Body mass; Cotesia; development time; fitness; Gelis; host; Pieris; Insect Science; Ecology
Abstract :
[en] 1. The optimisation theory predicts that insect mothers should oviposit on resources on which they attain the highest exclusive fitness. The development of parasitoid wasps is dependent on limited host resources that are often not much larger than the adult parasitoid. 2. In the present study preference and development in three congeneric species of secondary hyperparasitoids attacking cocoons of two congeneric primary parasitoids that differ significantly in size were compared. Gelis agilis (Fabricius) and G. acarorum (L.) are wingless hyperparasitoids that forage in grassy habitats, whereas G. areator (Panzer) is fully winged and forages higher in the canopy of forbs. 3. The three species were reared on cocoons containing pupae of a small gregarious endoparasitoid, Cotesia glomerata (L.), and a larger solitary species, C. rubecula (Marshall), both of which develop in the caterpillars of pierid butterflies. 4. Adult mass was correlated with initial cocoon mass in all three species, whereas development time was unaffected. Wasps were larger when developing in C. rubecula. However, for a given host mass, wasps were larger when developing on the smaller host, C. glomerata. This suggests that there is a physiological limit to hyperparasitoid size that was exceeded when C. rubecula served as host. 5. All three hyperparasitoids strongly preferred to attack cocoons of the larger species, C. rubecula, often avoiding cocoons of C. glomerata entirely. 6. Preference and performance are correlated in the three Gelis species. However, owing to variation in the distribution and thus abundance of their hosts, it is argued that cumulative fitness may be still higher in the smaller host species.
Disciplines :
Zoology
Author, co-author :
Harvey, Jeffrey A.; Section Animal Ecology, Department of Ecological Sciences, VU University Amsterdam, Amsterdam
Rieta Gols; Laboratory of Entomology, Wageningen University, Wageningen, the Netherlands
Helen Snaas; Department of Terrestrial Ecology, Netherlands Institute of Ecology, Wageningen, the Netherlands
Visser, Bertanne ; Université de Liège - ULiège > Département GxABT > Gestion durable des bio-agresseurs
Language :
English
Title :
Host preference and offspring performance are linked in three congeneric hyperparasitoid species
Agosta, S.J. & Klemens, J.A. (2009) Resource specialization in a phytophagous insect: no evidence for genetically-based performance trade-offs across hosts in the field or laboratory. Journal of Evolutionary Biology, 22, 907-912.
van Alphen, J.J.M. & Drijver, R.A.B. (1982) Host selection by Asobara rabida Nees (Braconidae; Alysiinae), a larval parasitoid of fruit-inhabiting Drosophila species. I. Host stage selection with Drosophila melanogaster as host species. Netherlands Journal of Zoology, 32, 215-231.
van Alphen, J.J. & Visser, M.E. (1990) Superparasitism as an adaptive strategy for insect parasitoids. Annual review of entomology, 35, 59-79.
Arthur, A.P. & Wylie, H.G. (1959) Effects of host size on sex ratio, development time and size of Pimpla turionellae (L.)( Hymenoptera: Ichneumonidae). Biocontrol, 4, 297-301.
Askew, R.R., & Shaw, M.R. (1986) Parasitoid communities: their size, structure and development. Insect Parasitoids (ed. by J Waage & D. Greathead ), pp. 225-264. Academic Press, London, U.K.
Boivin, G. (2012) Sperm as a limiting factor in mating success in Hymenoptera parasitoids. Entomologia Experimentalis et Applicata, 146, 149-155.
Brodeur, J., Geervliet, J.B.F. & Vet, L.E.M. (1998) Effects of Pieris host species on life history parameters in a solitary specialist and gregarious generalist parasitoid (Cotesia species). Entomologia Experimentalis et Applicata, 86, 145-152.
Charnov, E.L. (1982) The Theory of Sex Allocation. Princeton University Press, Princeton, New Jersey.
Chau, A. & Mackauer, M. (2001a) Host-instar selection in the aphid parasitoid Monoctonus paulensis (Hymenoptera: Braconidae, Aphidiinae): assessing costs and benefits. Canadian Entomologist, 133, 549-564.
Chau, A. & Mackauer, M. (2001b) Preference of the aphid parasitoid Monoctonus paulensis (Hymenoptera: Braconidae, Aphidiinae) for different aphid species: female choice and offspring survival. Biological Control, 20, 30-38.
Cobb, L.M. & Cobb, V.A. (2004) Occurrence of parasitoid wasps, Baeus sp and Gelis sp., in the egg sacs of the wolf spiders Pardosa moesta and Pardosa sternalis (Araneae, Lycosidae) in southeastern Idaho. Canadian Field Naturalist, 118, 122-123.
Craig, T.P., Price, P.W. & Itami, J.K. (1986) Resource regulation by a stem-galling sawfly, on the arroyo willow. Ecology, 67, 419-425.
Eben, A., Benrey, B., Sivinski, J. & Aluja, M. (2000) Host species and host plant effects on preference and performance of Diachasmimorpha longicauda (Hymenoptera: Braconidae). Environmental Entomology, 29, 87-94.
Fidgen, J.G., Eldon, S.E. & Quiring, D.T. (2000) Influence of host size on oviposition, behaviour and fitness of Elachertus cacoeciae attacking a low-density population of spruce budworm Choristoneura fumiferana larvae. Ecological Entomology, 25, 156-164.
Flanders, S.E. (1947) Elements of host discovery exemplified by the parasitic Hymenoptera. Ecology, 28, 299-309.
García-Robledo, C. & Horvitz, C.C. (2012) Parent-offspring conflicts, "optimal bad motherhood" and the "mother knows best" principles in insect herbivores colonizing novel host plants. Ecology and Evolution, 2, 1446-1457.
Godfray, H.C.J. (1994) Parasitoids: Behavioral and Evolutionary Ecology. Princeton University Press, Princeton, New Jersey.
Gols, R., van Dam, N.M., Raaijmakers, C.E., Dicke, M. & Harvey, J.A. (2009) Are population differences in plant quality reflected in the preference and performance of two endoparasitoid wasps? Oikos, 118, 733-742.
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, 1-13.
Harvey, J.A. (2008) Comparing and contrasting development and reproductive strategies in the pupal hyperparasitoids Lysibia nana and Gelis agilis. Evolutionary Ecology, 22, 153-166.
Harvey, J.A., Jervis, M.A., Gols, R., Jiang, N. & Vet, L.E.M. (1999) Development of the parasitoid, Cotesia rubecula (Hymenoptera: Braconidae) in Pieris rapae and Pieris brassicae (Lepidoptera: Pieridae): evidence for host regulation. Journal of Insect Physiology, 145, 173-182.
Harvey, J.A., Bezemer, T.M., Elzinga, J.A. & Strand, M.R. (2004) Development of the solitary endoparasitoid Microplitis demolitor: host quality does not increase with host age and size. Ecological Entomology, 29, 35-43.
Harvey, J.A., Vet, L.E.M., Witjes, L.M.A. & Bezemer, T.M. (2006) Remarkable similarity in body mass of a secondary hyperparasitoid Lysibia nana and its primary parasitoid host Cotesia glomerata emerging from cocoons of comparable size. Archives of Insect Biochemistry and Physiology, 61, 170-183.
Harvey, J.A., Wagenaar, R. & Gols, R. (2011) Differing host exploitation efficiencies in two hyperparasitoids: when is a 'match made in heaven'? Journal of Insect Behavior, 24, 282-292.
Harvey, J.A., Snaas, H., Malcicka, M., Visser, B. & Bezemer, T.M. (2014) Small-scale spatial resource partitioning in a hyperparasitoid community. Arthropod-Plant Interactions, 8, 393-401.
Heaversedge, R.C. (1967) Variation in the size of insect parasites of puparia of Glossina spp. Bulletin of Entomological Research, 58, 153-158.
Henry, L.M., Gillespie, D.R. & Roitberg, B.D. (2005) Does mother really know best? Oviposition preference reduces reproductive performance in the generalist parasitoid Aphidius ervi. Entomologia Experimentalis et Applicata, 116, 167-174.
Hopper, K.R. (1986) Preference, acceptance, and fitness components of Microplitis croceipes (Hymenoptera: Braconidae) attacking various instars of Heliothis virescens (Lepidoptera: Noctuidae). Environmental Entomology, 15, 274-280.
Jervis, M.A. & Kidd, N.A.C. (1986) Host-feeding strategies in hymenopteran parasitoids. Biological Reviews, 61, 395-434.
Jervis, M.A., Heimpel, G.E., Ferns, P.N., Harvey, J.A. & Kidd, N.A.C. (2001) Life-history strategies in parasitoid wasps: a comparative analysis of "ovigeny". Journal of Animal Ecology, 70, 442-458.
Jervis, M.A., Ellers, J. & Harvey, J.A. (2008) Resource acquisition, allocation and utilization in parasitoid reproductive strategies. Annual Review of Entomology, 52, 361-365.
King, B.H. (1989) Host-size dependent sex ratios among parasitoid wasps: does host size matter? Oecologia, 78, 420-426.
Kivan, M. & Kilic, N. (2002) Host preference: parasitism, emergence and development of Trissolcus semistriatus (Hym., Scelonidae) in various host eggs. Journal of Applied Entomology, 126, 395-399.
Luhring, K.A., Millar, J.G., Paine, T.D., Reed, D. & Christiansen, H. (2004) Ovipositional preferences and progeny development of the egg parasitoid Avetianella longoi: factors mediating replacement of one species by a congener in a shared habitat. Biological Control, 30, 382-391.
Mackauer, M. & Sequeira, R. (1993) Patterns of development in insect parasites. Parasites and Pathogens of Insects (ed. by N. E. Beckage, S. N. Thompson & B. A. Federici ), pp. 1-20. Academic Press, New York, New York.
Mayhew, P.J. (2001) Herbivore host choice and optimal bad motherhood. Trends in Ecology & Evolution, 16, 165-167.
Mayhew, P.J. & Blackburn, T.M. (1999) Does development mode organize life-history traits in the parasitoid Hymenoptera? Journal of Animal Ecology, 68, 906-916.
Moratorio, M.S. (1987) Effect of host species on the parasitoids Anagrus mutans and Anagrus silwoodensis Walker (Hymenoptera: Mymaridae). Environmental Entomology, 16, 825-827.
Nechols, J.R. & Kikuchi, R.S. (1985) Host selection of the spherical mealybug (Homoptera: Pseudococcidae) by Anagyrus indicus (Hymenoptera: Encyrtidae): influence of host stage on parasitoid oviposition, development, sex ratio, and survival. Environmental Entomology, 14, 32-37.
van Nouhuys, S. & Hanski, I. (2000) Apparent competition between parasitoids mediated by a shared hyperparasitoid. Ecology Letters, 3, 82-84.
van Nouhuys, S., Reudler-Talsma, J., Biere, A. & Harvey, J.A. (2012) Performance of secondary parasitoids on chemically defended and undefended hosts. Basic & Applied Ecology, 13, 241-249.
Ode, P.J. (2006) Plant chemistry and natural enemy fitness: effects on herbivore and natural enemy interactions. Annual Review of Entomology, 51, 163-185.
Otto, M. & Mackauer, M. (1998) The developmental strategy of an idiobiont ectoparasitoid, Dendrocerus carpenteri: influence of variations in host quality on offspring growth and fitness. Oecologia, 117, 353-364.
Poelman, E.H. (2008) Linking variation in plant defence to biodiversity at higher trophic levels: a multidisciplinary approach. Unpublished PhD thesis, Wageningen University, Wageningen, the Netherlands.
Reznik, S.Y., Chernoguz, D.G. & Zinovjeva, K.B. (1992) Host searching, oviposition preferences and optimal synchronization in Alysia manducator (Hymenoptera: Braconidae), a parasitoid of the blowfly, Calliphora vicina. Oikos, 65, 81-88.
Roff, D.A. (1992) The Evolution of Life Histories: Theory and Analysis. Chapman and Hall, New York, New York.
Ruberson, J.R. & Kring, T.J. (1993) Parasitism of developing eggs by Trichogramma pretiosum (Hymenoptera: Trichogrammatidae): host age preference and suitability. Biological Control, 3, 39-46.
Salt, G. (1940) The effects of hosts upon their insect parasites. Biological Reviews, 16, 239-336.
Sandlan, K.P. (1982) Host suitability and its effects on parasitoid biology in Coccygomimus turionellae (Hymenoptera: Ichneumonidae). Annals of the Entomological Society of America, 75, 217-221.
Scheirs, J., De Bruyn, L. & Verhagen, R. (2000) Optimization of adult performance determines host choice in a grass miner. Proceedings of the Royal Society B, 267, 2065-2069.
Schwarz, M. & Shaw, M.R. (1999) Western Palaearctic Cryptinae (Hymenoptera: Ichneumonidae) in the National Museums of Scotland, with nomenclatural changes, taxonomic notes, rearing records and special reference to the British check list. Part 2. Genus Gelis Thunberg (Phygadeuontini: Gelina). Entomologist's Gazette, 50, 117-142.
Stevens, P.S. (1995) Host preferences of Trichogrammatoidea bactrae fumata (Hym.: Trichogrammatidae) an egg parasitoid of leafrollers (Lep.: Tortricidae). Biocontrol, 40, 379-385.
Sullivan, D.J. & Völkl, W. (1999) Hyperparasitism: multitrophic ecology and behavior. Annual Review of Entomology, 44, 291-315.
Ueno, T. (1997) Host age preference and sex allocation in the pupal parasitoid Itoplectis naranyae (Hymenoptera: Ichneumonidae). Annals of the Entomological Society of America, 90, 640-645.
Videla, M., Valladares, G. & Salvo, A. (2006) A tritrophic analysis of host preference and performance in a polyphagous leafminer. Entomologia Experimentalis et Applicata, 121, 105-114.
Visser, B., Le Lann, C., Snaas, H., Hardy, I.C.W. & Harvey, J.A. (2014) Consequences of resource competition for sex allocation and discriminative behaviors in a hyperparasitoid wasp. Behavioral Ecology and Sociobiology, 68, 105-113.
Wang, X.G. & Liu, S.S. (2002) Effects of host age on the performance of Diadromus collaris, a pupal parasitoid of Plutella xylostella. Biocontrol, 47, 293-307.
Weseloh, R.M. (1978) Seasonal and spatial mortality patterns of Apanteles melanoscelus due to predators and Gypsy moth hyperparasitoids. Environmental Entomology, 7, 662-665.
Wieber, A.M., Cook, S.P., Webb, R.E., Tatman, K.M. & Reardon, R.C. (1995) Niche partitioning by four Gelis spp. (Hymenoptera: Ichneumonidae) hyperparastioids of the primary Gypsy moth parasitoid Cotesia melanoscela (Hymenoptera: Braconidae). Annals of the Entomological Society of America, 88, 427-433.
Wieber, A.M., Webb, R.E., Reardon, R.C. & Tatman, K.M. (2001) Characterization of the hyperparasitoidcomplex of Cotesia melanoscelus (Hymenoptera: Braconidae) at three Maryland locations. Entomological News, 112, 241-254.
Zhao, H.Y., Zeng, L., Xu, Y.J., Lu, Y.Y. & Liang, G.W. (2013) Effects of host age on the parasitism of Pachycrepoideus vindemmiae (Hymenoptera:Pteromalidae), an ectoparasitic pupal parasitoid of Bactrocera cucurbitae (Diptera: Tephritidae). Florida Entomologist, 96, 451-457.