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Mortality estimates from ovarian age distributions of the tsetse fly Glossina pallidipes Austen sampled in Zimbabwe suggest the need for new analytical approaches

Published online by Cambridge University Press:  25 March 2015

J.W. Hargrove  and
S.F. Ackley
J.W. Hargrove*
Affiliation:
SACEMA, University of Stellenbosch, Stellenbosch, South Africa
S.F. Ackley
Affiliation:
Department of Epidemiology and Biostatistics, University of California, San Francisco, CA, USA
*
*Author for correspondence Phone: (+27) 21 808 2589 Fax: (+27) 21 808 2586 E-mail: jhargrove@sun.ac.za
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Abstract

Mortality estimates are central to understanding tsetse fly population dynamics, but are difficult to acquire from wild populations. They can be obtained from age distribution data but, with limited data, it is unclear whether the assumptions required to make the estimates are satisfied and, if not, how violations affect the estimates. We evaluate the assumptions required for existing mortality estimation techniques using long-term longitudinal ovarian dissection data from 144,106 female tsetse, Glossina pallidipes Austen, captured in Zimbabwe between 1988 and 1999. At the end of the hot-dry season each year, mean ovarian ages peaked, and maximum-likelihood mortality estimates declined to low levels, contrary to mark-recapture estimates, suggesting violations of the assumptions underlying the estimation technique. We demonstrate that age distributions are seldom stable for G. pallidipes at our study site, and hypothesize that this is a consequence of a disproportionate increase in the mortality of pupae and young adults at the hottest times of the year. Assumptions of age-independent mortality and capture probability are also violated, the latter bias varying with capture method and with pregnancy and nutritional status. As a consequence, mortality estimates obtained from ovarian dissection data are unreliable. To overcome these problems we suggest simulating female tsetse populations, using dynamical modelling techniques that make no assumptions about the stability of the age distribution.

Keywords

Glossina pallidipestsetsemortality estimatesovarian dissectionstable age distribution
Type
Research Papers
Information
Bulletin of Entomological Research , Volume 105 , Issue 3 , June 2015 , pp. 294 - 304
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Copyright
Copyright © Cambridge University Press 2015 

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References

Bursell, E. & Glasgow, J.P. (1960) Further observations on lakeside and riverine communities of Glossina palpalis fuscipes Newstead. Bulletin of Entomological Research 51, 47–56.Google Scholar
Carey, J.R. (2011) Biodemography of the Mediterranean fruit fly: aging, longevity and adaptation in the wild. Experimental Gerontology 46, 404–411.Google Scholar
Carey, J.R., Papadopoulos, N.T., Papanastasiou, S., Diamantidis, A. and Nakas, C.T. (2012 a) Estimating changes in mean population age using the death distributions of live-captured medflies. Ecological Entomology 37, 359–369.Google Scholar
Carey, J.R., Müller, H.G., Wang, J.L., Papadopoulos, N.T., Diamantidis, A. and Koulousis, N.A. (2012 b) Graphical and demographic synopsis of the captive cohort method for estimating population age structure in the wild. Experimental Gerontology 47, 787–791.Google Scholar
Carey, J.R., Papadopoulos, N.T., Müller, H.G., Katsoyannos, B.I., Kouloussis, N.A., Wang, J.L., Wachter, K., Yu, W. and Liedo, P. (2008) Age structure changes and extraordinary lifespan in wild medfly populations. Aging Cell 7, 426–437.Google Scholar
Challier, A. (1965) Amélioration de la méthode de détermination de l'âge physiologique des glossines. Études faites sur Glossina palpalis palpalis Vanderplank, 1949. Bulletin de la Société de Pathologie Exotique 58, 250–259.Google Scholar
Curtis, C.F. & Jordan, A.M. (1968) Calculations on the productivity of Glossina austeni Newst. maintained on goats and on lop-eared rabbits. Bulletin of Entomological Research 59, 651–658.CrossRefGoogle Scholar
Dransfield, R.D., Brightwell, R., Kiilu, J., Chaudhury, M.F. & Adabie, D.A. (1989) Size and mortality rates of Glossina pallidipes in the semi-arid zone of southwestern Kenya. Medical and Veterinary Entomology 3, 83–95.Google Scholar
Glasgow, P.A. (1961) Selection for size in tsetse flies. Journal of Animal Ecology 30, 87–94.CrossRefGoogle Scholar
Hargrove, J.W. (1990) Age-dependent changes in the probabilities of survival and capture of the tsetse fly Glossina morsitans morsitans Westwood. Insect Science and its Application 11, 323–330.Google Scholar
Hargrove, J.W. (1991) Ovarian ages of tsetse flies (Diptera: Glossinidae) caught from mobile and stationary baits in the presence and absence of humans. Bulletin of Entomological Research 81, 43–50.CrossRefGoogle Scholar
Hargrove, J.W. (1993) Age-dependent sampling biases in tsetse flies (Glossina). Problems associated with estimating mortality from sample age distributions. pp. 549–556. in Management of Insect Pests: Nuclear and Related Molecular and Genetic Techniques. Vienna, Austria, International Atomic Energy Agency.Google Scholar
Hargrove, J.W. (1999 a) Nutritional levels of female tsetse Glossina pallidipes from artificial refuges. Medical and Veterinary Entomology 13, 150–164.Google Scholar
Hargrove, J.W. (1999 b) Lifetime changes in the nutritional characteristics of female tsetse flies Glossina pallidipes caught in odour-baited traps. Medical and Veterinary Entomology 13, 165–176.Google Scholar
Hargrove, J.W. (1999 c) Reproductive abnormalities in field tsetse flies in Zimbabwe. Entomologia Experimentalis et Applicata 92, 89–99.Google Scholar
Hargrove, J.W. (2001 a) The effect of temperature and saturation deficit on mortality in populations of male Glossina m. morsitans (Diptera: Glossinidae) in Zimbabwe and Tanzania. Bulletin of Entomological Research 91, 79–86.Google Scholar
Hargrove, J.W. (2001 b) Factors affecting density-independent survival of an island population of tsetse flies in Zimbabwe. Entomologia Experimentalis et Applicata 100, 151–164.Google Scholar
Hargrove, J.W. (2004) Tsetse population dynamics. pp 113–137. in Maudlin, I., Holmes, P.H. & Miles, P.H. (Eds). The Trypanosomiases. Oxford, UK, CABI Publishing.Google Scholar
Hargrove, J.W. & Brady, J. (1992) Activity rhythms of tsetse flies (Glossina spp.) (Diptera: Glossinidae) at low and high temperatures in nature. Bulletin of Entomological Research 82, 321–326.Google Scholar
Hargrove, J.W. & Langley, P.A. (1990) Sterilizing tsetse in the field: a successful field trial. Bulletin of Entomological Research 80, 397–403.CrossRefGoogle Scholar
Hargrove, J.W. & Langley, P.A. (1993) A field trial of pyriproxyfen-treated targets as an alternative method for controlling tsetse (Diptera: Glossinidae). Bulletin of Entomological Research 83, 361–368.Google Scholar
Hargrove, J.W. & Williams, B.G. (1998) Optimized simulation as an aid to modelling, with an application to the study of a population of tsetse flies, Glossina morsitans morsitans Westwood (Diptera: Glossinidae). Bulletin of Entomological Research 88, 425–435.Google Scholar
Hargrove, J.W., Holloway, M.T.P., Vale, G.A., Gough, A.J.E. & Hall, D.J. (1995) Catches of tsetse flies (Glossina spp.) (Diptera: Glossinidae) from traps baited with large doses of natural and synthetic host odour. Bulletin of Entomological Research 85, 215–227.Google Scholar
Hargrove, J.W., Ouifki, R. & Ameh, J.E. (2011) A general model for mortality in adult tsetse (Glossina spp). Medical and Veterinary Entomology 25, 385–394.Google Scholar
Jackson, C.H.N. (1941) The analysis of a tsetse fly population. Annals of Eugenics 10, 332–369.Google Scholar
Jackson, C.H.N. (1944) The analysis of a tsetse fly population II. Annals of Eugenics 12, 176–205.Google Scholar
Jackson, C.H.N. (1945) Comparative studies of the habitat requirements of tsetse fly species. Journal of Animal Ecology 14, 46–51.Google Scholar
Jackson, C.H.N. (1948) Some further isolated generation of tsetse flies. Bulletin of Entomological Research 39, 441–451.Google Scholar
Jarry, M., Gouteux, J.-P. & Khaladi, M. (1996) Are tsetse fly populations close to equilibrium? Acta Biotheoretica 44, 317–33.Google Scholar
Jarry, M., Gouteux, J.-P. & Khaladi, M. (1999) Estimation of age-dependent survival rates of female tsetse flies (Diptera: Glossinidae) from ovarian age distributions. Bulletin of Entomological Research 89, 515–521.Google Scholar
Jolly, G.M. (1965) Explicit estimates from capture–recapture data with both death and immigration – stochastic model. Biometrika 52, 225–247.Google Scholar
Jordan, A.M. & Curtis, C.F. (1968) Productivity of Glossina austeni Newst. maintained on lop-eared rabbits. Bulletin of Entomological Research 58, 399–410.Google Scholar
Jordan, A.M. & Curtis, C.F. (1972) Productivity of Glossina morsitans Westwood maintained in the laboratory, with particular reference to the sterile – insect release method. Bulletin of the World Health Organisation 46, 33–38.Google Scholar
Novoseltsev, V.N., Michalski, A.I., Novoseltseva, J.A., Yashin, A.I., Carey, J.R. and Ellis, A.M. (2012) An age-structured extension to the vectorial capacity model. PLoS ONE 7, e39479. doi:10.1371/journal.pone.0039479 Google Scholar
Phelps, R.J. (1973) The effect of temperature on fat consumption during the puparial stages of Glossina morsitans morsitans Westw. (Dipt., Glossinidae) under laboratory conditions, and its implication in the field. Bulletin of Entomological Research 62, 423–438.Google Scholar
Phelps, R.J. & Clarke, G.P.Y. (1974) Seasonal elimination of some size classes in males of Glossina morsitans morsitans Westw. (Diptera, Glossinidae). Bulletin of Entomological Research 64, 313–324.Google Scholar
Rogers, D.J. (1988) A general model for the African trypanosomiases. Parasitology 97, 193–212.Google Scholar
Rogers, D.J., Randolph, S.E. & Kuzoe, F.A.S. (1984) Local variation in the population dynamics of Glossina palpalis palpalis (Robineau-Desvoidy) (Diptera: Glossinidae). I. Natural population regulation. Bulletin of Entomological Research 74, 403–423.Google Scholar
Saunders, D.S. (1960) The ovulation cycle in Glossina morsitans Westwood (Diptera: Muscidae) and a possible method of age determination for female tsetse flies by the examination of their ovaries. Transaction of the Royal Entomological Society London 112, 221–238.Google Scholar
Saunders, D.S. (1962) Age determination for female tsetse flies and the age compositions of samples of Glossina pallidipes Aust., G. palpalis fuscipes Newst. and G. brevipalpis Newst. Bulletin of Entomological Research 53, 579–595.Google Scholar
Seber, G.A.F. (1965) A note on the multiple recapture census. Biometrika 52, 249–259.Google Scholar
Seber, G.A.F. (1982) The Estimation of Animal Abundance and Related Parameters. London, UK, Charles Griffin & Co. 654 pp.Google Scholar
Vale, G.A. (1971) Artificial refuges for tsetse flies (Glossina spp.). Bulletin of Entomological Research 61, 331–350.Google Scholar
Vale, G.A. (1974) The responses of tsetse flies (Diptera: Glossinidae) to mobile and stationary baits. Bulletin of Entomological Research 64, 545–588.Google Scholar
Van Sickle, J. & Phelps, R.J. (1988) Age distributions and reproductive status of declining and stationary populations of Glossina pallidipes Austen (Diptera: Glossinidae) in Zimbabwe. Bulletin of Entomological Research 78, 51–61.Google Scholar
Williams, B., Dransfield, R. & Brightwell, R. (1990) Tsetse fly (Diptera: Glossinidae) population dynamics and the estimation of mortality rates from life-table data. Bulletin of Entomological Research 80, 479–485.Google Scholar
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