Thermal tolerance in a south-east African population of the tsetse fly Glossina pallidipes (Diptera, Glossinidae): Implications for forecasting climate change impacts

Journal of Insect Physiology

Volumn 54, Issue 1, 2008, Pages 114-127

  Terblanche, John S ^a   Clusella Trullas, Susana ^a   Deere, Jacques A ^a   Chown, Steven L ^a  

^a STELLENBOSCH UNIVERSITY   (South Africa)

Author keywords

Climate change; Cold tolerance; Fitness costs; Geographic distribution; Insect vector; Phenotypic plasticity; Seasonal variation; Trade offs

Indexed keywords

CLIMATE CHANGE; FLY; GEOGRAPHICAL DISTRIBUTION; PHENOTYPIC PLASTICITY; POPULATION DYNAMICS; POPULATION STRUCTURE; SEASONAL VARIATION;

ACCLIMATIZATION; ANALYSIS OF VARIANCE; ANIMAL; ARTICLE; CLIMATE; COMPARATIVE STUDY; GEOGRAPHY; GREENHOUSE EFFECT; KENYA; MOTOR ACTIVITY; PHYSIOLOGY; POPULATION DYNAMICS; SURVIVAL; TEMPERATURE; TSETSE FLY; ZAMBIA;

ACCLIMATIZATION; ANALYSIS OF VARIANCE; ANIMALS; CLIMATE; GEOGRAPHY; GREENHOUSE EFFECT; KENYA; MOTOR ACTIVITY; POPULATION DYNAMICS; SURVIVAL ANALYSIS; TEMPERATURE; TSETSE FLIES; ZAMBIA;

AFRICA; EAST AFRICA; KENYA; SOUTHERN AFRICA; SUB-SAHARAN AFRICA; ZAMBIA;

ANIMALIA; DIPTERA; GLOSSINA (GENUS); GLOSSINA PALLIDIPES; GLOSSINIDAE; HEXAPODA;

EID: 38149139296     PISSN: 00221910     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jinsphys.2007.08.007     Document Type: Article

References (101)

1. Benjamini Y., and Hochberg Y. Controlling the false discovery rate: a practical and powerful approach to multiple testing. Journal of the Royal Statistical Society B 57 (1995) 289-300
2. Bourne D., Reid R.S., Rogers D.J., Snow W.F., and Wint W. Environmental Change and the Autonomous Control of Tsetse and Trypanosomiasis in Sub-Saharan Africa (2001), Environmental Research Group Oxford Limited, Oxford, UK
3. Bouyer J., Pruvot M., Bengaly Z., Guerin P.M., and Lancelot R. Learning influences host choice in tsetse. Biology Letters 3 (2007) 113-116
4. Burnett G.F. The relation between age and cold resistance in tsetse flies and the value of chilling when transporting tsetse for experiments. Proceedings of the Royal Entomological Society of London A 32 (1957) 53-58
5. Bursell E. The water balance of tsetse flies. Transactions of the Royal Entomological Society of London 111 (1959) 205-235
6. Bursell E. The effect of temperature on the consumption of fat during pupal development in Glossina. Bulletin of Entomological Research 51 (1960) 583-598
7. Bursell E. Environmental aspects: temperature. In: Rockstein M. (Ed). The Physiology of Insecta (1964), Academic Press, New York 283-321
8. Bursell E., and Taylor P. An energy budget for Glossina (Diptera: Glossinidae). Bulletin of Entomological Research 70 (1980) 187-196
9. Buxton P.A., and Lewis D.J. Climate and tsetse flies: laboratory studies upon Glossina submorsitans and tachinoides. Philosophical Transactions of the Royal Society of London B 224 (1934) 175-242
10. Cattand P., Desjeux P., Guzmán M.G., Jannin J., Kroeger A., Médici A., Musgrove P., Nathan M.B., Shaw A., and Schofield C.J. Tropical diseases lacking adequate control measures: dengue, leishmaniasis, and African trypanosomiasis. In: Jamison D.T., et al. (Ed). Disease Control Priorities in Developing Countries. second ed. (2006), Oxford University Press, New York 451-466
11. Chown S.L., and Nicolson S.W. Insect Physiological Ecology. Mechanisms and Patterns (2004), Oxford University Press, Oxford
12. Chown S.L., and Terblanche J.S. Physiological diversity in insects: ecological and evolutionary contexts. Advances in Insect Physiology 33 (2007) 50-152
13. Colinet H., Hance T., and Vernon P. Water relations, fat reserves, survival, and longevity of a cold-exposed parasitic wasp Aphidius colemani (Hymenoptera: Aphidiinae). Environmental Entomology 35 (2006) 228-236
14. David R.J., Gibert P., Pla E., Petavy G., Karan D., and Moreteau B. Cold stress tolerance in Drosophila: analysis of chill coma recovery in D. melanogaster. Journal of Thermal Biology 23 (1998) 291-299
15. David J.R., Gibert P., Moreteau B., Gilchrist G.W., and Huey R.B. The fly that came in from the cold: geographic variation in recovery time from low-temperature exposure in Drosophila subobscura. Functional Ecology 17 (2003) 425-430
16. Esterhuizen J., Kappmeier Green K., Marcotty T., and van den Bossche P. Abundance and distribution of the tsetse flies, Glossina austeni and G. brevipalpis, in different habitats in South Africa. Medical and Veterinary Entomology 19 (2005) 367-371
17. FAO/IAEA, 2002. Annual Report. FAO/IAEA Entomology Unit, Agriculture and Biotechnology Laboratory, Seibersdorf, Austria.
18. Gaston K.J. The Structure and Dynamics of Geographic Ranges (2003), Oxford University Press, Oxford
19. Gibert P., Moreteau B., Petavy G., Karan D., and David J.R. Chill-coma tolerance, a major climatic adaptation among Drosophila species. Evolution 55 (2001) 1063-1068
20. Githeko A.K., Lindsay S.W., Confalonieri U.E., and Patz J.A. Climate change and vector-borne diseases: a regional analysis. Bulletin of the World Health Organisation 78 (2000) 1136-1147
21. Graham C.H., and Hijmans R.J. A comparison of methods for mapping species ranges and species richness. Global Ecology and Biogeography 15 (2006) 578-587
22. Hargrove J.W. 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 (2001) 79-86
23. Hargrove J.W. Tsetse population dynamics. In: Maudlin I., Holmes P.H., and Miles M.A. (Eds). The Trypanosomiases (2004), CABI Publishing, Wallingford 113-138
24. Hargrove J.W., and Brady J. Activity rhythms of tsetse flies (Glossina spp.) (Diptera: Glossinidae) at low and high temperatures in nature. Bulletin of Entomological Research 82 (1992) 321-326
25. Hargrove J.W., and Williams B.G. 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 (1998) 425-435
26. Harvell C.D., Mitchell C.E., Ward J.R., Altizer S., Dobson A.P., Ostfeld R.S., and Samuel M.D. Climate warning and disease risks for terrestrial and marine biota. Science 296 (2002) 2158-2162
27. Hawes T.C., Couldridge C.E., Bale J.S., Worland M.R., and Convey P. Habitat temperature and the temporal scaling of cold hardening in the high Arctic collembolan, Hypogastrura tullbergi (Schäffer). Ecological Entomology 31 (2006) 450-459
28. Helmuth B., Harley C.D.G., Halpin P.M., O'Donnel M., Hofmann G.E., and Blanchette C.A. Climate change and latitudinal patterns of intertidal thermal stress. Science 298 (2002) 1015-1017
29. Helmuth B., Kingsolver J.G., and Carrington E. Biophysics, physiological ecology, and climate change: does mechanism matter?. Annual Review of Physiology 67 (2005) 177-201
30. Hendrickx G., Napala A., Dao B., Batawui D., De Deken R., Vermeilen A., and Slingenbergh J.H.W. A systematic approach to area-wide tsetse distribution and abundance maps. Bulletin of Entomological Research 89 (1999) 231-244
31. Hijmans R.J., and Graham C.H. The ability of climate envelope models to predict the effect of climate change on species distributions. Global Change Biology 12 (2006) 2272-2281
32. Hijmans R.J., Cameron S.E., Parra J.L., Jones P.G., and Jarvis A. Very high resolution interpolated climate surfaces for global land areas. International Journal of Climatology 25 (2005) 1965-1978
33. Hoffmann A.A., Hallas R., Anderson A.R., and Telonis-Scott M. Evidence for a robust sex-specific trade-off between cold resistance and starvation resistance in Drosophila melanogaster. Journal of Evolutionary Biology 18 (2005) 804-810
34. Hulme M. Climate Change and Southern Africa. An Exploration of Some Potential Impacts and Implications in the SADC Region (1996), WWF International Climate Research Unit, Norwich
35. Huyton P.M., and Brady J. Some effects of light and heat on feeding and resting behavior of tsetse flies, Glossina morsitans Westwood. Journal of Entomology A-Physiology and Behaviour 50 (1975) 23-30
36. Jack R.W. The life economy of a tsetse fly. Proceedings of the Rhodesia Scientific Association 34 (1942) 2-15
37. Jackson C.H.N. The hunger-cycles of Glossina morsitans Westwood and G. swynnertoni Austen. Journal of Animal Ecology 23 (1954) 368-372
38. Kearney M., and Porter W.P. Mapping the fundamental niche: physiology, climate and the distribution of a nocturnal lizard. Ecology 85 (2004) 3119-3131
39. Kelty J.D., and Lee R.E. Induction of rapid cold hardening by cooling at ecologically relevant rates in Drosophila melanogaster. Journal of Insect Physiology 45 (1999) 719-726
40. Kerr J.T., Kharouba H.M., and Currie D.J. The macroecological contribution to global change solutions. Science 316 (2007) 1581-1584
41. Kitron U., Otieno L.H., Hungerford L.L., Odulaja A., Brigham W.U., Okello O.O., Joselyn M., Mohamed-Ahmed M.M., and Cook E. Spatial analysis of the distribution of tsetse flies in the Lambwe Valley, Kenya using Landsat TM satellite imagery and GIS. Journal of Animal Ecology 65 (1996) 371-380
42. Kovats R.S., Campbell-Lendrum D.H., McMichael A.J., Woodward A., and Cox J.St.H. Early effects of climate change: do they include changes in vector-borne disease?. Philosophical Transactions of the Royal Society of London B 356 (2001) 1057-1068
43. Kuhn K.G., Campbell-Lendrum D.H., Armstrong B., and Davies C.R. Malaria in Britain: past, present, and future. Proceedings of the National Academy of Sciences of the USA 100 (2003) 9997-10001
44. Langley P.A. Physiology of tsetse flies (Glossina ssp.) (Diptera: Glossinidae): a review. Bulletin of Entomological Research 67 (1977) 523-574
45. Leak S.G.A. Tsetse Biology and Ecology (1999), CABI Publishing, Wallingford
46. Lee Jr. R.E., Chen C.-P., and Denlinger D.L. A rapid cold-hardening process in insects. Science 238 (1987) 1415-1417
47. Lee R.E., Elnitsky M.A., Rinehart J.P., Hayward S.A.L., Sandro L.H., and Denlinger D.L. Rapid cold-hardening increases the freezing tolerance of the Antarctic midge Belgica antarctica. Journal of Experimental Biology 209 (2006) 399-406
48. MacDonald S.S., Rako L., Batterham P., and Hoffmann A.A. Dissecting chill coma recovery as a measure of cold resistance: evidence for a biphasic response in Drosophila melanogaster. Journal of Insect Physiology 50 (2004) 695-700
49. Macfie J.W.S. Experiments and observations upon Glossina palpalis. Bulletin of Entomological Research 3 (1912) 61-72
50. Martens P., Kovats R.S., Nijhof S., deVries P., Livermore M.T.J., Bradley D.J., Cox J., and McMichael A.J. Climate change and future populations at risk of malaria. Global Environmental Change 9 (1999) S89-S107
51. Mellanby K. Experimental work with the tsetse fly Glossina palpalis in Uganda. Bulletin of Entomological Research 27 (1936) 611-633
52. Misener S.R., Chen C.-P., and Walker V.K. Cold tolerance and proline metabolic gene expression in Drosophila melanogaster. Journal of Insect Physiology 47 (2001) 393-400
53. Mohamed-Ahmed M.M., and Wynholds Y. Effects of vegetation and weather on trap catches of Glossina fuscipes fuscipes near Lake Victoria, Kenya. Entomologia Experimentalis et Applicata 85 (1997) 231-236
54. Mutika G.N., Opiyo E., and Robinson A.S. Assessing mating performance of male Glossina pallidipes (Diptera: Glossinidae) using a walk-in field cage. Bulletin of Entomological Research 91 (2001) 281-287
55. Muzari M.O., and Hargrove J.W. Artificial larviposition sites for field collections of the puparia of tsetse flies Glossina pallidipes and G. m. morsitans (Diptera: Glossinidae). Bulletin of Entomological Research 95 (2005) 221-229
56. Nilson T.L., Sinclair B.J., and Roberts S.P. The effects of carbon dioxide anesthesia and anoxia on rapid cold-hardening and chill coma recovery in Drosophila melanogaster. Journal of Insect Physiology 52 (2006) 1027-1033
57. Parmesan C., and Yohe G. A globally coherent fingerprint of climate change impacts across natural systems. Nature 421 (2003) 37-42
58. Pascual M., Ahumada J.A., Chaves L.F., Rodo X., and Bouma M. Malaria resurgence in the East African highlands: temperature trends revisited. Proceedings of the National Academy of Sciences USA 103 (2006) 5829-5834
59. Patz J.A. A human disease indicator for the effects of recent global climate change. Proceedings of the National Academy of Sciences USA 99 (2002) 12506-12508
60. Patz J.A., Graczyk T.K., Geller N., and Vittor A.Y. Effects of environmental change on emerging parasitic diseases. International Journal for Parasitology 30 (2000) 1395-1405
61. Phelps R.J., and Burrows P.M. Lethal temperature for puparia of Glossina morsitans orientalis. Entomologia Experimentalis et Applicata 22 (1969) 23-32
62. Pörtner H.O., and Knust R. Climate change affects marine fishes through oxygen limitation of thermal tolerance. Science 315 (2007) 95-97
63. Potts W.H. Observations on Glossina morsitans, Westw., in East Africa. Bulletin of Entomological Research 24 (1933) 293-300
64. Purse B.V., Mellor P.S., Rogers D.J., Samuel A.R., Mertens P.P.C., and Baylis M. Climate change and the recent emergence of bluetongue in Europe. Nature Reviews Microbiology 3 (2005) 171-181
65. Rako L., and Hoffmann A.A. Complexity of the cold acclimation response in Drosophila melanogaster. Journal of Insect Physiology 52 (2006) 94-104
66. Robays J., Kadima A.E., Lutumba P., Bilenge C.M.M., Mesu V.K.B.K., De Deken R., Makabuza J., Deguerry M., Van der Stuyft P., and Boelaert M. Human African trypanosomiasis amongst urban residents in Kinshasa: a case-control study. Tropical Medicine and International Health 9 (2004) 869-875
67. Robinson T., Rogers D., and Williams B. Mapping tsetse habitat suitability in the common fly belt of Southern Africa using multivariate analysis of climate and remotely sensed vegetation data. Medical and Veterinary Entomology 11 (1997) 235-245
68. Robinson T., Rogers D., and Williams B. Univariate analysis of tsetse habitat in the common fly belt of Southern Africa using climate and remotely sensed vegetation data. Medical and Veterinary Entomology 11 (1997) 223-234
69. Rogers D.J. A general model for tsetse populations. Insect Science and its Application 11 (1990) 331-346
70. Rogers D.J. Satellites, space, time and the African trypanosomiases. Advances in Parasitology 47 (2000) 129-171
71. Rogers D.J. Models for vectors and vector-borne diseases. Advances in Parasitology 62 (2006) 1-37
72. Rogers D.J., and Packer M.J. Vector-borne diseases, models, and global change. The Lancet 342 (1993) 1282-1284
73. Rogers D.J., and Randolph S.E. Distribution and abundance of tsetse flies (Glossina spp.). Journal of Animal Ecology 55 (1986) 1007-1025
74. Rogers D.J., and Randolph S.E. Mortality rates and population density of tsetse flies correlated with satellite imagery. Nature 351 (1991) 739-741
75. Rogers D.J., and Randolph S.E. Distribution of tsetse and ticks in Africa: past, present and future. Parasitology Today 9 (1993) 266-271
76. Rogers D.J., and Randolph S.E. The global spread of malaria in a future, warmer world. Science 289 (2000) 1763-1766
77. Rogers D.J., and Randolph S.E. A response to the aim of eradicating tsetse from Africa. Trends in Parasitology 18 (2002) 534-536
78. Rogers D.J., and Randolph S.E. Climate change and vector-borne diseases. Advances in Parasitology 62 (2006) 346-382
79. Rogers D.J., and Robinson T.P. Tsetse distribution. In: Maudlin I., Holmes P.H., and Miles M.A. (Eds). The Trypanosomiases (2004), CABI Publishing, Wallingford 139-180
80. Rogers D.J., and Williams B.G. Tsetse distribution in Africa: seeing the wood and the trees. In: Edwards P.J., May R.M., and Webb N.R. (Eds). Large-Scale Ecology and Conservation Biology (1994), Blackwell Science, Oxford 247-271
81. Rogers D.J., Randolph S.E., Snow R.W., and Hay S.I. Satellite imagery in the study and forecast of malaria. Nature 415 (2002) 710-715
82. Roura-Pascual N., Suarez A.V., Gomez C., Pons P., Touyama Y., Wild A.L., and Peterson A.T. Geographical potential of Argentine ants (Linepithema humile Mayr) in the face of global climate change. Proceedings of the Royal Society of London B 271 (2004) 2527-2534
83. Sinclair B.J., and Chown S.L. Rapid responses to high temperature and desiccation but not to low temperature in the freeze-tolerant sub-Antarctic caterpillar Pringleophaga marioni (Lepidoptera, Tineidae). Journal of Insect Physiology 49 (2003) 45-52
84. Sinclair B.J., and Chown S.L. Deleterious effects of repeated cold exposure in a freeze-tolerant sub-Antarctic caterpillar. Journal of Experimental Biology 208 (2005) 869-879
85. Sinclair B.J., and Chown S.L. Rapid cold-hardening in a Karoo beetle, Afrinus sp. Physiological Entomology 31 (2006) 98-101
86. Sinclair B.J., Terblanche J.S., Scott M.B., Blatch G.L., Klok C.J., and Chown S.L. Environmental physiology of three species of Collembola at Cape Hallett, North Victoria Land, Antarctica. Journal of Insect Physiology 52 (2006) 29-50
87. Sumilo D., Asokliene L., Bormane A., Vasilenko V., Golovljova I., and Randolph S.E. Climate change cannot explain the upsurge of tick-borne encephalitis in the Baltics. PLoS One 6 (2007) e500
88. Sutherst R.W. Global change and human vulnerability to vector-borne diseases. Clinical Microbiology Reviews 17 (2004) 136-173
89. Terblanche J.S., and Chown S.L. The relative contributions of developmental plasticity and adult acclimation to physiological variation in the tsetse fly, Glossina pallidipes (Diptera, Glossinidae). Journal of Experimental Biology 209 (2006) 1064-1073
90. Terblanche J.S., and Chown S.L. The effects of temperature, body mass and feeding on metabolic rate in the tsetse fly Glossina morsitans centralis. Physiological Entomology 32 (2007) 175-180
91. Terblanche J.S., Klok C.J., and Chown S.L. Temperature-dependence of metabolic rate in Glossina morsitans morsitans (Diptera, Glossinidae) does not vary with gender, age, feeding, pregnancy or acclimation. Journal of Insect Physiology 51 (2005) 861-870
92. Terblanche J.S., Klok C.J., Krafsur E.S., and Chown S.L. Phenotypic flexibility and geographic variation in thermal tolerance and water loss of the tsetse fly Glossina pallidipes (Diptera: Glossinidae): implications for distribution modelling. American Journal of Tropical Medicine and Hygiene 74 (2006) 786-794
93. Terblanche J.S., Marais E., and Chown S.L. Stage-related variation in rapid cold hardening as a test of the environmental predictability hypothesis. Journal of Insect Physiology 53 (2007) 455-462
94. Terblanche, J.S., Deere, J.A., Clusella Trullas, S., Janion, C., Chown, S.L. Critical thermal limits are context dependent. Proceedings of the Royal Society of London B, in press, doi:10.1098/rspb.2007.0985.
95. Thomas C.D., Cameron A., Green R.E., Bakkenes M., Beaumont L.J., Collingham Y.C., et al. Extinction risk from climate change. Nature 427 (2004) 145-148
96. Thuiller W., Lavorel S., Araujo M.B., Sykes M.T., and Prentice I.C. Climate change threats to plant diversity in Europe. Proceedings of the National Academy of Sciences USA 102 (2005) 8245-8250
97. Torr S.J., and Hargrove J.W. Behaviour of tsetse (Diptera: Glossinidae) during the hot season in Zimbabwe: the interaction of micro-climate and reproductive status. Bulletin of Entomological Research 89 (1999) 365-379
98. Urban M.C., Phillips B.L., Skelly D.K., and Shine R. The cane toad's (Chaunus [Bufo] marinus) increasing ability to invade Australia is revealed by a dynamically updated range model. Proceedings of the Royal Society of London B 274 (2007) 1413-1419
99. Van Etten J. Comparative studies on the diurnal activity pattern in two field and laboratory populations of Glossina pallidipes. Entomologia Experimentalis et Applicata 32 (1982) 38-45
100. Walther G.-R., Post E., Convey P., Menzel A., Parmesan C., Beebee T.J.C., Fromentin J.-M., Hoegh-Guldberg O., and Bairlein F. Ecological responses to recent climate change. Nature 416 (2002) 389-395
101. Wilson R.J., Gutiérrez D., Gutiérrez J., Martínez D., Agudo R., and Monserrat V.J. Changes to the elevational limits and extent of species ranges associated with climate change. Ecology Letters 8 (2005) 1138-1146