Hostname: page-component-cd9895bd7-gxg78 Total loading time: 0 Render date: 2024-12-22T18:26:42.407Z Has data issue: false hasContentIssue false

Cornicle secretions by Aphis fabae (Hemiptera: Aphididae) result in age-dependent costs and improved host suitability for Lysiphlebus fabarum (Marshall) (Hymenoptera: Braconidae)

Published online by Cambridge University Press:  04 December 2017

Y. Parvizi
Affiliation:
Department of Plant Protection, College of Agriculture, Shahid Chamran University of Ahvaz, Ahvaz, Iran
A. Rasekh*
Affiliation:
Department of Plant Protection, College of Agriculture, Shahid Chamran University of Ahvaz, Ahvaz, Iran
J.P. Michaud
Affiliation:
Department of Entomology, Agricultural Research Center-Hays, Kansas State University, 1232 240th Ave, Hays, KS 67601, USA
*
*Author for correspondence Phone: +98 91 2660 3166 Fax: +98 61 3333 0079 E-mail: [email protected]

Abstract

We examined the life history consequences of cornicle secretion by Aphis fabae Scopoli in second and fourth instars, and its effects on host suitability for its parasitoid, Lysiphlebus fabarum (Marshall). Cornicle secretion did not affect aphid fecundity, but secretion in the second instar enhanced life table parameters, whereas secretion in the fourth instar affected them negatively, suggesting a higher cost of secretion in later instars. Secretion in either instar improved host suitability for L. fabarum. Although control and treated aphids were parasitized at similar rates, and with similar success, wasps developed faster and emerged as larger adults in aphids that had secreted, regardless of instar. Transgenerational effects were also evident. Progeny emergence was higher when parental wasps developed in fourth instars than in seconds, whether aphids secreted or not, and progeny were larger when parental hosts secreted in the second instar, but not in the fourth. Secreting fourth instars were preferred to controls by L. fabarum females in choice tests, but not secreting second instars, and fourth-instar secretion improved wasp emergence. When control aphids were attacked, second instars were more likely to secrete than fourth instars, whereas the latter were more likely to kick the parasitoid. Cornicle secretion reduced the probability of subsequent secretion events and the frequency of other aphid defensive behaviors, indicating energetic tradeoffs among defensive tactics. Overall, our results revealed that cornicle secretion by immature A. fabae exacts both physiological and behavioral costs and results in improved host suitability for its parasitoid.

Type
Research Papers
Copyright
Copyright © Cambridge University Press 2017 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Acar, E.B., Medina, J.C., Lee, M.L. & Booth, G.M. (2001) Olfactory behavior of convergent lady beetles (Coleoptera: Coccinellidae) to alarm pheromone of green peach aphid (Hemiptera: Aphididae). Canadian Entomologist 133, 389397.Google Scholar
Alfaress, S., Hijaz, F. & Killiny, N. (2016) Chemical composition of cornicle secretion of the brown citrus aphid Toxoptera citricida. Physiological Entomology 41, 48–37.Google Scholar
Ameri, M., Rasekh, A. & Michaud, J.P. (2014) Body size affects host defensive behavior and progeny fitness in a parasitoid wasp, Lysiphlebus fabarum. Entomologia Experimentalis et Applicata 150, 259268.Google Scholar
Barry, A. & Ohno, K. (2016) Cornicle secretions of Uroleucon nigrotuberculatum (Homoptera: Aphididae) as the last bullet against lady beetle larvae. Entomological Science 19, 410415.Google Scholar
Battaglia, D., Poppy, G., Powell, W., Romano, A., Tranfaglia, A. & Pennacchio, F. (2000) Physical and chemical cues influencing the oviposition behaviour of Aphidius ervi. Entomologia Experimentalis et Applicata 94, 219227.Google Scholar
Bayoumy, M.H., Ramaswamy, P. & Michaud, J.P. (2015) Comparative life histories of greenbugs and sugarcane aphids (Hemiptera: Aphididae) coinfesting susceptible and resistant sorghums. Journal of Economic Entomology 109, 385391.Google Scholar
Butler, C.D. & O'Neil, R.J. (2006) Defensive response of soybean aphid (Hemiptera: Aphididae) to predation by insidious flower bug (Hemiptera: Anthocoridae). Annals of the Entomological Society of America 99, 317320.Google Scholar
Callow, R.K., Greenway, A.R. & Griffiths, D.C. (1973) Chemistry of the secretion from the cornicles of various species of aphids. Journal of Insect Physiology 19, 737748.Google Scholar
Carey, J.R. (1993) Applied Demography for Biologists. New York, NY, Oxford University Press.Google Scholar
Carton, Y., Poirié, M. & Nappi, A.J. (2008) Insect immune resistance to parasitoids. Insect Science 15, 6787.Google Scholar
Charnov, E.L., Los-den Hartogh, R.L., Jones, W.T. & van den Assem, J. (1981) Sex ratio evolution in a variable environment. Nature 289, 2733.Google Scholar
Chau, A. & Mackauer, M. (1997) Dropping of pea aphids from feeding site, a consequence of parasitism by the wasp Monoctonus paulensis. Entomologia Experimentalis et Applicata 83, 247252.Google Scholar
Crawley, M.J. (1993) GLIM for Ecologists. Oxford, UK, Blackwell Scientific.Google Scholar
Dill, L.M., Fraser, A.H.D. & Roitberg, B.D. (1990) The economics of escape behaviour in the pea aphid, Acyrthosiphon pisum. Oecologia 83, 473478.Google Scholar
Eichele, J.L., Dreyer, J., Heinz, R., Foster, S.P., Prischmann-Voldseth, D.A. & Harmon, J.P. (2016) Soybean aphid response to their alarm pheromone e-beta-farnesene (EBF). Journal of Insect Behavior 29, 385394.Google Scholar
Godfray, H.C.J. (1994) Parasitoids: Behavioral and Evolutionary Ecology. Princeton, New Jersey, Princeton University Press.Google Scholar
Harvey, J.A. (2005) Factors affecting the evolution of development strategies in parasitoid wasps: the importance of functional constraints and incorporating complexity. Entomologia Experimentalis et Applicata 117, 113.Google Scholar
Ingerslew, K.S. & Finke, D.L. (2017) Mechanisms underlying the nonconsumptive effects of parasitoid wasps on aphids. Environmental Entomology 46, 7583.Google Scholar
Joachim, C., Hatano, E., David, A., Kunert, M., Linse, C. & Weisser, W.W. (2013) Modulation of aphid alarm pheromone emission of pea aphid prey by predators. Journal of Chemical Ecology 39, 773782.Google Scholar
Mackauer, M. (1983) Quantitative assessment of Aphidius smithi (Hymenoptera: Aphidiidae): fecundity, intrinsic rate of increase, and functional response. Canadian Entomologist 115, 399415.Google Scholar
Micha, S.G. & Wyss, U. (1996) Aphid alarm pheromone (E)-ß-farnesene: a host finding kairomone for the aphid primary parasitoid Aphidius uzbekistanicus (Hymenoptera: Aphidiinae). Chemoecology 7, 132139.Google Scholar
Moayeri, H.R.S., Mohandesi, A.R. & Ashouri, A. (2012) Fitness costs of cornicle secretions as a defense mechanism for cotton aphid, Aphis gossypii (Hem.: Aphididae). Journal of Entomological Society of Iran 31, 5161.Google Scholar
Moayeri, H.R.S., Rasekh, A. & Enkegaard, A. (2014) Influence of cornicle droplet secretions of the cabbage aphid, Brevicoryne brassicae, on parasitism behavior of naïve and experienced Diaeretiella rapae. Insect Science 21, 5664.Google Scholar
Mondor, E. & Roitberg, B. (2003) Aphid alarm signalling: direct effects on the emitter's development and reproduction. Canadian Journal of Zoology 81, 756762.Google Scholar
Mondor, E.B., Baird, D.S., Slessor, K.N. & Roitberg, B.D. (2000) Ontogeny of alarm pheromone secretion in pea aphid, Acyrthosiphon pisum. Journal of Chemical Ecology 26, 28752882.Google Scholar
Rakhshani, E., Talebi, A.A., Kavallieratos, N.G., Rezwani, A., Manzari, S. & Tomanović, Z. (2005) Parasitoid complex (Hymenoptera, Braconidae, Aphidiinae) of Aphis craccivora Koch (Hemiptera: Aphidoidea) in Iran. Journal of Pest Science 78, 193198.Google Scholar
Rasekh, A., Michaud, J.P., Kharazi-Pakdel, A. & Allahyari, H (2010 a) Ant mimicry by an aphid parasitoid, Lysiphlebus fabarum (Marshall) (Hymenoptera: Aphidiidae). Journal of Insect Science 10, 126.Google Scholar
Rasekh, A., Michaud, J.P., Allahyari, H. & Sabahi, Q. (2010 b). The foraging behavior of Lysiphlebus fabarum (Marshall) a thelytokous parasitoid of the black bean aphid in Iran. Journal of Insect behavior 23, 165179.Google Scholar
Rasekh, A., Kharazi-Pakdel, A., Michaud, J.P., Allahyari, H. & Rakhshani, E. (2011) Report of a thelytokous population of Lysiphlebus fabarum (Marshall) (Hymenoptera: Aphidiidae) from Iran. Journal of Entomological Society of Iran 30, 8384.Google Scholar
Salt, G. (1941) The effects of hosts upon their insect parasites. Biological Reviews 16, 239264.Google Scholar
Sequeira, R. & Mackauer, M. (1992) Nutritional ecology of an insect host-parasitoid association: the pea aphid-Aphidius ervi system. Ecology 73, 183189.Google Scholar
Shonouda, M.L., Bombosch, S., Shalaby, A.M. & Osman, S.I. (1998) Biological and chemical characterization of a kairomone excreted by the bean aphids, Aphis fabae Scop. (Hom., Aphididae) and its effect on the predator Metasyrphus corollae Fabr. I. Isolation, identification and bioassay of aphid-kairomone. Journal of Applied Entomology 122, 1523.Google Scholar
Slansky, F. Jr. (1986) Nutritional ecology of endoparasitic insects and their hosts: an overview. Journal of Insect Physiology 32, 255261.Google Scholar
Southwood, T.R.E. & Henderson, P.A. (2000) Ecological Methods. 3rd edn. Oxford, UK, Blackwell.Google Scholar
SPSS Inc. (1998) SPSS 8.0 for Windows. Prentice Hall, NJ, SPSS Inc.Google Scholar
Stary, P. (1986) Specificity of parasitoids (Hymenoptera: Aphidiidae) to the black bean aphid Aphis fabae complex in agrosystems. Acta Entomologica Bohemoslovaca 83, 2429.Google Scholar
Talebi, A.A., Rakhshani, E., Fathipour, Y., Starý, P. & Tomanović, Ž. (2009) Aphids and their parasitoids (Hym., Braconidae: Aphidiinae) associated with medicinal plants in Iran. American-Eurasian Journal of Sustainable Agriculture 3, 205219.Google Scholar
Verheggen, F.J., Arnaud, L., Bartram, S., Gohy, M. & Haubruge, E. (2008) Aphid and plant volatiles induce oviposition in an aphidophagous hoverfly. Journal of Chemical Ecology 34, 301307.Google Scholar
Villagra, C.A., Ramirez, C.C. & Niemeyer, H.M. (2002) Antipredator responses of aphids to parasitoids change as a function of aphid physiological state. Animal Behaviour 64, 677683.Google Scholar
Vinson, S.B. & Iwantsch, G. (1980) Host suitability for insect parasitoids. Annual Review of Entomology 25, 397419.Google Scholar
Völkl, W. (1992) Aphids or their parasitoids: who actually benefits from ant-attendance? Journal of Animal Ecology 61, 273281.Google Scholar
Völkl, W. & Mackauer, M. (2000) Oviposition behavior of Aphidiine wasps: morphological adaptations and evolutionary trends. Canadian Entomologist 132, 197212.Google Scholar
Weisser, W.W. (1994) Age-dependent foraging behaviour and host-instar preference of the aphid parasitoid Lysiphlebus cardui. Entomologia Experimentalis et Applicata 70, 110.Google Scholar