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Metamorphosis behaviour and regulation in tsetse flies (Glossina spp.) (Diptera: Glossinidae): a review

Published online by Cambridge University Press:  10 July 2009

J. Žďárek
Affiliation:
International Centre of Insect Physiology and Ecology, P.O. Box 30772, Nairobi, Kenya
D. L. Denlinger*
Affiliation:
International Centre of Insect Physiology and Ecology, P.O. Box 30772, Nairobi, Kenya
*
Department of Entomology, Ohio State University, 1735 Neil Avenue, Columbus, OH 43210, USA.

Abstract

This review examines the recent literature on tsetse (Glossina spp.) metamorphosis behaviour and its regulation. The behavioural events associated with metamorphosis are highly specific and most occur only once during the life of the fly. The review begins with the larva's commitment to metamorphosis and then discusses the behaviour associated with parturition, wandering of the third instar larva, pupariation, pupation and adult eclosion. While certain aspects of tsetse metamorphosis behaviour are common to the higher Diptera, the peculiar reproductive strategy of tsetse has dictated many modifications. Most notable of the tsetse peculiarities are the larva's late commitment to metamorphosis, the contribution by the mother in deciding the onset of the wandering period, the brevity of the wandering period, the involvement of the nervous system in co-ordinating puparial tanning, the tight pack aging of the pupa within the puparium, the long duration of pharate adult development, and the great expansion of the body that occurs following eclosion. A final section discusses the potential for disrupting tsetse metamorphosis.

Type
Original Articles
Copyright
Copyright © Cambridge University Press 1993

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References

Allsopp, R. (1984) Control of tsetse flies (Diptera: Glossinidae) using insecticides: a review and future prospects. Bulletin of Entomological Research 74, 123.CrossRefGoogle Scholar
Atkinson, P.R. (1971) Relative humidity in the breeding sites of Glossina morsitans Westw. in northern Botswana. Bulletin of Entomological Research 61, 241246.Google Scholar
Benettová, B. & Fraenkel, G. (1981) What determines the number of ovarioles in a fly ovary? Journal of Insect Physiology 27, 403410.Google Scholar
Bequaert, J.C. (1952) The Hippoboscidae or louse-flies (Diptera) of mammals and birds. Part 1. Structure, physiology and natural history. Entomologica Americana 32, 1209.Google Scholar
Brady, J. (1988) The circadian organization of behaviour: time keeping in the tsetse fly, a model system. Advances in the Study of Behavior 18, 153191.CrossRefGoogle Scholar
Brady, J. & Gibson, G. (1983) Activity patterns in pregnant tsetse flies, Glossina morsitans. Physiological Entomology 8, 359369.CrossRefGoogle Scholar
Bursell, E. (1959) The water balance of tsetse flies. Transactions of the Royal Entomological Society of London 111, 205235.Google Scholar
Bursell, E. (1961) Post teneral development of the thoracic musculature in tsetse flies. Proceedings of the Royal Entomological Society of London, Series A 36, 6974.Google Scholar
Burtt, E. (1952) The occurrence in nature of tsetse pupae (Glossina swynnertoni Austen). Acta Tropica 9, 304344.Google ScholarPubMed
Burtt, E. & Jackson, C.H.N. (1951) Illustrations of tsetse larvae. Bulletin of Entomological Research 41, 523527.Google Scholar
Buxton, P.A. (1955) The natural history of tsetse flies. Memoirs of the London School of Hygiene and Tropical Medicine no. 10, 816 pp.Google Scholar
Chang, F. (1972) The effect of ligation on tanning in the larva of a tachinid parasite, Lespesia archippivora. Journal of Insect Physiology 18, 729735.CrossRefGoogle Scholar
Chorley, J.K. (1929) The bionomics of Glossina morsitans in the Umniati fly belt, Southern Rhodesia, 1922–1923. Bulletin of Entomological Research 20, 279301.Google Scholar
Colvin, J. & Gibson, G. (1992) Host-seeking behavior and management of tsetse. Annual Review of Entomology 37, 2140.Google Scholar
Cottrell, C.B. (1962) The imaginal ecdysis of blowflies. Observations on the hydrostatic mechanisms involved in digging and expansion. Journal of Experimental Biology 39, 431448.CrossRefGoogle Scholar
Crossley, A.C.S. (1964) Transformation of the abdominal muscles of the blue blow-fly Calliphora erythrocephala (Meign.) during metamorphosis. Journal of Embryology and Experimental Morphology 14, 95110.Google Scholar
Dean, G.J., Wilson, F. & Wortham, S. (1968) Some factors affecting eclosion of Glossina morsitans Westw. from pupae. Bulletin of Entomological Research 58, 367377.Google Scholar
Denlinger, D.L. (1975) Insect hormones as tsetse abortifacients. Nature, London 253, 347348.CrossRefGoogle ScholarPubMed
Denlinger, D.L. (1983) Who controls the rhythm of tsetse parturition: mother or larva? Physiological Entomology 8, 2528.Google Scholar
Denlinger, D.L. & Ma, W.C. (1974) Dynamics of the pregnancy cycle in the tsetse Glossina morsitans. Journal of Insect Physiology 20, 10151026.Google Scholar
Denlinger, D.L. & Žďárek, J. (1991a) Commitment to metamorphosis in tsetse (Glossina morsitans centralis): temporal, nutritional and hormonal aspects of the decision. Journal of Insect Physiology 37, 333338.CrossRefGoogle Scholar
Denlinger, D.L. & Žďárek, J. (1991b) Intrapuparial development in the tsetse fly, Glossina brevipalpis (Diptera, Glossinidae): behaviour associated with pupation. Acta Entomologica Bohemoslovaca 88, 353358.Google Scholar
Denlinger, D.L. & Žďárek, J. (1992) Rhythmic pulses of haemolymph pressure associated with parturition and ovulation in the tsetse fly, Glossina morsitans. Physiological Entomology 17, 127130.Google Scholar
Denlinger, D.L. & Žďárek, J. (in press) Metamorphosis behavior of flies. Annual Review of Entomology.Google Scholar
Denlinger, D.L., Chaudhury, M.F.B. & Dhadialla, T.S. (1978) Cyclic AMP is a likely mediator of ovulation in the tsetse fly. Experientia 34, 12961297.Google Scholar
Denlinger, D.L., Saini, R.K. & Chaudhury, M.F.B. (1983) Parturition in the tsetse fly Glossina morsitans: pattern of activity, sound production and evidence for control by the mother's brain. Journal of Insect Physiology 29, 715721.Google Scholar
Denlinger, D.L., Gnagey, A.L., Rockey, S.J., Chaudhury, M.F.B. & Fertel, R.H. (1984) Changes in levels of cyclic AMP and cyclic GMP during pregnancy and larval development of the tsetse fly, Glossina morsitans. Comparative Biochemistry and Physiology 77C, 233236.Google Scholar
Dransfield, R.D., Brightwell, R., Kiilu, J., Chaudhury, M.F.B. & Adabie, D.A. (1989) Size and mortality rates of Glossina pallidipes in the semi-arid zone of southwestern Kenya. Medical and Veterinary Entomology 3, 8395.CrossRefGoogle ScholarPubMed
Ejezie, G.C. & Davey, K.G. (1974) Changes in the neurosecre tory cells, corpus cardiacum and corpus allatum during pregnancy in Glossina austeni Newst.(Diptera, Glossindae). Bulletin of Entomological Research 64, 247256.Google Scholar
Evans, G.O. (1950) Studies on the bionomics of the sheep ked, Melophagus ovinus L., inwest Wales. Bulletin of Entomological Research 40, 459478.Google Scholar
Finlayson, L.H. (1967) Behaviour and regulation of puparium formation in the larva of the tsetse fly Glossina morsitans orientalis Vanderplank in relation to humidity, light and mechanical stimuli. Bulletin of Entomological Research 57, 301313.CrossRefGoogle ScholarPubMed
Finlayson, L.H. (1972) Chemoreceptors, cuticular mechanoreceptors, and peripheral multiterminal neurones in the larva of the tsetse fly (Glossina). Journal of Insect Physiology 18, 22652276.Google Scholar
Fogal, W. & Fraenkel, G. (1969) The role of bursicon in melanization and endocuticle formation in the adult fleshfly, Sarcophaga bullata. Journal of Insect Physiology 15, 12351247.Google Scholar
Foster, W.A. (1974) Surgical inhibition of ovulation and gestation in the tsetse fly Glossina austeni Newst. (Dipt., Glossinidae). Bulletin of Entomological Research 63, 483493.Google Scholar
Fraenkel, G. & Bhaskaran, G. (1973) Pupariation and pupation in cyclorrhaphous flies (Diptera): terminology and interpretation. Annals of the Entomological Society of America 66, 14181422.Google Scholar
Fraenkel, G. & Hsiao, C. (1962) Hormonal and nervous control of tanning in the fly. Science 137, 2729.Google Scholar
Fraenkel, G. & Hsiao, C. (1965) Bursicon, a hormone which mediates tanning of the cuticle in the adult fly and other insects. Journal of Insect Physiology 11, 513556.Google Scholar
Fraenkel, G. & Su, J. (1984) Hormonal control of eclosion of flies from the puparium. Proceedings of the National Academy of Sciences, USA 81, 14571459.CrossRefGoogle ScholarPubMed
Fraenkel, G. & Žďárek, J. (1970) The evaluation of the ‘Calliphora test’ as an assay for ecdysone. Biological Bulletin 139, 138150.Google Scholar
Fraenkel, G., Su, J. & Žďárek, J. (1984) Neuromuscular and hormonal control of post-eclosion processes in flies. Archives of Insect Biochemistry and Physiology 1, 345366.Google Scholar
Geigy, R. (1948) Elevage de Glossina palpalis. Acta Tropica 5, 201218.Google ScholarPubMed
Hargrove, J.W. (1975) Some changes in the flight apparatus of tsetse flies, G. morsitans and G. pallidipes, during maturation. Journal of Insect Physiology 21, 14851489.Google Scholar
Jackson, C.H.N. (1948) Some further isolated generations of tsetse flies. Bulletin of Entomological Research 39, 441451.CrossRefGoogle ScholarPubMed
Jordan, A.M. (1986) Trypanosomiasis control and African rural development. 357 pp. London, Longman.Google Scholar
Jordan, A.M. & Trewern, M.A. (1973) Sub-lethal effect of sulphaquinoxaline on the tsetse fly, Glossina austeni Newst. Nature, London 245, 462.CrossRefGoogle ScholarPubMed
Jordan, A.M., Trewern, M.A., Borkovec, A.B. & DeMilo, A.B. (1979) Laboratory studies on the potential of three insect growth regulators for control of the tsetse fly, Glossina morsitans morsitans Westwood (Diptera: Glossinidae). Bulletin of Entomological Research 69, 5564.Google Scholar
Laing, J. (1935) On the ptilinum of the blow-fly (Calliphora erythrocephala). Quarterly Journal of Microscopic Science 77, 497521.Google Scholar
Lamborn, W.A. (1915) Second report on Glossina investigations in Nyasaland. Bulletin of Entomological Research 6, 249265.Google Scholar
Langley, P.A. (1967) Effect of ligaturing on puparium formation in the larva of the tsetse fly, Glossina morsitans Westwood. Nature, London 214, 389390.Google Scholar
Langley, P.A. (1972) The role of physical and chemical stimuli in the development of in vitro feeding techniques for tsetse flies Glossina spp. (Dipt. Glossinidae). Bulletin of Entomological Research 62, 215228.Google Scholar
Langley, P.A. (1977) Physiology of tsetse flies (Glossina spp.) (Diptera: Glossindae): a review. Bulletin of Entomological Research 67, 523574.Google Scholar
Langley, P.A. & Ely, R. (1978) X-ray investigation of gas bubble formation, and water loss in tsetse fly pupae. Physiological Entomology 3, 303307.Google Scholar
Langley, P.A., Felton, T. & Oouchi, H. (1988) Juvenile hormone mimics as effective sterilants for the tsetse fly Glossina morsitans morsitans. Medical and Veterinary Entomology 2, 2935.Google Scholar
Langley, P.A., Felton, T., Stafford, K. & Oouchi, H. (1990) Formulation of pyriproxfen, a juvenile hormone mimic, for tsetse control. Medical and Veterinary Entomology 4, 127133.Google Scholar
Langley, P.A. & Pimley, R.W. (1986) A role for juvenile hormone and the effects of so-called anti-juvenile hormones in Glossina morsitans. Journal of Insect Physiology 32, 727734.Google Scholar
Lenoble, B.J. & Denlinger, D.L. (1982) The milk gland of the sheep ked, Melophagus ovinus: a comparison with Glossina. Journal of Insect Physiology 28, 165172.CrossRefGoogle Scholar
Leonard, D.E. & Saini, R.K. (in press) Semiochemicals from the anal exudate of larvae of tsetse flies Glossina morsitans morsitans Westwood and G. morsitans centralis Machado attract gravid females. Journal of Chemical Ecology.Google Scholar
Lewis, D.J. (1934) Movement of the ptilinum in newly-emerged tse-tse flies. Proceedings of the Entomological Society of London 9, 78.Google Scholar
Ma, W.C. & Denlinger, D.L. (1974) Secretory discharge and microflora of milk gland in tsetse flies. Nature, London 247, 301303.CrossRefGoogle Scholar
Madubunyi, L.C. (1978) Relative frequency of reproductive abnormalities in a natural population of Glossina morsitans morsitans Westwood (Diptera: Glossinidae) in Zambia. Bulletin of Entomological Research 68, 437442.CrossRefGoogle Scholar
Meidell, E.M. (1982) Effects of a synthetic juvenile hormonemimic on the reproduction of the tsetse fly Glossina morsitans. Insect Science and its Application 3, 263266.Google Scholar
Miyan, J.A. (1989) The thoracic mechanism for eclosion and digging during the extrication behaviour of Diptera. Physiological Entomology 14, 309317.Google Scholar
Mulligan, H.W. (Ed.) (1970) The African trypanosomiasis. 950 pp. London, Allen & Unwin.Google Scholar
Nash, T.A.M. & Trewern, M.A. (1972) Hourly distribution of larviposition by Glossina austeni Newst. and G. morsitans morsitans Westw. (Dipt., Glossinidae). Bulletin of Entomological Research 61, 693700.CrossRefGoogle Scholar
Nash, T.A.M., Trewern, M.A. & Moloo, S.K. (1976) Observations on the free larval stage of Glossina morsitans morsitans Westw. (Diptera, Glossinidae):the possibility of a larval pheromone. Bulletin of Entomological Research 66, 1724.Google Scholar
Nkouka, E. (1977) Controle neuro-endocrine de l'ovulation et de la parturition chez un insecte vivipare Glossina fuscipes fuscipes (Diptera, Muscidae). Compte Rendu de I'Academie des Sciences Paris, Serie D 285, 7780.Google Scholar
Nogge, G. (1976) Sterility in tsetse flies (Glossina morsitans Westwood) caused by loss of symbionts. Experientia 32, 995.Google Scholar
Parker, A.H. (1955) Experiments on the behaviour of Glossina palpalis larvae, together with observations on the natural breeding-places of the species during the wet season. Annals of Tropical Medicine and Parasitology 50 6974.Google Scholar
Pell, P.E. & Southern, D.I. (1976) Effect of the coccidiostat, sulphaquinoxaline, on symbiosis in the tsetse fly, Glossina species. Microbios Letters 2, 203211.Google Scholar
Phelps, R.J. & Jackson, P.J. (1971) Factors influencing the moment of larviposition and eclosion in Glossina morsitans orientalis Vanderplank (Diptera: Muscidae). Journal of the Entomological Society of South Africa 34, 145157.Google Scholar
Ratnasiri, N.P. & Fraenkel, G. (1974a) Anterior inhibition of pupariation in ligated larvae of Sarcophaga bullata and other fly species: incidence and expression. Annals of the Entomological Society of America 67, 195203.CrossRefGoogle Scholar
Ratnasiri, N.P. & Fraenkel, G. (1974b) The physiological basis of anterior inhibition of puparium formation in ligated fly larvae. Journal of Insect Physiology 20, 105119.Google Scholar
Reid, S.N.M., Fraenkel, G. & Friedman, S. (1987a) Extrication, the primary event in eclosion, and its relationship to digging, pumping and tanning in Sarcophaga bullata. Journal of Insect Physiology 33, 339348.Google Scholar
Reid, S.N.M., Fraenkel, G. & Friedman, S. (1987b) Extrication, the primary event in eclosion, and its neural control in Sarcophaga bullata. Journal of Insect Physiology 33, 481486.CrossRefGoogle Scholar
Retnakaran, A. & Wright, J.E. (1987) Control of insect pests with benzoylphenyl ureas. pp. 205282 in Wright, J. E. & Retnakaran, A. (Eds) Chitin and benzoylphenyl ureas. Dordrecht, Dr W. Junk.Google Scholar
Richard, D.S., Warren, J.T., Saunders, D.S. & Gilbert, L.I. (1987) Haemolymph ecdysteroid titres in diapause- and non diapause-destined larvae and pupae of Sarcophaga argyros toma. Journal of Insect Physiology 33, 115122.Google Scholar
Riordan, E.K. (1986) Abortion by the tsetse fly Glossina palpalis palpalis after treatment with insecticides. Entomologia Experimentalis et Applicata 41, 193200.Google Scholar
Riordan, E.K. (1987) Condition and fate of larvae from insecticide-treated female tsetse flies Glossina palpalis. Entomologia Experimentalis et Applicata 43, 245250.Google Scholar
Robert, A., Grillot, J.P. & Raabe, M. (1981) La larviposition chez la mouche tse-tse Glossina fuscipes. Recherches preliminaires sur son controle. Compte Rendu de l'Academie des Sciences Paris, Serie III 293, 611618.Google Scholar
Robert, A., Grillot, J.P. & Raabe, M. (1984) Experimental and ultrastructural study of the control of ovulation and parturition in the tsetse fly Glossina fuscipes (Diptera). Journal of Insect Physiology 30, 671684.Google Scholar
Robert, A., Strambi, A. & Strambi, C. (1986a) Haemolymph ecdysteroid levels in female tsetse fly Glossina fuscipes (Diptera) during the first reproductive cycle: a comparison between virgin and mated females. Journal of Insect Physiology 32, 665671.Google Scholar
Robert, A., Strambi, A., Strambi, C. & Gonella, J. (1986b) Opposite effects of ecdysone and 20-hydroxyecdysone on in vitro uterus motility of a tsetse fly. Life Sciences 39, 26172622.Google Scholar
Robertson, C.W. (1936) The metamorphosis of Drosophila melanogaster, including an accurately timed account of the principal morphological changes. Journal of Morphology 59, 351400.CrossRefGoogle Scholar
Rogers, D.J. (1988) A general model for the African trypanosomiases. Parasitology 97, 193212.Google Scholar
Rowcliffe, C. & Finlayson, L.H. (1981) Factors influencing the selection of larviposition sites in the laboratory by Glossina morsitans morsitans Westwood (Diptera: Glossinidae). Bulletin of Entomological Research 71, 8196.Google Scholar
Rowcliffe, C. & Finlayson, L.H. (1982) Active and resting behaviour of virgin and pregnant females of Glossina morsitans morsitans Westwood (Diptera: Glossinidae) in the laboratory. Bulletin of Entomological Research 72, 271288.Google Scholar
Ruegg, R.P., Kriger, F.L., Davey, K.G. & Steel, C.G.H. (1981) Ovarian ecdysone elicits release of a mytropic ovulation hormone in Rhodnius (Insecta: Hemiptera). International Journal of Invertebrate Reproduction 3, 357361.Google Scholar
Saunders, D.S. (1972) The effect of starvation on the length of the interlarval period in the tsetse fly Glossina morsitans orientalis Vanderplank. Journal of Entomology, A 46, 197202.Google Scholar
Saunders, D.S. (1982) Insect clocks, 2nd edn. 409 pp. Oxford, Pergamon.Google Scholar
Schlein, Y. (1977) Lethal effect of tetracycline on tsetse flies following damage to bacteroid symbionts. Experientia 33, 450451.Google Scholar
Sehnal, F. & Žďárek, J. (1976) Action of juvenoids on the metamorphosis of cyclorrhaphous Diptera. Journal of Insect Physiology 22, 673682.CrossRefGoogle Scholar
Seligman, I.M. (1980) Bursicon. pp. 137153 in Miller, T.A. (Ed.) Neurohormonal techniques in insects. New York, Springer-Verlag.Google Scholar
Simpson, J.J. (1918) Bionomics of tsetse and other parasitological notes in the Gold Coast. Bulletin of Entomological Research 8, 193214.Google Scholar
Tanaka, S.Guardia, M.Denlinger, D.L. & Wolda, H. (1990) Relationships between body size, reproductive traits, and food resources in three species of tropical flesh flies. Researches on Population Ecology. 32, 303317.CrossRefGoogle Scholar
Tobe, S.S. & Langley, P.A. (1978) Reproductive physiology of Glossina. Annual Review of Entomology 23, 283307.Google Scholar
Truman, J.W. (1985) Hormonal control of ecdysis. pp. 413440 in Kerkut, G.A. & Gilbert, L.I. (Eds) Comprehensive insect physiology, biochemistry and pharmacology. Vol. 8. Oxford, Pergamon.Google Scholar
Turner, D.A. & Snow, W.F. (1984) Reproductive abnormality and loss in natural populations of Glossina pallidipes Austen (Diptera: Glossinidae) in Kenya. Bulletin of Entomological Research 74, 299309.Google Scholar
Wahl, B. (1914) Uber die Kopfbildung cyclorhaphen Dipterenlarven und die postembryonal Entwicklung des Fliegenkopfes. Arbeiten aus den Zoologischen Instituten der Universitat Wein 20, 159272.Google Scholar
Whitehead, D.L. (1974) The retardation of puparium formation in Diptera: could factors other than ecdysone control cuticle stabilisation in Glossina and Sarcophaga species? Bulletin of Entomological Research 64, 223240.Google Scholar
Žďárek, J. (1981) The role of hormones in the control of premetamorphic behaviour in insects. pp. 9931009 in Sehnal, F. & Zabza, A. (Eds). Regulation of insect development and behavior. Wroclaw, Wroclaw Technical University Press.Google Scholar
Žďárek, J. (1985) Regulation of pupariation in flies. pp. 301333 in Kerkut, G.A.Gilbert, L.I. (Eds) Comprehensive insect physiology, biochemistry and pharmacology. Vol. 8. Oxford, Pergamon.Google Scholar
Žďárek, J. & Denlinger, D.L. (1987) Pupal ecdysis in flies: the role of ecdysteroids in its regulation. Journal of Insect Physiology 33, 123128.Google Scholar
Žďárek, J. & Denlinger, D.L. (1991) Wandering behaviour and pupariation in tsetse larvae. Physiological Entomology 16, 523529.Google Scholar
Žďárek, J. & Denlinger, D.L. (1992a) Eclosion behavior in tsetse: extrication from the puparium and expansion of the adult. Journal of Insect Behavior 5, 657668.CrossRefGoogle Scholar
Žďárek, J. & Denlinger, D.L. (1992b) Neural regulation of pupariation in tsetse larvae. Journal of Experimental Biology 173, 1124.CrossRefGoogle ScholarPubMed
Žďárek, J. & Denlinger, D.L. (1992c) Disruption of Glossina mor sitans morsitans (Diptera: Glossinidae) eclosion behaviour: a novel method for evaluating the action of neurotoxic agents. Bulletin of Entomological Research 82, 547552.Google Scholar
Žďárek, J. & Fraenkel, G. (1972) The mechanism of puparium formation in flies. General and Comparative Endocrinology 17, 483489.Google Scholar
Žďárek, J. & Friedman, S. (1986) Pupal ecdysis in flies: mechanisms of evagination of the head and expansion of the thoracic appendages. Journal of Insect Physiology 32, 917923.Google Scholar
Žďárek, J., Sláma, K. &Fraenkel, G. (1979) Changes in internal pressure during puparium formation in flies. Journal of Experimental Zoology 207, 187196.Google Scholar
Žďárek, J., Zavadilová, J., Su, J. & Fraenkel, G. (1984) Post-eclosion behaviour of flies after emergence from the puparium. Acta Entomologica Bohemoslovaca 81, 161170.Google Scholar
Žďárek, J., Reid, S. & Fraenkel, G. (1986) How does an eclosing fly deal with obstacles? Physiological Entomology 11, 107114.Google Scholar
Žďárek, J., Denlinger, D.L. & Otieno, L.H. (1992) Does the tsetse parturition rhythm have a circadian basis? Physiological Entomology 17, 305307.Google Scholar