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Reduced mobility but high survival: thermal tolerance and locomotor response of the specialist herbivore, Pareuchaetes insulata (Walker) (Lepidoptera: Erebidae), to low temperatures

Published online by Cambridge University Press:  15 December 2016

O.O. Uyi*
Affiliation:
Department of Animal and Environmental Biology, University of Benin, P.M.B. 1154, Benin City, Nigeria Department of Zoology and Entomology, Rhodes University, P.O. Box 94, Grahamstown 6140, South Africa
C. Zachariades
Affiliation:
ARC – Plant Protection Research Institute, Private Bag X6006, Hilton 3245, South Africa School of Life Sciences, University of KwaZulu-Natal, Private Bag X01, Scottsville 3209, South Africa
E. Marais
Affiliation:
Centre for Invasion Biology, Stellenbosch University, Private Bag X01, Matieland 7602, South Africa
M.P. Hill
Affiliation:
Department of Zoology and Entomology, Rhodes University, P.O. Box 94, Grahamstown 6140, South Africa
*
*Author for correspondence Phone: +234 80380 130 12 Fax: +234 052 602370 E-mail: [email protected]

Abstract

Disentangling the responses of insects to variations in their thermal environment is central to our understanding of the evolution of temperature-dependent performance in these species. Here, we report results of experiments examining the effects of high (upper lethal temperature = ULT) and low (lower lethal temperature = LLT) temperature and exposure time on the survival of larvae and adults of a multivoltine, nocturnal moth species, Pareuchaetes insulata, a biological control agent whose impact on an invasive weed, Chromolaena odorata has been variable in South Africa. The influence of temperature and acclimation on locomotion performance of the moth was also investigated. Temperature and duration of exposure significantly affected survival of both adults and larvae of P. insulata with more extreme temperatures and/or longer durations proving to be more lethal. Third instar larvae and adults are both freeze intolerant and had LT50 of −5.9 and −4.7°C, respectively, after a 2 h exposure. Although cold acclimation was beneficial to the nocturnal larvae, temperatures below 10°C significantly reduce their locomotion activities. The average daily minimum temperatures in the coldest months at three locations in South Africa are over 5°C lower than those of Fort Lauderdale, Florida, USA, where P. insulata was originally collected. Our results suggest that lethal high or low temperatures at short timescales are trivial in explaining the variable performance of P. insulata, but reduced locomotion at sub-lethal temperatures may be an important driver of the population dynamics of the biocontrol agent (especially in winter months) and may consequently explain the low population levels of the moth because of possible reduced feeding by larvae during night-time low temperatures.

Type
Research Papers
Copyright
Copyright © Cambridge University Press 2016 

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References

Angilletta, M.J. Jr (2009) Thermal Adaptation: A Theoretical and Empirical Synthesis. New York, USA, Oxford University Press.Google Scholar
Angilletta, M.J., Niewiarowski, P.H. & Navas, C.A. (2002) The evolution of thermal physiology in ectotherms. Journal of Thermal Biology 27, 249268.CrossRefGoogle Scholar
Bale, J.S., Masters, G.J., Hodkinson, I.D., Awmack, C., Bezemer, T.M., Brown, V.K., Butterfield, J., Buse, A., Coulson, J.C., Farrar, J., Good, J.E.G., Harrington, R., Hartley, S., Jones, T.H., Lindroth, R.L., Press, M.C., Symrnioudis, I., Watt, A.D. & Whittaker, J.B. (2002) Herbivory in global climate change research: direct effects of rising temperature on insect herbivores. Global Change Biology 8, 116.CrossRefGoogle Scholar
Boersma, M. & Elser, J.J. (2006) Too much of a good thing: on stoichiometrically balanced diets and maximal growth. Ecology 87, 13251330.Google Scholar
Boiteau, C. & Mackinley, P. (2012) Locomotor response of Folsomia candida (Collembola: Isotomidae) to cooling temperatures. Environmental Entomology 41, 917924.Google Scholar
Byrne, M.J., Currin, S. & Hill, M.P. (2002) The influence of climate on the establishment and success of the biological control agent, Gratiana spadicea, released on Solanum sisymbriifolium in South Africa. Biological Control 24, 128134.Google Scholar
Byrne, M.J., Coetzee, J., McConnachie, A.J., Parasram, W. & Hill, M.P. (2003) Predicting climate compatibility of biological control agents in their region of introduction. p. 2835 in Cullen, J.M., Briese, D.T., Kriticos, D.J., Londsdale, W.M., Morin, L. & Scott, J.K. (eds) Proceedings of the XI International Symposium on Biological Control of Weeds, 27 April–2 May, 2003, Canberra, Australia, CSIRO Entomology.Google Scholar
Chidawanyika, F. & Terblanche, J.S. (2011) Rapid thermal response and thermal tolerance in adult codling moth Cydia pomonella (Lepidoptera: Tortricidae). Journal of Insect Physiology 57, 108117.Google Scholar
Chown, S.L. & Nicholson, S.W. (2004) Insect Physiological Ecology: Mechanisms and Patterns. New York, USA, Oxford Press.Google Scholar
Chown, S.L. & Terblanche, J.S. (2007) Physiological diversity in insects: ecological and evolutionary contexts. Advances in Insect Physiology 33, 50152.CrossRefGoogle Scholar
Chown, S.L., Slabber, S., McGeoch, M.A., Janion, C. & Leinaas, H.P. (2007) Phenotypic plasticity mediates responses among invasive and indigenous arthropods. Proceedings of the Royal Society B274, 25312537.Google Scholar
Clissold, F.J., Sanson, G.D. & Read, J. (2006) The paradoxical effects of nutrient ratios and supply rates on outbreaking insect herbivore, the Australian plague locust. Journal of Animal Ecology 75, 10001013.Google Scholar
Clissold, F.J., Coggan, N. & Simpson, S.J. (2013) Insect herbivores can choose microclimates to achieve nutritional homeostasis. Journal of Experimental Biology 216, 20892096.Google Scholar
Cock, M.W.J. & Holloway, J.D. (1982) The history of, and prospects for the biological control of Chromolaena odorata (Compositae) by Pareuchaetes pseudoinsulata Rego Barros and allies (Lepidoptera, Arctiidae). Bulletin of Entomological Research 72, 193205.CrossRefGoogle Scholar
Coulson, S.J. & Bale, J.S. (1991) Effect of rapid cold hardening on reproduction and survival of the housefly Musca domestica . Journal of Insect Physiology 38, 421424.CrossRefGoogle Scholar
Deere, J.A. & Chown, S.L. (2006) Testing the beneficial acclimation hypothesis and its alternatives for locomotor performance. American Naturalist 168, 630644.Google Scholar
Denlinger, D.L. & Lee, R.E. (2010) Low Temperature Biology of Insects. New York, USA, Cambridge University Press.Google Scholar
Esterhuizen, N., Clusella-Trullas, S., van Daalen, C.E., Schoombie, R.E., Boardman, L. & Terblanche, J.S. (2014) Effects of within-generation thermal history on the flight performance of Ceratitis capitata: colder is better. Journal of Experimental Biology 217, 35453556.Google Scholar
Ferrer, A., Dorn, S. & Mazzi, D. (2013) Cross-generational effects of temperature on flight performance, and associated life-history traits in an insect. Journal of Evolutionary Biology 26, 23212330.Google Scholar
Ferrer, A., Mazzi, D. & Dorn, S. (2014) Stay cool, travel far: cold acclimated oriental fruit moth females have enhanced flight performance but lay fewer eggs. Entomologia Experimentalis et Applicata 151, 1118.CrossRefGoogle Scholar
Frazier, M.R., Harrison, J.F., Kirkton, S.D. & Roberts, S.P. (2008) Cold rearing improves cold-flight performance in Drosophila via changes in wing morphology. Journal of Experimental Biology 211, 21162122.CrossRefGoogle ScholarPubMed
Gautier, L. (1992) Taxonomy and distribution of a tropical weed, Chromolaena odorata (L.) R. King and H. Robinson. Candollea 47, 645662.Google Scholar
Hochachka, P.W. & Somero, G.N. (2002) Mechanisms and Processes in Physiological Evolution. New York, USA, Oxford University Press.Google Scholar
Hoffmann, A.A. & Watson, M. (1993) Geographical variation in the acclimation responses of Drosophila to temperature extremes. American Naturalist 142, S93S113.CrossRefGoogle ScholarPubMed
Hoffmann, A.A., Chown, S.L. & Clusella-Trullas, S. (2013) Upper thermal limits in terrestrial ectotherms: how constrained are they? Functional Ecology 27, 934949.Google Scholar
Hopper, K.R. & Roush, R.T. (1993) Mate finding, dispersal, number released, and the success of biological control introductions. Ecological Entomology 18, 321331.Google Scholar
Hough-Goldstein, J., Lake, E.C., Shropshire, K.J., Moore, R.A. & D'Amico, V. (2016) Laboratory and field-based temperature-dependent development of a monophagous weevil: implications for integrated weed management. Biological Control 92, 120127.CrossRefGoogle Scholar
Hughes, J., Hern, A. & Dorn, S. (2004) Pre-imaginal environment influences adult flight in Cydia molesta (Lepidoptera: Tortricidae). Environmental Entomology 33, 11551162.Google Scholar
Jensen, D., Overgaard, J. & Sørensen, J.G. (2007) The influence of developmental stage on cold shock resistance and ability to cold-hardening in Drosophila melanogaster . Journal of Insect Physiology 53, 179186.Google Scholar
Klok, C.J. & Chown, S.L. (2000) Lack of cold tolerance in a small, brachypterous sub-Antarctic fly, Apetaenus litoralis Eaton (Diptera: Tethinidae), from Marion Island. African Entomology 8, 305308.Google Scholar
Kluge, R.L. (1994) Ant predation and the establishment of Pareuchaetes pseudoinsulata Rego Barros (Lepidoptera: Arctiidae) for biological control of triffid weed, Chromolaena odorata (L.) King and Robinson, in South Africa. African Entomology 2, 7172.Google Scholar
Kluge, R.L. & Caldwell, P.M. (1993 a) Host specificity of Pareuchaetes insulata (Lep.: Arctiidae), a biological control agent for Chromolaena odorata (Compositae). Entomophaga 38, 451457.CrossRefGoogle Scholar
Kluge, R.L. & Caldwell, P.M. (1993 b) The biology and host specificity of Pareuchaetes aurata aurata (Lepidoptera: Arctiidae), a “new association” biological control agent for Chromolaena odorata (Compositae). Bulletin of Entomological Research 83, 8794.CrossRefGoogle Scholar
Lachenicht, M.W., Clusella-Trullas, S., Boardman, L., Le Roux, C. & Terblanche, J.S. (2010) Effects of acclimation temperature on thermal tolerance, locomotion performance and respiratory metabolism in Acheta domesticus L. (Orthoptera: Gryllidae). Journal of Insect Physiology 56, 822830.CrossRefGoogle ScholarPubMed
Li, H.B., Shi, L., Lu, M.X., Wang, J.J. & Du, Y.Z. (2011) Thermal tolerance of Frankliniella occidentalis: effects of temperature, exposure time, and gender. Journal of Thermal Biology 36, 437442.Google Scholar
Mahroof, R., Subramanyam, B., Therone, J.E. & Menon, A. (2003) Time-mortality relationships for Tribolium castaneum (Coleopteran: Tenebrionidae) lifestages exposed to elevated temperatures. Journal of Economic Entomology 96, 13451351.CrossRefGoogle Scholar
Marais, E., Terblanche, J.S. & Chown, S.L. (2009) Life stage-related differences in hardening and acclimation of thermal tolerance traits in the kelpfly, Paractora dreuxi (Diptera, Helcomyzidae). Journal of Insect Physiology 55, 336343.Google Scholar
Martin, T.L. & Huey, R.B. (2008) Why “suboptimal” is optimal: Jensen's inequality and ectotherm thermal preferences. American Naturalist 171, 102118.CrossRefGoogle ScholarPubMed
May, B. & Coetzee, J. (2013) Comparisons of the thermal physiology of water hyacinth biological control agents: predicting establishment and distribution pre- and post-release. Entomologia Experimentalis et Applicata 147, 241250.Google Scholar
McClay, A.S. (1996) Biological control in a cold climate: temperature responses and climatic adaptation of weed biocontrol agents. pp. 377383 in Moran, V.C. & Hoffmann, J.H. (eds) Proceedings of the IX International Symposium on Biological Control of Weeds, 19–26 January 1996, Stellenbosch, University of Cape Town.Google Scholar
McEvoy, P.B. and Coombs, E.M. (2001) Why things bite back: unintended consequences of biological control. pp 167197 in Follett, P.A. & Duan, J.J. (eds) Nontarget effects of Biological Control. Boston, Kluwer Academic Publishers.Google Scholar
Paterson, I.D. & Zachariades, C. (2013) ISSRs indicate that Chromolaena odorata invading southern Africa originates in Jamaica or Cuba. Biological Control 66, 132139.Google Scholar
Régnière, J., Powell, J., Bentz, B. & Nealis, V. (2012) Effects of temperature on development, survival and reproduction of insects: experimental design, data analysis and modeling. Journal of Insect Physiology 58, 634647.CrossRefGoogle ScholarPubMed
Sinclair, B.J., Terblanche, J.S., Scott, M.B., Blatch, G.L., Klok, C.J. & Chown, S.L. (2006) Environmental physiology of three species of Collembola at Cape Hallett, North Victoria Land, Antarctica. Journal of Insect Physiology 52, 2950.CrossRefGoogle Scholar
Strathie, L.W. & Zachariades, C. (2014) Unexpected spread and outbreaks of Pareuchaetes insulata, the defoliating moth on Chromolaena odorata, in northern KwaZulu-Natal. Plant Protection News 101, 1011.Google Scholar
Tamiru, A., Getu, E., Jembere, B. & Bruce, T. (2012) Effect of temperature and relative humidity of the development and fecundity of Chilo partellus (Swinhoe) (Lepidoptera: Crambidae). Bulletin of Entomological Research 102, 915.Google Scholar
Terblanche, J.S. (2013) Thermal relations. pp. 588621 in Chapman, R.F., Simpson, S.J. & Douglas, A.E. (eds) The Insects: Structure and Function. 5th edn. Cambridge, UK, Cambridge University Press.Google Scholar
Terblanche, J.S. (2014) Physiological performance of field-released insects. Current Opinion in Insect Science 5, 17.Google Scholar
Terblanche, J.S., Clusella-Trullas, S., Deere, J.A. & Chown, S.L. (2008) Thermal tolerance in a south-east African population of tsetse fly Glossina pallidipes (Diptera: Glossinidae): implications for forecasting climate change impacts. Journal of Insect Physiology 54, 114127.Google Scholar
Uyi, O.O. (2014) Aspects of the biology, thermal physiology and nutritional ecology of Pareuchaetes insulata (Walker) (Lepidoptera: Erebidae: Arctiinae), a specialist herbivore introduced into South Africa for the biological control of Chromolaena odorata (L.) King and Robinson (Asteraceae). Unpublished doctoral dissertation, Rhodes University, Grahamstown.Google Scholar
Uyi, O.O., Ekhator, F., Ikuenobe, C.E., Borokini, T.I., Aigbokhan, E.I., Egbon, I.N., Adebayo, A.R., Igbinosa, I.B., Okeke, C.O., Igbinosa, E.O. & Omokhua, A.G. (2014 a) Chromolaena odorata invasion in Nigeria: a case for coordinated biological control. Management of Biological Invasions 5, 377397.Google Scholar
Uyi, O.O., Zachariades, C. & Hill, M.P. (2014 b) The life history traits of the arctiine moth Pareuchaetes insulata, a biological control agent of Chromolaena odorata in South Africa. African Entomology 22, 611624.Google Scholar
Uyi, O.O., Zachariades, C., Hill, M.P. & Conlong, D. (2015) The nocturnal larvae of a specialist folivore perform better on Chromolaena odorata leaves from a shaded environment. Entomologia Experimentalis et Applicata 156, 187199.Google Scholar
Uyi, O.O., Zachariades, C., Hill, M.P. & McConnachie, A.J. (2016 a) Temperature-dependent performance of Pareuchaetes insulata, a biological control agent of Chromolaena odorata in South Africa. BioControl 61, 815825.Google Scholar
Uyi, O.O., Zachariades, C. & Hill, M.P. (2016 b) Nitrogen fertilization improves growth of Chromolaena odorata (Asteraceae) and the performance of the biological control agent, Pareuchaetes insulata (Erebidae). Biocontrol Science and Technology 26, 373385.Google Scholar
Watt, T., Duan, J.J., Tallamy, D.W., Hough-Goldstein, J., Ilvento, T.W., Yue, X. & Ren, H. (2016) Reproductive and developmental biology of the emerald ash borer parasitoid Spathius galinae (Hymenoptera: Braconidae) as affected by temperature. Biological Control 96, 17.Google Scholar
Weldon, C.W., Terblanche, J.S. & Chown, S.L. (2011) Time-course for attainment and reversal of acclimation to constant temperature in two Ceratitis species. Journal of Thermal Biology 36, 479485.Google Scholar
Wu, L., Wang, C. & Wu, W. (2013) Effects of temperature and adult nutrition on the development of Acanthoscelides macrophthalmus, a natural enemy of an invasive tree, Leucaena leucocephala . Biological Control 65, 322329.CrossRefGoogle Scholar
Yoder, J.A., Chambers, M.J., Tank, J.L. & Keeney, G.D. (2009) High temperature effects on water loss and survival examining the hardiness of female adults of the spider beetles, Mezium affine and Gibbium aequinoctiale . Journal of Insect Science 9, 68.Google Scholar
Zachariades, C., Strathie-Korrûbel, L.W. & Kluge, R.L. (1999) The South African programme on the biological control of Chromolaena odorata (L.) King & Robinson using insects. African Entomology Memoir 1, 89102.Google Scholar
Zachariades, C., Day, M., Muniappan, R. & Reddy, G.V.P. (2009) Chromolaena odorata (L.) King and Robinson (Asteraceae). pp. 130160 in Muniappan, R., Reddy, G.V.P. & Raman, A. (eds) Biological Control of Tropical Weeds Using Arthropods, Cambridge, Cambridge University Press.Google Scholar
Zachariades, C., Strathie, L.W., Retief, E. & Dube, N. (2011) Progress towards the biological control of Chromolaena odorata (L.) R.M. King and H. Rob. (Asteraceae) in South Africa. African Entomology 19, 282302.CrossRefGoogle Scholar
Zhao, L., Jia, D., Yuan, X., Guo, Y., Zhou, W. and Ma, R. (2015) Cold hardiness of the biological control agent, Agasicles hygrophila, and implications for its potential distribution. Biological Control 87, 15.Google Scholar