Evidence for transient deleterious thermal acclimation in field recapture rates of an invasive tropical species, Bactrocera dorsalis (Diptera: Tephritidae)

Kevin Malod , Anandi Bierman , Minette Karsten , Aruna Manrakhan , Christopher W. Weldon , John S. Terblanche

Insect Science ›› 2025, Vol. 32 ›› Issue (3) : 1004 -1018.

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Insect Science ›› 2025, Vol. 32 ›› Issue (3) : 1004 -1018. DOI: 10.1111/1744-7917.13435
ORIGINAL ARTICLE

Evidence for transient deleterious thermal acclimation in field recapture rates of an invasive tropical species, Bactrocera dorsalis (Diptera: Tephritidae)

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Abstract

Knowing how environmental conditions affect performance traits in pest insects is important to improve pest management strategies. It can be informative for monitoring, but also for control programs where insects are mass-reared, and field-released. Here, we investigated how adult thermal acclimation in sterile Bactrocera dorsalis affects dispersal and recapture rates in the field using a mark-release-recapture method. We also considered how current abiotic factors may affect recapture rates and interact with thermal history. We found that acclimation at 20 or 30 °C for 4 d prior to release reduced the number of recaptures in comparison with the 25 °C control group, but with no differences between groups in the willingness to disperse upon release. However, the deleterious effects of acclimation were only detectable in the first week following release, whereafter only the recent abiotic conditions explained recapture rates. In addition, we found that recent field conditions contributed more than thermal history to explain patterns of recaptures. The two most important variables affecting the number of recaptures were the maximum temperature and the average relative humidity experienced in the 24 h preceding trapping. Our results add to the handful of studies that have considered the effect of thermal acclimation on insect field performance, but notably lend support to the deleterious acclimation hypothesis among the various hypotheses that have been proposed. Finally, this study shows that there are specific abiotic conditions (cold/hot and dry) in which recaptures will be reduced, which may therefore bias estimates of wild population size.

Keywords

dispersal / mark-release-recapture / sterile insects / thermal acclimation / Tephritidae

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Kevin Malod, Anandi Bierman, Minette Karsten, Aruna Manrakhan, Christopher W. Weldon, John S. Terblanche. Evidence for transient deleterious thermal acclimation in field recapture rates of an invasive tropical species, Bactrocera dorsalis (Diptera: Tephritidae). Insect Science, 2025, 32(3): 1004-1018 DOI:10.1111/1744-7917.13435

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References

[1]

Adzim, C.A. Billah, M.K. and Afreh-Nuamah, K. (2016) Abundance of African invader fly, Bactrocera invadens Drew, tsuruta and white (Diptera: Tephritidae) and influence of weather parameters on trap catches in mango in the Volta region of Ghana. SpringerPlus, 5, 968.

[2]

Ben-Yosef, M. Verykouki, E. Altman, Y. Nemni-Lavi, E. Papadopoulos, N.T. and Nestel, D. (2021) Effects of thermal acclimation on the tolerance of Bactrocera zonata (Diptera: Tephritidae) to hydric stress. Frontiers in Physiology, 12, 686424.

[3]

Berger, D. Walters, R. and Gotthard, K. (2008) What limits insect fecundity? Body size- and temperature-dependent egg maturation and oviposition in a butterfly. Functional Ecology, 22, 523-529.

[4]

Boersma, N. Boardman, L. Gilbert, M. and Terblanche, J.S. (2018) Sex-dependent thermal history influences cold tolerance, longevity and fecundity in false codling moth Thaumatotibia leucotreta (Lepidoptera: Tortricidae). Agricultural and Forest Entomology, 20, 41-50.

[5]

Boersma, N. Boardman, L. Gilbert, M. and Terblanche, J.S. (2019) Cold treatment enhances low-temperature flight performance in false codling moth, Thaumatotibia leucotreta (Lepidoptera: Tortricidae). Agricultural and Forest Entomology, 21, 243-251.

[6]

Bolker, B.M. Brooks, M.E. Clark, C.J. Geange, S.W. Poulsen, J.R. Stevens, M.H.H. et al. (2009) Generalized linear mixed models: a practical guide for ecology and evolution. Trends in Ecology & Evolution, 24, 127-135.

[7]

Bowler, K. and Terblanche, J.S. (2008) Insect thermal tolerance: what is the role of ontogeny, ageing and senescence? Biological Reviews, 83, 339-355.

[8]

Chailleux, A. Thiao, D.S. Diop, S. Bouvery, F. Ahmad, S. Caceres-Barrios, C. et al. (2021) Understanding Bactrocera dorsalis trapping to calibrate area-wide management. Journal of Applied Entomology, 145, 831-840.

[9]

Chen, M. Chen, P. Ye, H. Yuan, R. Wang, X. and Xu, J. (2015) Flight capacity of Bactrocera dorsalis (Diptera: Tephritidae) adult females based on flight mill studies and flight muscle ultrastructure. Journal of Insect Science, 15, 141.

[10]

Chidawanyika, F. and Terblanche, J.S. (2011) Costs and benefits of thermal acclimation for codling moth, Cydia pomonella (Lepidoptera: Tortricidae): implications for pest control and the sterile insect release programme. Evolutionary Applications, 4, 534-544.

[11]

Chown, S.L. and Terblanche, J.S. (2006) Physiological diversity in insects: ecological and evolutionary contexts. Advances in Insect Physiology (ed. S.J. Simpson), pp. 50-152. Academic Press.

[12]

Crawley, M.J. (2013) The R Book, 2nd edn. Wiley, Chichester, West Sussex, United Kingdom.

[13]

De Meyer, M. Robertson, M.P. Mansell, M.W. Ekesi, S. Tsuruta, K. Mwaiko, W. et al. (2010) Ecological niche and potential geographic distribution of the invasive fruit fly Bactrocera invadens (Diptera, Tephritidae). Bulletin of Entomological Research, 100, 35-48.

[14]

Diouf, E.G. Brévault, T. Ndiaye, S. Faye, E. Chailleux, A. Diatta, P. et al. (2022) An agent-based model to simulate the boosted sterile insect technique for fruit fly management. Ecological Modelling, 468, 109951.

[15]

EFSA Panel on Plant Health (PLH), Bragard, C. Dehnen-Schmutz, K. Di Serio, F. Gonthier, P. Jacques, M.-A. et al. (2020) Pest categorisation of non-EU Tephritidae. EFSA Journal, 18, e05931.

[16]

Ekesi, S. De Meyer, M. Mohamed, S.A. Virgilio, M. and Borgemeister, C. (2016) Taxonomy, ecology and management of native and exotic fruit fly species in Africa. Annual Review of Entomology, 61, 219-238.

[17]

Fay, H. and Meats, A. (1987a) The sterile insect release method and the importance of thermal conditioning before release—field-cage experiments with Dacus tryoni in spring weather. Australian Journal of Zoology, 35, 197-204.

[18]

Fay, H. and Meats, A. (1987b) Survival rates of the Queensland fruit-fly, Dacus tryoni, in early spring - field-cage studies with cold-acclimated wild flies and irradiated, warm-acclimated or cold-acclimated, laboratory flies. Australian Journal of Zoology, 35, 187-195.

[19]

Feng, C.X. (2021) A comparison of zero-inflated and hurdle models for modeling zero-inflated count data. Journal of Statistical Distributions and Applications, 8, 8.

[20]

Fezza, T.J. Follett, P.A. and Shelly, T.E. (2021) Effect of the timing of pupal irradiation on the quality and sterility of oriental fruit flies (Diptera: Tephritidae) for use in sterile insect technique. Applied Entomology and Zoology, 56, 443-450.

[21]

Fezza, T.J. and Shelly, T.E. (2021) Comparative dispersal and survival of male oriental fruit flies (Diptera: Tephritidae) from wild and genetic sexing strains. International Journal of Tropical Insect Science, 41, 751-757.

[22]

Francis, J.S. Mueller, T.G. and Vannette, R.L. (2023) Intraspecific variation in realized dispersal probability and host quality shape nectar microbiomes. New Phytologist, 240, 1233-1245.

[23]

Frazier, M.R. Harrison, J.F. Kirkton, S.D. and Roberts, S.P. (2008) Cold rearing improves cold-flight performance in Drosophila via changes in wing morphology. Journal of Experimental Biology, 211, 2116-2122.

[24]

Frazier, M.R. Huey, R.B. and Berrigan, D. (2006) Thermodynamics constrains the evolution of insect population growth rates: “warmer is better.” The American Naturalist, 168, 512-520.

[25]

Froerer, K.M. Peck, S.L. Mcquate, G.T. Vargas, R.I. Jang, E.B. and Mcinnis, D.O. (2010) Long-distance movement of Bactrocera dorsalis (Diptera: Tephritidae) in Puna, Hawaii: how far can they go? American Entomologist, 56, 88-95.

[26]

Guo, Z. Li, N. Lu, Y. Qin, D. Xiao, C. Xie, Z. et al. (2023) Rapid cold hardening and cold acclimation promote cold tolerance of oriental fruit fly, Bactrocera dorsalis (Hendel) by physiological substances transformation and cryoprotectants accumulation. Bulletin of Entomological Research, 113, 574-586.

[27]

Gutierrez, A.P. Ponti, L. Neteler, M. Suckling, D.M. and Cure, J.R. (2021) Invasive potential of tropical fruit flies in temperate regions under climate change. Communications Biology, 4, 1141.

[28]

Hill, M.P. and Terblanche, J.S. (2014) Niche overlap of congeneric invaders supports a single-species hypothesis and provides insight into future invasion risk: implications for global management of the Bactrocera dorsalis complex. PLoS ONE, 9, e90121.

[29]

Hoffmann, A.A. and Bridle, J. (2022) The dangers of irreversibility in an age of increased uncertainty: revisiting plasticity in invertebrates. Oikos, 2022, e08715.

[30]

Hoskins, J.L. Janion-Scheepers, C. Ireland, E. Monro, K. and Chown, S.L. (2020) Constant and fluctuating temperature acclimations have similar effects on phenotypic plasticity in springtails. Journal of Thermal Biology, 93, 102690.

[31]

Hou, Q.L. Chen, E.H. Dou, W. and Wang, J.J. (2020) Assessment of Bactrocera dorsalis (Diptera: Tephritidae) diets on adult fecundity and larval development: insights into employing the sterile insect technique. Journal of Insect Science, 20, 7.

[32]

Huey, R.B. Berrigan, D. Gilchrist, G.W. and Herron, J.C. (1999) Testing the adaptive significance of acclimation: a strong inference approach. American Zoologist, 39, 323-336.

[33]

Inskeep, J.R. Allen, A.P. Taylor, P.W. Rempoulakis, P. and Weldon, C.W. (2021) Canopy distribution and microclimate preferences of sterile and wild Queensland fruit flies. Scientific Reports, 11, 13010.

[34]

Kellermann, V. Van Heerwaarden, B. and Sgrò, C.M. (2017) How important is thermal history? Evidence for lasting effects of developmental temperature on upper thermal limits in Drosophila melanogaster. Proceedings of the Royal Society B: Biological Sciences, 284, 20170447.

[35]

Kingsolver, J.G. Arthur Woods, H. Buckley, L.B. Potter, K.A. Maclean, H.J. and Higgins, J.K. (2011) Complex life cycles and the responses of insects to climate change. Integrative and Comparative Biology, 51, 719-732.

[36]

Klowden, M.J. (2013) Chapter 10—locomotor systems. Physiological Systems in Insects, 3rd edn (ed. M.J. Klowden). Academic Press, San Diego.

[37]

Kotzé, Z. Villet, M.H. and Weldon, C.W. (2015) Effect of temperature on development of the blowfly, Lucilia cuprina (Wiedemann) (Diptera: Calliphoridae). International Journal of Legal Medicine, 129, 1155-1162.

[38]

Kristensen, T.N. Hoffmann, A.A. Overgaard, J. Sørensen, J.G. Hallas, R. and Loeschcke, V. (2008) Costs and benefits of cold acclimation in field-released Drosophila. Proceedings of the National Academy of Sciences USA, 105, 216-221.

[39]

Lance, D.R. and Mcinnis, D.O. (2005) Biological basis of the sterile insect technique. Sterile Insect Technique: Principles and Practice in Area-Wide Integrated Pest Management (eds. V. A. Dyck, J. Hendrichs & A. S. Robinson). Springer Netherlands, Dordrecht.

[40]

Lemke, A. Kowarik, I. and Von Der Lippe, M. (2019) How traffic facilitates population expansion of invasive species along roads: the case of common ragweed in Germany. Journal of Applied Ecology, 56, 413-422.

[41]

Loeschcke, V. and Hoffmann, A.A. (2007) Consequences of heat hardening on a field fitness component in Drosophila depend on environmental temperature. The American Naturalist, 169, 175-183.

[42]

López-Martínez, G. and Hahn, D.A. (2014) Early life hormetic treatments decrease irradiation-induced oxidative damage, increase longevity, and enhance sexual performance during old age in the Caribbean fruit fly. PLoS ONE, 9, e88128.

[43]

Makumbe, L.D.M. Moropa, T.P. Manrakhan, A. and Weldon, C.W. (2020) Effect of sex, age and morphological traits on tethered flight of Bactrocera dorsalis (Hendel) (Diptera: Tephritidae) at different temperatures. Physiological Entomology, 45, 110-119.

[44]

Malacrida, A.R. Gomulski, L.M. Bonizzoni, M. Bertin, S. Gasperi, G. and Guglielmino, C.R. (2007) Globalization and fruitfly invasion and expansion: the medfly paradigm. Genetica, 131, 1-9.

[45]

Malod, K. Bali, E.-M.D. Gledel, C. Moquet, L. Bierman, A. Bataka, E. et al. (2023) Tethered-flight performance of thermally-acclimated pest fruit flies (Diptera: Tephritidae) suggests that heat waves may promote the spread of Bactrocera species. Pest Management Science, 79, 4153-4161.

[46]

Manoukis, N.C. and Carvalho, L.A.F.N. (2020) Flight burst duration as an indicator of flight ability and physical fitness in two species of tephritid fruit flies. Journal of Insect Science, 20, 11.

[47]

Manoukis, N.C. Cha, D.H. Collignon, R.M. and Shelly, T.E. (2018) Terminalia larval host fruit deduces the response of Bactrocera dorsalis (Diptera: Tephritidae) adults to the male lure methyl eugenol. Journal of Economic Entomology, 111, 1644-1649.

[48]

Marec, F. and Vreysen, M.J.B. (2019) Advances and challenges of using the sterile insect technique for the management of pest Lepidoptera. Insects, 10, 371.

[49]

Marinho, R.A. Beserra, E.B. Bezerra-Gusmão, M.A. Porto, V.D.S. Olinda, R.A. and Dos Santos, C.A.C. (2016) Effects of temperature on the life cycle, expansion, and dispersion of Aedes aegypti (Diptera: Culicidae) in three cities in Paraiba, Brazil. Journal of Vector Ecology, 41, 1-10.

[50]

Meats, A. (1973) Rapid acclimatization to low temperature in the Queensland fruit fly, Dacus tryoni. Journal of Insect Physiology, 19, 1903-1911.

[51]

Mudavanhu, P. Addison, P. and Conlong, D.E. (2014) Impact of mass rearing and gamma irradiation on thermal tolerance of Eldana saccharina. Entomologia Experimentalis et Applicata, 153, 55-63.

[52]

Mutamiswa, R. Nyamukondiwa, C. Chikowore, G. and Chidawanyika, F. (2021) Overview of oriental fruit fly, Bactrocera dorsalis (Hendel) (Diptera: Tephritidae) in Africa: from invasion, bio-ecology to sustainable management. Crop Protection, 141, 105492.

[53]

Mutamiswa, R. Tarusikirwa, V.L. Nyamukondiwa, C. Cuthbert, R.N. and Chidawanyika, F. (2023) Thermal stress exposure of pupal oriental fruit fly has strong and trait-specific consequences in adult flies. Physiological Entomology, 48, 35-44.

[54]

Nyamakondiwa, C. Kleynhans, E. and Terblanche, J.S. (2010) Phenotypic plasticity of thermal tolerance contributes to the invasion potential of Mediterranean fruit flies (Ceratitis capitata). Ecological Entomology, 35, 565-575.

[55]

Nyamukondiwa, C. and Terblanche, J.S. (2010) Within-generation variation of critical thermal limits in adult Mediterranean and Natal fruit flies Ceratitis capitata and Ceratitis rosa: thermal history affects short-term responses to temperature. Physiological Entomology, 35, 255-264.

[56]

Orankanok, W. Chinvinijkul, S. Thanaphum, S. Sitilob, P. and Enkerlin, W.R. (2007) Area-wide integrated control of oriental fruit fly Bactrocera dorsalis and guava fruit fly Bactrocera correcta in Thailand. Area-Wide Control of Insect Pests (eds. M.J.B. Vreysen, A.S. Robinson & J. Hendrichs), pp. 517-526. Springer, Dordrecht.

[57]

Parratt, S.R. Walsh, B.S. Metelmann, S. White, N. Manser, A. Bretman, A.J. et al. (2021) Temperatures that sterilize males better match global species distributions than lethal temperatures. Nature Climate Change, 11, 481-484.

[58]

Pieterse, W. Terblanche, J.S. and Addison, P. (2017) Do thermal tolerances and rapid thermal responses contribute to the invasion potential of Bactrocera dorsalis (Diptera: Tephritidae)? Journal of Insect Physiology, 98, 1-6.

[59]

Resilva, S.S. and Pereira, R. (2014) Age- and temperature-related pupal eye colour changes in various tephritid fruit fly species with a view to optimizing irradiation timing. International Journal of Tropical Insect Science, 34, S59-S65.

[60]

Sgrò, C.M. Terblanche, J.S. and Hoffmann, A.A. (2016) What can plasticity contribute to insect responses to climate change? Annual Review of Entomology, 61, 433-451.

[61]

Shelly, T.E. and Edu, J. (2010) Mark-release-recapture of males of Bactrocera cucurbitae and B. dorsalis (Diptera: Tephritidae) in two residential areas of Honolulu. Journal of Asia-Pacific Entomology, 13, 131-137.

[62]

Shelly, T.E. Edu, J. Pahio, E. Wee, S.L. and Nishida, R. (2008) Re-examining the relationship between sexual maturation and age of response to methyl eugenol in males of the oriental fruit fly. Entomologia Experimentalis et Applicata, 128, 380-388.

[63]

Shelly, T.E. and Nishimoto, J. (2011) Additional measurements of distance-dependent capture probabilities for released males of Bactrocera cucurbitae and B. dorsalis (Diptera: Tephritidae) in Honolulu. Journal of Asia-Pacific Entomology, 14, 271-276.

[64]

Shinner, R. Terblanche, J.S. and Clusella-Trullas, S. (2020) Across-stage consequences of thermal stress have trait-specific effects and limited fitness costs in the harlequin ladybird, Harmonia axyridis. Evolutionary Ecology, 34, 555-572.

[65]

Sinclair, B.J. Sørensen, J.G. and Terblanche, J.S. (2022) Harnessing thermal plasticity to enhance the performance of mass-reared insects: opportunities and challenges. Bulletin of Entomological Research, 112, 441-450.

[66]

Steyn, V.M. Mitchell, K.A. Nyamukondiwa, C. and Terblanche, J.S. (2022) Understanding costs and benefits of thermal plasticity for pest management: insights from the integration of laboratory, semi-field and field assessments of Ceratitis capitata (Diptera: Tephritidae). Bulletin of Entomological Research, 112, 458-468.

[67]

Sutantawong, M. Orankanok, W. Enkerlin, W. Wornoayporn, V. Caceres, C. and Barnes, B. (2002) The sterile insect technique for control of the oriental fruit fly, Bactrocera dorsalis (Hendel), in mango orchards in Ratchaburi Province, Thailand. Proceedings, Symposium: 6th International Symposium on Fruit Flies of Economic Importance, pp. 223-232. Stellenbosch, South Africa

[68]

Telles-Romero, R. Toledo, J. Hernández, E. Quintero-Fong, J.L. and Cruz-López, L. (2011) Effect of temperature on pupa development and sexual maturity of laboratory Anastrepha obliqua adults. Bulletin of Entomological Research, 101, 565-571.

[69]

Terblanche, J.S. and Chown, S.L. (2006) 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, 1064-1073.

[70]

Terblanche, J.S. and Kleynhans, E. (2009) Phenotypic plasticity of desiccation resistance in Glossina puparia: are there ecotype constraints on acclimation responses? Journal of Evolutionary Biology, 22, 1636-1648.

[71]

Theron, C.D. Manrakhan, A. and Weldon, C.W. (2017) Host use of the oriental fruit fly, Bactrocera dorsalis (Hendel) (Diptera: Tephritidae), in South Africa. Journal of Applied Entomology, 141, 810-816.

[72]

Thomson, L.J. Robinson, M. and Hoffmann, A.A. (2001) Field and laboratory evidence for acclimation without costs in an egg parasitoid. Functional Ecology, 15, 217-221.

[73]

Vayssières, J.-F. Korie, S. and Ayegnon, D. (2009) Correlation of fruit fly (Diptera Tephritidae) infestation of major mango cultivars in Borgou (Benin) with abiotic and biotic factors and assessment of damage. Crop Protection, 28, 477-488.

[74]

Weldon, C.W. Nyamukondiwa, C. Karsten, M. Chown, S.L. and Terblanche, J.S. (2018) Geographic variation and plasticity in climate stress resistance among southern African populations of Ceratitis capitata (Wiedemann) (Diptera: Tephritidae). Scientific Reports, 8, 9849.

[75]

Weldon, C.W. Schutze, M.K. and Karsten, M. (2014) Trapping to monitor Tephritid movement: results, best practice, and assessment of alternatives. Trapping and the Detection, Control, and Regulation of Tephritid Fruit Flies: Lures, Area-Wide Programs, and Trade Implications (eds. T. Shelly, N. Epsky, E. B. Jang, J. Reyes-Flores & R. Vargas). Springer Netherlands, Dordrecht.

[76]

Weldon, C.W. Terblanche, J.S. and Chown, S.L. (2011) Time-course for attainment and reversal of acclimation to constant temperature in two Ceratitis species. Journal of Thermal Biology, 36, 479-485.

[77]

Weldon, C.W. Yap, S. and Taylor, P.W. (2013) Desiccation resistance of wild and mass-reared Bactrocera tryoni (Diptera: Tephritidae). Bulletin of Entomological Research, 103, 690-699.

[78]

Willot, Q. Loos, B. and Terblanche, J.S. (2021) Interactions between developmental and adult acclimation have distinct consequences for heat tolerance and heat stress recovery. Journal of Experimental Biology, 224, jeb242479.

[79]

Wilson, R.S. and Franklin, C.E. (2002) Testing the beneficial acclimation hypothesis. Trends in Ecology & Evolution, 17, 66-70.

[80]

Yusof, S. Mohamad Dzomir, A.Z. and Yaakop, S. (2019) Effect of irradiating puparia of oriental fruit fly (Diptera: Tephritidae) on adult survival and fecundity for sterile insect technique and quarantine purposes. Journal of Economic Entomology, 112, 2808-2816.

[81]

Zhang, W. Chang, X.-Q. Hoffmann, A. Zhang, S. and Ma, C.-S. (2015) Impact of hot events at different developmental stages of a moth: the closer to adult stage, the less reproductive output. Scientific Reports, 5, 10436.

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