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Slow and fast development in two aphidophagous ladybirds on scarce and abundant prey supply

Published online by Cambridge University Press:  22 February 2016

N. Singh ,
G. Mishra  and
Omkar
N. Singh
Affiliation:
Ladybird Research Laboratory, Department of Zoology, University of Lucknow, Lucknow-226007, India
G. Mishra
Affiliation:
Ladybird Research Laboratory, Department of Zoology, University of Lucknow, Lucknow-226007, India
Omkar*
Affiliation:
Ladybird Research Laboratory, Department of Zoology, University of Lucknow, Lucknow-226007, India
*
*Author for correspondence Fax: +91-522-2740462 Phone: +91-9415757747 E-mail: [email protected]
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Abstract

Developmental rates are highly variable, both within and between genotypes and populations. But the rationale for two differential (slow and fast) developmental rates within same cohort under varying prey supply has yet not been explored. For this purpose, we investigated the effect of scarce and abundant prey supply on slow and fast development at 27°C in two aphidophagous ladybirds, Menochilus sexmaculatus (Fabricius) and Propylea dissecta (Mulsant) and its effect on their body mass and reproductive attributes. The ladybirds were provided with scarce and abundant supply of Aphis craccivora Koch under standardized abiotic conditions in the laboratory. A clear bimodal (two peaks, where the first peak represented the fast developing individuals and the second peak slow developing individuals) pattern of distribution for both prey supplies was obtained, which got skewed with change in prey supply. On abundant prey supply, more fast developing individuals (139 M. sexmaculatus and 123 P. dissecta) were found and less (46 M. sexmaculatus and 36 P. dissecta) on scarce prey supply. Slow developing individuals had female biased sex ratio, higher longevity and lower body mass. Fast developing females laid higher number of eggs with higher egg viability. Results of the study are indicative of occurrence and constancy of the slow and fast developing individuals in the egg batch.

Keywords

coccinellidaedevelopmental durationMenochilus sexmaculatusprey quantityPropylea dissectaslow:fast emergence
Type
Research Papers
Information
Bulletin of Entomological Research , Volume 106 , Issue 3 , June 2016 , pp. 347 - 358
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Copyright
Copyright © Cambridge University Press 2016 

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References

Agarwala, B.K., Bardhanroy, P., Yasuda, H. & Takizawa, T. (2001) Prey consumption and oviposition of the aphidophagous predator Menochilus sexmaculatus (Coleoptera: Coccinellidae) in relation to prey density and adult size. Environmental Entomology 30, 1182–1187.Google Scholar
Agarwala, B.K., Singh, T.K., Lokeshwari, R.K. & Sharmila, M. (2009) Functional response and reproductive attributes of the aphidophagous ladybird beetle, Harmonia dimidiata (F.) in oak trees of sericultural importance. Journal of Asia-Pacific Entomology 12, 179–182.CrossRefGoogle Scholar
Atlıhan, R. & Guldal, H. (2009) Prey density-dependent feeding activity and life history of Scymnus subvillosus. Phytoparasitica 37, 35–41.Google Scholar
Avila, F.W., Sirot, L.K., LaFlamme, B.A., Rubinstein, C.D. & Wolfner, M.F. (2011) Insect seminal fluid proteins: identification and function. Annual Review of Entomology 56, 21–40.Google Scholar
Beldade, P., Mateus, R.A. & Keller, R.A. (2011) Evolution and molecular mechanisms of adaptive developmental plasticity. Molecular Ecology 20, 1347–1363.CrossRefGoogle ScholarPubMed
Benelli, M., Leather, S.R., Francati, S., Marchetti, E. & Dindo, M.L. (2015) Effect of two temperatures on biological traits and susceptibility to a pyrethroid insecticide in an exotic and native coccinellid species. Bulletin of Insectology 68, 23–29.Google Scholar
Bergland, A.O., Genissel, A., Nuzhdin, S.V. & Tatar, M. (2008) Quantitative trait loci affecting phenotypic plasticity and the allometric relationship of ovariole number and thorax length in Drosophila melanogaster. Genetics 180, 567–582.Google Scholar
Bielby, J., Mace, G.M., Bininda-Emonds, O.R.P., Cardillo, M., Gittleman, J.L. & Jones, K.E. (2007) The fast-slow continuum in mammalian life history: an empirical re-evaluation. American Naturalist 169, 748–775.Google Scholar
Charnov, E.L. & Ernest, S.K.M. (2006) The offspring-size/clutchsize trade-off in mammals. American Naturalist 167, 578–582.Google Scholar
Chown, S.L. & Gaston, K.J. (2010) Body size variation in insects: a macroecological perspective. Biological Review 85, 139–169.Google Scholar
Cope, J.M. & Fox, C.W. (2003) Oviposition decisions in the seed beetle Callosobruchus maculatus (Coleoptera: Bruchidae): effects of seed size on superparasitism. Journal of Stored Products Research 39, 355–365.Google Scholar
D'Amico, L.J., Davidowitz, G. & Nijhout, H.F. (2001) The developmental and physiological basis of body size evolution in an insect. Proceedings of the Royal Society of London B: Biological Sciences 268, 1589–1593.Google Scholar
Darwin, C. (1874) The Descent of Man and Selection in Relation to Sex. 2nd edn.New York, Appleton.Google Scholar
Davidowitz, G. (2008) Population and environmental effects on the size-fecundity relationship in a common grasshopper across an aridity gradient. Journal of Orthoptera Research 17(2), 265–271.Google Scholar
Davidowitz, G. & Nijhout, H.F. (2004) The physiological basis of reaction norms: the interaction among growth rate, the duration of growth and body size. Integrative and Comparative Biology 44, 443–449.Google Scholar
Dixon, A.F.G. (2000) Insect Predator-Prey Dynamics: Ladybird Beetles and Biological Control. Cambridge, UK, Cambridge University Press, pp. 257.Google Scholar
Dixon, A.F.G., Sato, S. & Kindlmann, P. (2015) Evolution of slow and fast development in predatory ladybirds. Journal of Applied Entomology 140, 103–114.CrossRefGoogle Scholar
Dmitriew, C. & Rowe, L. (2011) The effects of larval nutrition on reproductive performance in a food limited adult environment. PLoS ONE 6(3), e17399. Doi:10.1371/journal.pone.0017399Google Scholar
Fox, C.W. & Czesak, M.E. (2000) Evolutionary ecology of progeny size in arthropods. Annual Review of Entomology 45, 341–369.Google Scholar
Garcia-Barros, E. (2000) Body size, egg size, and their inter-specific relationships with ecological and life history traits in butterflies (Lepidoptera: Papilionoidae, Hesperiodea). Biological Journal of the Linnaean Society 70, 251–284.Google Scholar
Gouws, E.J., Gaston, K.J. & Chown, S.L. (2011) Intraspecific body size frequency distributions of insects. PloS ONE 6(3), e16606.Google Scholar
Greer, E.L., Maures, T.J., Ucar, D., Hauswirth, A.G., Mancini, E., Lim, J.P., Benayoun, B.A., Shi, Y. & Brunet, A. (2011) Transgenerational epigenetic inheritance of longevity in Caenorhabditis elegans. Nature 479, 365–371.CrossRefGoogle ScholarPubMed
Gross, M.R. (1985) Disruptive selection for alternative life histories in salmon. Nature 313, 47–48.CrossRefGoogle Scholar
Hanski, I. (1988) Four kinds of extra long diapause: a review of theory and observations. Annales Entomologici Fennici 25, 37–53.Google Scholar
Helinski, M.E.H. & Harrington, L.C. (2011) Male mating history and body size influence female fecundity and longevity of the dengue vector Aedes aegypti. Journal of Medical Entomology 48(2), 202–211.Google Scholar
Hiyama, A., Taira, W. & Otaki, J.M. (2012) Color-pattern evolution in response to environmental stress in butterflies. Frontiers in Genetics 3, 15.Google Scholar
Hodek, I., Van Emden, H.F. & Honek, A. (2012) Ecology and Behaviour of the Ladybird Beetles (Coccinellidae). UK, Wiley. pp. 4229.CrossRefGoogle Scholar
Hoffmann, A. & Parsons, P.A. (1989) An integrated approach to environmental stress tolerance and life-history variation: desiccation tolerance in Drosophila. Biological Journal of the Linnaean Society 37, 117–136.Google Scholar
Jalali, M., Mehrnejad, M. & Kontodimas, D. (2014) Temperature dependent development of the five psyllophagous ladybird predators of Agonoscena pistaciae (Hemiptera: Psyllidae). Annals of the Entomological Society of America 107, 445–452.Google Scholar
Jeschke, J.M. & Kokko, H. (2009) The roles of body size and phylogeny in fast and slow life histories. Evolutionary Ecology 23, 867–878.Google Scholar
Joschinski, J., Hovestadt, T., Krauss, J. (2015) Coping with shorter days: do phenology shifts constrain aphid fitness? PeerJ 3, e1103. https://dx.doi.org/10.7717/peerj.1103Google Scholar
Juliano, S.A. (1986) Resistance to desiccation and starvation of two species of Brachinus (Coleoptera: Carabidae) from southeastern Arizona. Canadian Journal of Zoology 64(1), 73–80.Google Scholar
Katvala, M. & Kaitala, A. (2001) Male choice for current female fecundity in a polyandrous egg-carrying bug. Animal Behaviour 62, 133–137.Google Scholar
Kawai, A. (1978) Sibling cannibalism in the first instar larvae of Harmonia axyridis Pallas (Coleoptera: Coccinellidae). Kontyû 46, 14–19.Google Scholar
Kuzawa, C.W. (2005) Fetal origins of developmental plasticity: are fetal cues reliable predictors of future nutritional environments? American Journal of Human Biology 17, 5–21.Google Scholar
Kuzawa, C.W. (2008) The developmental origins of adult health: intergenerational inertia in adaptation and disease. pp. 325–349in Trevathan, W.R., Smith, E.O. & McKenna, J.J. (Eds) Evolutionary Medicine and Health. New York, Oxford University Press.Google Scholar
Lee, J.H. & Kang, T.J. (2004) Functional response of Harmonia axyridis (Pallas) (Coleoptera: Coccinellidae) to Aphis gossypii Glover (Homoptera: Aphididae) in the laboratory. Biological Control 31, 306–331.Google Scholar
Lewis, Z., Brakefield, P.M. & Wedell, N. (2010) Speed or sperm: a potential trade-off between development and reproduction in the butterfly, Bicyclus anynana (Lepidoptera: Nymphalidae). European Journal of Entomology 107, 55–59.Google Scholar
Maleszka, R. (2008) Epigenetic integration of environmental and genomic signals in honey bees: the critical interplay of nutritional, brain and reproductive networks. Epigenetics 3, 188–192.Google Scholar
Marinkovic, D., Milosevic, M. & Milanovic, M. (1986) Enzyme activity and dynamics of Drosophila development. Genetica 70, 43–52.Google Scholar
Maurice, N. & Kumar, A. (2011) Effect of quantity and consumption of food on body weight and development of two species of ladybird beetles. Annals of Plant Protection Sciences 19(1), 59–62.Google Scholar
Mishra, G. & Omkar, (2012) Slow and fast development in ladybirds: occurrence, effects and significance. Web Ecology 12, 19–26.CrossRefGoogle Scholar
Moczek, A.P. (1998) Horn polyphenism in the beetle Onthophagus taurus: larval diet quality and plasticity in parental investment determine adult body size and male horn morphology. Behavioral Ecology 9, 636–641.Google Scholar
O'Brien, D.M., Boggs, C.L. & Fogel, M.L. (2005) The amino acids used in reproduction by butterflies: a comparative study of dietary sources using compound-specific stable isotope analysis. Physiological and Biochemical Zoology 78(5), 819–827.Google Scholar
Oli, M.K. (2004) The fast-slow continuum and mammalian life-history patterns: an empirical evaluation. Basic and Applied Ecology 5, 449–463.Google Scholar
Omkar, & Afaq, U. (2013) Evaluation of Darwin's fecundity advantage hypothesis in Parthenium beetle, Zygogramma bicolorata Pallister. Insect Science 20, 531–540.Google Scholar
Omkar, & Pervez, A. (2003) Influence of prey deprivation on biological attributes of pale morphs of the lady beetle Propylea dissecta (Mulsant). Insect Science and its Application 23(2), 143–148.Google Scholar
Omkar, , Sahu, J. & Kumar, G. (2010) Effect of prey quantity in a ladybird beetle, Anegleis cardoni (Weise) (Coleoptera: Coccinellidae). International Journal of Tropical Insect Science 30(1), 48–56.Google Scholar
Osawa, N. (1992) Sibling cannibalism in the ladybird beetle Harmonia axyridis Pallas: fitness consequences for mother and offspring. Researches on Population Ecology 34, 45–55.Google Scholar
Osawa, N. (2003). The influence of female oviposition strategy on sibling cannibalism in the ladybird beetle Harmonia axyridis (Coleoptera: Coccinellidae). European Journal of Entomology 100, 43–48.Google Scholar
Osawa, N. & Ohashi, K. (2008) Sympatric coexistence of sibling species Harmonia yedoensis and H. axyridis (Coleoptera: Coccinellidae) and the roles of maternal investment through egg and sibling cannibalism. European Journal of Entomology 105, 445–454.Google Scholar
Pandey, P., Mishra, G. & Omkar, (2013) Slow and fast development in Parthenium beetle and its effect on reproductive attributes. Journal of Asia-Pacific Entomology 16(4), 395–399.Google Scholar
Partridge, L. & Fowler, K. (1992) Direct and correlated responses to selection on at age reproduction in Drosophila melanogaster. Evolution 46, 76–91.Google Scholar
Phoofolo, M.W., Giles, K.L. & Elliott, N.C. (2008) Larval life history responses to food deprivation in three species of predatory lady beetles (Coleoptera: Coccinellidae). Environmental Entomology 37, 315–322.Google Scholar
Pigliucci, M. (2001) Phenotypic Plasticity: Beyond Nature and Nurture. Baltimore, MD, Johns Hopkins University Press.Google Scholar
R Development Core Team (2013) R: A Language and Environment for Statistical Computing. Vienna: R Foundation for Statistical Computing. ISBN 3-900051-07-0. Available on line at http://www.R-project.org/Google Scholar
Rath, S.S. (2010) Food utilization efficiency in Antheraea mylitta fed on Terminalia arjuna leaves. Academic Journal of Entomology 3(1), 23–28.Google Scholar
Reznik, SYa. & Vaghina, N.P. (2013) Effects of photoperiod and diet on diapause tendency, maturation and fecundity in Harmonia axyridis (Coleoptera: Coccinellidae). Journal of Applied Entomology 137, 452–461.Google Scholar
Rodriguez-Saona, C. & Miller, J.C. (1995) Life history traits in Hippodamia convergens. (Coleoptera: Coccinellidae) after selection for fast development. Biological Control 5, 389–396.Google Scholar
Roff, D.A. (2002) Life History Evolution. Sunderland, MA, Sinauer.Google Scholar
Santos-Cividanes, T.M., dos Anjos, A.C.R., Cividanes, F.J. & Dias, P.C. (2011) Effects of food deprivation on the development of Coleomegilla maculata (De Geer) (Coleoptera: Coccinellidae). Neotropical Entomology 40, 112–116.CrossRefGoogle Scholar
Schönrogge, K., Wardlaw, J.C., Thomas, J.A. & Elmes, G.W. (2000) Polymorphic growth rates in myrmecophilous insects. Proceedings of the Royal Society of London B: Biological Sciences 267, 771–777.Google Scholar
Schuder, I., Hommes, M. & Larink, O. (2004) The influence of temperature and food supply on the development of Adalia bipunctata (Coleoptera: Coccinellidae). European Journal of Entomology 101, 379–384.Google Scholar
Sentis, A., Hemptinne, J.L. & Brodeur, J. (2012) Using functional response modeling to investigate the effect of temperature on predator feeding rate and energetic efficiency. Oecologia 169, 1117–1125.Google Scholar
Service, P.M. (1987) Physiological mechanisms of increased stress resistance in Drosophila melanogaster selected for postponed senescence. Physiological Zoology 60, 321–326.CrossRefGoogle Scholar
Sevenster, J.G. & Van Alphen, J.J. (1993) A life history trade-off in Drosophila species and community structure in variable environments. Journal of Animal Ecology 62, 720–736.Google Scholar
Sibly, R.M. & Brown, J.H. (2007) Effects of body size and lifestyle on evolution of mammal life histories. Proceedings of the National Academy of Science of the United States of America 104, 17707–17712.CrossRefGoogle ScholarPubMed
Singh, N., Mishra, G. & Omkar, (2014) Does temperature modify slow and fast development in two aphidophagous ladybirds? Journal of Thermal Biology 39, 24–31.Google Scholar
Singh, N., Mishra, G. & Omkar, (2016) Effect of photoperiod on slow and fast developing individuals in aphidophagous ladybirds, Menochilus sexmaculatus and Propylea dissecta (Coleoptera: Coccinellidae). Insect Science 23, 117–133.Google Scholar
Skorping, A. (2007) Selecting for fast and slow maturing worms. Proceedings of the Royal Society of London B: Biological Sciences 22(274), 1465–1466.Google Scholar
Sloggett, J.J. & Lorenz, M.W. (2008) Egg composition and reproductive investment in aphidophagous ladybird beetles (Coccinellidae: Coccinellini): egg development and interspecific variation. Physiological Entomology 33, 200–208.Google Scholar
Sørensen, C.H., Toft, S. & Kristensen, T.N. (2013) Cold-acclimation increases the predatory efficiency of the aphidophagous coccinellid Adalia bipunctata. Biological Control 65, 87–94.Google Scholar
Stamp, N.E. (2001) Effects of prey quantity and quality on predatory wasp. Ecological Entomology 26, 292–301.Google Scholar
Stearns, S.C. (1992) The Evolution of Life Histories. Oxford, Oxford University Press.Google Scholar
Stern, D.L. (2010) Evolution, Development, and the Predictable Genome. Greenwood Village, Colorado, Roberts and Company Publishers.Google Scholar
Stillwell, R.C., Morse, G.E. & Fox, C.W. (2007) Geographic variation in body size and sexual size dimorphism of a seed-feeding beetle. American Naturalist 170, 358–369.Google Scholar
Stillwell, R.C., Blanckenhorn, W.U., Teder, T., Davidowitz, G. & Fox, C.W. (2010) Sex differences in phenotypic plasticity affect variation in sexual size dimorphism in insects: from physiology to evolution. Annual Review of Entomology 55, 227–245.Google Scholar
Tauber, C.A., Tauber, M.J. & Tauber, M.J. (1991) Egg size and taxon: their influence on survival and development of chrysopid hatchlings after food and water-deprivation. Canadian Journal of Zoology-Revue Canadienne De Zoologie 69, 2644–2650.Google Scholar
Walker, R., Gurven, M., Hill, K., Migliano, A., Chagnon, N. & De Souza, R. (2006). Growth rates and life histories in twenty-two small-scale societies. American Journal of Human Biology 18, 295–311.Google Scholar
Ware, R.L., Yguel, B. & Majerus, M.E.N. (2008) Effects of larval diet on female reproductive output of the European coccinellid. Adalia bipunctata and the invasive species Harmonia axyridis (Coleoptera: Coccinellidae). European Journal of Entomology 105, 437–443.Google Scholar
Witek, M., Sliwinska, E.B., Skorka, P., Nowicki, P., Settele, J. & Woyciechowski, M. (2006) Polymorphic growth in larvae of Maculinea butterflies, as an example of biennialism in myrmecophilous insects. Oecologia 148, 729–733.Google Scholar