
- Golyandina N, Zhigljavsky A. Singular Spectrum Analysis for time series. 2013. 125 p.
- Kondrashov D, Ghil M. Spatio-temporal filling of missing points in geophysical data sets.. Nonlin Processes Geophys 2006;13:151–9.
- Curriero FC, Shone SM, Glass GE. Cross correlation maps: a tool for visualizing and modeling time lagged associations.. Vector Borne Zoonotic Dis 2005;5(3):267–75.
- Lebl K, Brugger K, Rubel F. Predicting Culex pipiens/restuans population dynamics by interval lagged weather data.. Parasit Vectors 2013;6(1):129.
- Shone SM, Curriero FC, Lesser CR, Glass GE. Characterizing population dynamics of Aedes sollicitans (Diptera: Culicidae) using meteorological data.. J Med Entomol 2006;43(2):393–402.
- Walsh A, Glass G, Lesser C, Curriero F. Predicting seasonal abundance of mosquitoes based on off-season meteorological conditions.. Environ Ecol Stat 2008;15(3):279–91.
- Brugger K, Rubel F. Bluetongue disease risk assessment based on observed and projected Culicoides obsoletus spp. vector densities.. PLoS One 2013;8(4):e60330.
- McCullagh P, Nelder J. Generalized linear models 2 ed.. 1989.
- Elston DA, Moss R, Boulinier T, Arrowsmith C, Lambin X. Analysis of aggregation, a worked example: numbers of ticks on red grouse chicks.. Parasitology 2001;122(5):563–9.
- Tassi P. Méthodes Statistiques. 3e édition, Collection Economie et Statistiques avancées Paris, France, ISBN: 2-7178-4859-2.. 2004.
- R Core Team. R: A language and environment of statistical computing.. 2012.
- Boorman J, Goddard P. Observations on the biology of Culicoides impunctatus Goetgh. (Dipt., Ceratopogonidae) in southern England.. Bull Entomol Res 1970;60(02):189–98.
- Carpenter S, Mordue W. Oogenesis and laboratory survival in the Scottish biting midge Culicoides impunctatus .. Physiol Entomol 2006;31(1):89–93.
- Davis EL, Butler JF, Roberts RH, Reinert JF, Kline DL. Laboratory blood feeding of Culicoides mississippiensis (Diptera: Ceratopogonidae) through a reinforced silicone membrane.. J Med Entomol 1983;20(2):177–82.
- Lysyk TJ, Danyk T. Effect of temperature on life history parameters of adult Culicoides sonorensis (Diptera: Ceratopogonidae) in relation to geographic origin and vectorial capacity for bluetongue virus.. J Med Entomol 2007;44(5):741–51.
- Mullens BA, Rutz DA. Development of immature Culicoides variipennis (Diptera: Ceratopogonidae) at constant laboratory temperatures.. Ann Entomol Soc Am 1983;76(4):747–51.
- Vaughan J, Turner E. Development of immature Culicoides variipennis (Diptera: Ceratopogonidae) from Saltville, Virginia, at constant laboratory temperatures.. J Med Entomol 1987;24(3):390–5.
- Veronesi E, Venter GJ, Labuschagne K, Mellor PS, Carpenter S. Life-history parameters of Culicoides (Avaritia) imicola Kieffer in the laboratory at different rearing temperatures.. Vet Parasitol 2009;163(4):370–3.
- Ortega MD, Holbrook FR, Lloyd JE. Seasonal distribution and relationship to temperature and precipitation of the most abundant species of Culicoides in five provinces of Andalusia, Spain.. J Am Mosq Control Assoc 1999;15(3):391–9.
- Murray MD. The Seasonal Abundance of Female Biting-Midges, Culicoides-Brevitarsis Kieffer (Diptera, Ceratopogonidae), in Coastal South-Eastern Australia.. Aust J Zool 1991;39(3):333–42.
- Baylis M, Parkin H, Kreppel K, Carpenter S, Mellor PS, McIntyre KM. Evaluation of housing as a means to protect cattle from Culicoides biting midges, the vectors of bluetongue virus.. Med Vet Entomol 2010;24(1):38–45.
- Kluiters G, Sugden D, Guis H, Marie McIntyre K, Labuschagne K, Vilar MJ. Modelling the spatial distribution of Culicoides biting midges at the local scale.. J Appl Ecol 2013;50(1):232–42.
- Murray MD. Potential vectors of bluetongue in Australia.. Aust Vet J 1975;51(4):216–20.
- Nevill EM. Biological studies on some South African Culicoides species (Diptera: Ceratopogonidae) and the morphology of their immature stages: Thèse de Doctorat.. 1967.
- Calvete C, Estrada R, Miranda MA, Borras D, Calvo JH, Lucientes J. Modelling the distributions and spatial coincidence of bluetongue vectors Culicoides imicola and the Culicoides obsoletus group throughout the Iberian peninsula.. Med Vet Entomol 2008;22(2):124–34.
- Narasimha Rao PV, Venkataratnam L, Krishna Rao PV, Ramana KV, Singarao MN. Relation between root zone soil moisture and normalized difference vegetation index of vegetated fields.. Int J Remote Sens 1993;14(3):441–9.
- Rogers DJ, Randolph SE. Mortality rates and population density of tsetse flies correlated with satellite imagery.. Nature 1991;351:739–41.
- Tucker CJ, Vanpraet CL, Sharman MJ, Van Ittersum G. Satellite remote sensing of total herbaceous biomass production in the senegalese sahel: 1980–1984.. Remote Sensing of Environment 1985;17(3):233–49.
- Guis H. Geomatique et epidemiologie: Caracterisation des paysages favorables à Culicoides imicola, vecteur de la fievre catarrhale ovine en Corse. These de doctorat es Science de la vie et de la santé Universite de Franche-Comté.. 2007:392.
- Harrison XA. Using observation-level random effects to model overdispersion in count data in ecology and evolution.. PeerJ 2014;2:e616.
- Crawley MJ. The R book: Wiley; 2 edition. 2012. 1076 p.
- Hilbe JM. Negative binomial regression: Cambridge University Press. 2011. 553 p.
- Richards SA. Dealing with overdispersed count data in applied ecology.. J Appl Ecol 2008;45(1):218–27.
- Peters J, Conte A, Van doninck J, Verhoest NEC, De Clercq E, Goffredo M. On the relation between soil moisture dynamics and the geographical distribution of Culicoides imicola .. Ecohydrology 2014;7(2):622–32.
- Bishop AL, McKenzie HJ, Barchia IM, Spohr LJ. Moon phase and other factors affecting light-trap catches of Culicoides brevitarsis Kieffer (Diptera: Ceratopogonidae).. Aust J Entomol 2000;39:29–32.
- Blackwell A. Diel flight periodicity of the biting midge Culicoides impunctatus and the effects of meteorological conditions.. Med Vet Entomol 1997;11(4):361–7.
- Walker AR. Seasonal fluctuations of Culicoides species (Diptera: Ceratopogonidae) in Kenya.. Bull ent Res 1977;67:217–33.
- De Liberato C, Farina F, Magliano A, Rombola P, Scholl F, Spallucci V. Biotic and abiotic factors influencing distribution and abundance of Culicoides obsoletus group (Diptera: Ceratopogonidae) in central Italy.. J Med Entomol 2010;47(3):313–8.
- Guis H, Tran A, de La Rocque S, Baldet T, Gerbier G, Barragué B. Use of high spatial resolution satellite imagery to characterize landscapes at risk for bluetongue.. Vet Res 2007;38(5):669–83.
- Searle KR, Barber J, Stubbins F, Labuschagne K, Carpenter S, Butler A. Environmental Drivers of Culicoides Phenology: How Important Is Species-Specific Variation When Determining Disease Policy?. PLoS ONE 2014;9(11):e111876.
- Guis H, Caminade C, Calvete C, Morse AP, Tran A, Baylis M. Modelling the effects of past and future climate on the risk of bluetongue emergence in Europe.. J Roy Soc Interface 2011.
- Hartemink NA, Purse BV, Meiswinkel R, Brown HE, de Koeijer A, Elbers ARW. Mapping the basic reproduction number (R0) for vector-borne diseases: A case study on bluetongue virus.. Epidemics 2009;1(3):153–61.