Hostname: page-component-586b7cd67f-t7czq Total loading time: 0 Render date: 2024-11-24T17:09:17.105Z Has data issue: false hasContentIssue false

Freezing cold yet diverse: dissecting a high-Arctic parasitoid community associated with Lepidoptera hosts

Published online by Cambridge University Press:  22 February 2013

Gergely Várkonyi*
Affiliation:
Finnish Environment Institute, Natural Environment Centre, Friendship Park Research Centre, Lentiirantie 342B, FI-88900 Kuhmo, Finland
Tomas Roslin
Affiliation:
Spatial Foodweb Ecology Group, Department of Agricultural Sciences, University of Helsinki, PO Box 27 (Latokartanonkaari 5), FI-00014 Helsinki, Finland
*
1Corresponding author (e-mail: [email protected]).

Abstract

Despite increasing worldwide interest in host–parasitoid food webs, the parasitoid communities of the high Arctic remain poorly explored. To allow analyses of global patterns, and to detect the effects of ongoing climate change, such data are urgently needed. In this paper, we describe a systematic effort to characterise the high-Arctic Hymenoptera and Diptera parasitoid community associated with Lepidoptera hosts of the Zackenberg Valley (74°30′N, 21°00′W), northeast Greenland. Here, we first sampled adult parasitoids by a combination of Malaise traps, pitfall traps, and, less extensively, yellow pan traps and sweep netting. We then identified the host use of individual parasitoid taxa by rearing a large number of host individuals and species across multiple years. We now describe our preliminary findings on the species diversity of the target community, on trophic links between hosts and parasitoids, and on the sampling effort and techniques needed to characterise the community. We report on 30 local parasitoid taxa representing four families, three of which are species new to Greenland. In describing the community, we make a specific effort to summarise what is known about the taxonomy, phenology, and host use of the component species, to the benefit of future research in the area.

Résumé

Malgré un intérêt croissant pour les réseaux trophiques hôte-parasitoïdes à travers le monde, les communautés de parasitoïdes du haut-Arctique restent peu étudiées. Pour permettre des analyses de patrons globaux et détecter les effets des changements climatiques en cours, nous avons pourtant un besoin urgent de telles données. Dans cet article, nous documentons un effort systématique visant à caractériser les communautés d'hyménoptères et de diptères parasitoïdes du haut-Arctique, associées à des lépidoptères hôtes, dans la vallée de Zackenberg (74°30′N, 21°00′W) au Nord-Est du Groenland. Dans un premier temps, nous avons échantillonné des parasitoïdes adultes par l'utilisation combinée de pièges Malaise, de pièges à fosse (ou pièges Barber) et, dans une moindre mesure, de pièges colorés (bacs jaunes) et de filets dit « à papillons ». Nous avons ensuite identifié l'utilisation des hôtes par les individus des taxons de parasitoïdes en élevant un grand nombre d'individus et d'espèces d'hôtes durant plusieurs années. Nous décrivons aujourd'hui nos résultats préliminaires sur la diversité spécifique de la communauté ciblée, sur les relations trophiques entre hôtes et parasitoïdes, et sur la complémentarité entre efforts et techniques d’échantillonnage. Nous avons documenté la présence de 30 taxons locaux de parasitoïdes représentant quatre familles, dont trois taxons sont des nouvelles espèces pour le Groenland. En décrivant la communauté, nous nous efforçons à résumer, pour chacune des espèces qui la composent, l’état des connaissances sur la taxonomie, la phénologie et l'utilisation des hôtes, pour le bénéfice de recherches ultérieures qui seraient conduites dans la région.

Type
Behaviour & Ecology
Copyright
Copyright © Entomological Society of Canada 2013

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

Allen, A.P., Brown, J.H., Gillooly, J.F. 2002. Global biodiversity, biochemical kinetics and the energetic-equivalence rule. Science, 297: 15451548.CrossRefGoogle ScholarPubMed
Arnaud, P.H. Jr. 1978. A host–parasite catalog of North American Tachinidae (Diptera). United States Department of Agriculture. Miscellaneous Publication, 1319: 1860.Google Scholar
Askew, R.R. 1971. Parasitic insects. Heinemann Educational Books, London, United Kingdom.Google Scholar
Askew, R.R. 1975. The organisation of chalcid-dominated parasitoid communities centred upon endophytic hosts. In Evolutionary strategies of parasitic insects and mites. Edited by P.W. Price. Plenum Press, New York, United States of America and London, United Kingdom. Pp. 130153.CrossRefGoogle Scholar
Askew, R.R.Shaw, M.R. 1986. Parasitoid communities: their size, structure and development. In Insect parasitoids – 13th Symposium of the Royal Entomological Society of London. Edited by J. Waage and D. Greathead. Academic Press, London, United Kingdom. Pp. 225–264.Google Scholar
Baur, H. 2005. A review of the Eulophidae and Pteromalidae (Hymenoptera: Chalcidoidea) of Greenland. Acta Societatis Zoologicae Bohemicae, 69: 2334.Google Scholar
Bay, C. 1998. Vegetation mapping of Zackenberg valley, Northeast Greenland. Danish Polar Centre and Botanical Museum, University of Copenhagen, Copenhagen, Denmark.Google Scholar
Begon, M., Townsend, C.R., Harper, J.L. 2006. Ecology: from individuals to ecosystems, 4th edition. Blackwell Publishing, Oxford, United Kingdom.Google Scholar
Belshaw, R. 1994. Life history characteristics of Tachinidae (Diptera) and their effect on polyphagy. In Parasitoid community ecology. Edited by B.A. Hawkins and W. Sheehan. Oxford University Press, Oxford, United Kingdom. Pp. 145162.CrossRefGoogle Scholar
Böcher, J.Meltofte, H. 1997. Comparison of three different types of arthropod traps. In Zackenberg Ecological Research Operations, 2nd Annual Report 1996. Edited by H. Meltofte and H. Thing. Danish Polar Center, Ministry of Research and Information Technology, Copenhagen, Denmark. Pp. 6667.Google Scholar
Brown, J.Lomolino, M. 1998. Biogeography, 2nd edition. Sinauer, Sunderland, Massachusetts, United States of America.Google Scholar
Buhl, P.N. 1997. Microhymenoptera from Zackenberg, north east Greenland (Hymenoptera: Chalcidoidea, Cynipoidea et Ceraphronoidea). Entomologiske Meddelelser, 65: 161164.Google Scholar
Burnham, K.P.Overton, W.S. 1978. Estimation of the size of a closed population when capture probabilities vary among animals. Biometrika, 65: 625633.CrossRefGoogle Scholar
Chao, A. 1984. Non-parametric estimation of the number of classes in a population. Scandinavian Journal of Statistics, 11: 265270.Google Scholar
Chao, A. 1987. Estimating the population size for capture–recapture data with unequal catchability. Biometrics, 43: 783791.CrossRefGoogle ScholarPubMed
Chao, A. 2005. Species estimation and applications. In Encyclopedia of statistical sciences. Edited by S. Kotz, N. Balakrishnan, C.B. Read, and B. Vidakovic. Wiley, New York, United States of America. Pp. 79077916.Google Scholar
Chao, A., Hwang, W.-H., Chen, Y.-C., Kuo, C.-Y. 2000. Estimating the number of shared species in two communities. Statistica Sinica, 10: 227246.Google Scholar
Chao, A.Jost, L. 2012. Coverage-based rarefaction and extrapolation: standardizing samples by completeness rather than by size. Ecology, 93: 25332547.CrossRefGoogle ScholarPubMed
Chao, A.Lee, S.-M. 1992. Estimating the number of classes via sample coverage. Journal of the American Statistical Association, 87: 210217.CrossRefGoogle Scholar
Chao, A.Ma, M.-C., Yang, M.C.K. 1993. Stopping rule and estimation for recapture debugging with unequal detection rates. Biometrika, 80: 193201.CrossRefGoogle Scholar
Chao, A.Shen, T.-J. 2010. Program SPADE (Species Prediction And Diversity Estimation) [online]. Available from http://chao.stat.nthu.edu.tw/softwareCE.html [accessed 22 December 2012].Google Scholar
Chao, A., Shen, T.-J., Hwang, W.H. 2006. Application of Laplace's boundary-mode approximations to estimate species and shared species richness. Australian and New Zealand Journal of Statistics, 48: 117128.CrossRefGoogle Scholar
Currie, D.J. 1991. Energy and large-scale patterns of animal and plant-species richness. The American Naturalist, 137: 2749.CrossRefGoogle Scholar
Dasch, C.E. 1971. Ichneumon-flies of America north of Mexico: 6. Subfamily Mesochorinae. Memoirs of the American Entomological Institute, 16: 1376.Google Scholar
Dasch, C.E. 1979. Ichneumon-flies of America north of Mexico: 8. Subfamily Cremastinae. Memoirs of the American Entomological Institute, 29: 1702.Google Scholar
Dasch, C.E. 1988. Ichneumon-flies of America north of Mexico: 10. Subfamily Banchinae, tribe Glyptini. Memoirs of the American Entomological Institute, 43: 1644.Google Scholar
DeBach, P. 1964. Biological control of insect pests and weeds. Chapman and Hall, London, United Kingdom.Google Scholar
Dindo, M.L. 2011. Tachinid parasitoids: are they to be considered as koinobionts? BioControl, 56: 249255.CrossRefGoogle Scholar
Fernández-Triana, J.L. 2010. Eight new species and an annotated checklist of Microgastrinae (Hymenoptera, Braconidae) from Canada and Alaska. ZooKeys, 63: 153.CrossRefGoogle Scholar
Fernández-Triana, J., Smith, M.A., Boudreault, C., Goulet, H., Hebert, P.D.N., Smith, A.C., et al. 2011. A poorly known high-latitude parasitoid wasp community: unexpected diversity and dramatic changes through time. PLoS One, 6: e23719 . doi:10.1371/journal.pone.0023719.CrossRefGoogle ScholarPubMed
Fraser, S.E.M., Dytham, C., Mayhew, P.J. 2008. The effectiveness and optimal use of Malaise traps for monitoring parasitoid wasps. Insect Conservation and Diversity, 1: 2231.CrossRefGoogle Scholar
Gauld, I.D. 1987. Some factors affecting the composition of tropical ichneumonid faunas. Biological Journal of the Linnean Society, 30: 299312.CrossRefGoogle Scholar
Gauld, I.D.Bolton, B. 1988. The Hymenoptera. First impression. British Museum (Natural History), London, United Kingdom.Google Scholar
Godfray, H.C.J. 1994. Parasitoids – behavioral and evolutionary ecology. Princeton University Press, Princeton, New Jersey, United States of America.CrossRefGoogle Scholar
Good, I.J. 1953. The population frequencies of species and the estimation of population parameters. Biometrika, 40: 237264.CrossRefGoogle Scholar
Gripenberg, S.Roslin, T. 2007. Up or down in space? Uniting the bottom-up versus top-down paradigm and spatial ecology. Oikos, 116: 181188.Google Scholar
Haeselbarth, E. 1979. Zur Parasitierung der Puppen von Forleule (Panolis flammea [Schiff.]), Kiefernspanner (Bupalus piniarius [L.]) und Heidelbeerspanner (Boarmia bistortana [Goeze]) in bayerischen Kiefernwäldern. Zeitschrift für Angewandte Entomologie, 87: 186202, 311–322.CrossRefGoogle Scholar
Hairston, N.G., Smith, F.E., Slobodkin, L.B. 1960. Community structure, population control, and competition. The American Naturalist, 94: 421425.CrossRefGoogle Scholar
Hassell, M.P. 2000. The spatial and temporal dynamics of host–parasitoid interactions. Oxford University Press, Oxford, United Kingdom.CrossRefGoogle Scholar
Hawkins, B.A. 1994. Pattern and process in host–parasitoid interactions. Cambridge University Press, Cambridge, United Kingdom.CrossRefGoogle Scholar
Hawkins, B.A., Askew, R.R., Shaw, M.R. 1990. Influences of host feeding-niche and foodplant type on generalist and specialist parasitoids. Ecological Entomology, 15: 275280.CrossRefGoogle Scholar
Hawkins, B.A.Sheehan, W. 1994. Parasitoid community ecology. Oxford University Press, Oxford, United Kingdom.CrossRefGoogle Scholar
Heinrich, G.H. 1961. Synopsis of Nearctic Ichneumoninae Stenopneusticae with particular reference to the northeastern region (Hymenoptera). Part II. The Canadian Entomologist, 92 (Suppl. 18), 89205.Google Scholar
Henriksen, K.L. 1939. A revised index of the insects of Grønland, containing a supplement to the insect list in Kai L. Henriksen & Will. Lundbeck: Grønlands Landarthropoder (Medd. om Grønl. Bd 22. 1917). Meddelelser om Grønland, 119: 1111.Google Scholar
Henriksen, K.L.Lundbeck, W. 1918. Landarthropoder (Insecta et Arachnida). (Conspectus Faunae Groenlandica. Pars secunda. II). Meddelelser on Grønland, 22: 481823.Google Scholar
Holt, R.D.Lawton, J.H. 1994. The ecological consequences of shared natural enemies. Annual Review of Ecology and Systematics, 25: 495520.CrossRefGoogle Scholar
Horstmann, K. 1969. Typenrevision der europäischen Arten der Gattung Diadegma Förster (syn. Angitia Holmgren). Beiträge zur Entomologie, 19: 413472.Google Scholar
Horstmann, K. 1973. Nachtrag zur Revision der europäischen Diadegma-Arten (Hymenoptera: Ichneumonidae). Beiträge zur Entomologie, 23: 131150.Google Scholar
Horstmann, K. 2001. Revisionen von Schlupfwespen-Arten V (Hymenoptera: Ichneumonidae). Mitteilungen der Münchner Entomologischen Gesellschaft, 91: 7786.Google Scholar
Horstmann, K. 2002. Revisionen von Schlupfwespen-Arten VI (Hymenoptera: Ichneumonidae). Mitteilungen der Münchner Entomologischen Gesellschaft, 92: 7991.Google Scholar
Ilmonen, J.Várkonyi, G. 2011. First record of Prosimulium ursinum (Diptera: Simuliidae) in Northeast Greenland. Entomologiske Meddelelser, 79: 2730.Google Scholar
Janzen, D.H., Walker, A.K., Whitfield, J.B., Delvare, G., Gauld, I.D. 2003. Host specificity and hyperparasitoids of three new Costa Rican species of Microplitis Foerster (Hymenoptera: Braconidae: Microgastrinae), parasitoids of sphingid caterpillars. Journal of Hymenoptera Research, 12: 4276.Google Scholar
Jussila, R. 1996. Ichneumonidae (Hymenoptera) of Greenland found in Scoresbysund (Ittoggortoormiit). Entomologica Fennica, 7: 145156.CrossRefGoogle Scholar
Jussila, R. (in press). Ichneumonidae. In The Greenland entomofauna. An identification manual of insects, arachnids and their allies. Edited by J. Böcher and N.P. Kristensen, Apollo Books, Vester Skerninge, Denmark.Google Scholar
Kaartinen, R., Stone, G.N., Hearn, J., Lohse, K., Roslin, T. 2010. Revealing secret liaisons: DNA bar-coding changes our understanding of food webs. Ecological Entomology, 35: 623638.CrossRefGoogle Scholar
Kopelke, J.-P. 1994. Der Schmarotzerkomplex (Brutparasiten und Parasitoide) der gallenbildenden Pontania-Arten. Senckenbergiana biologica, 73: 83133.Google Scholar
Kukal, O.Kevan, P.G. 1987. The influence of parasitism on the life history of a high Arctic insect, Gynaephora groenlandica (Wöcke) (Lepidoptera: Lymantriidae). Canadian Journal of Zoology, 65: 156163.CrossRefGoogle Scholar
LaSalle, J. 1993. Parasitic Hymenoptera, biological control and biodiversity. In Hymenoptera and biodiversity. Edited by J. LaSalle and I.D. Gauld. CAB International, Wallingford, United Kingdom. Pp. 197215.Google Scholar
Lee, S.-M.Chao, A. 1994. Estimating population size via sample coverage for closed capture–recapture models. Biometrics, 50: 8897.CrossRefGoogle ScholarPubMed
Lewinsohn, T.M., Novotny, V., Basset, Y. 2005. Insects on plants: diversity of herbivore assemblages revisited. Annual Review of Ecology, Evolution, and Systematics, 36: 597620.CrossRefGoogle Scholar
Lewinsohn, T.M.Roslin, T. 2008. Four ways toward tropical herbivore megadiversity. Ecology Letters, 11: 398416.CrossRefGoogle Scholar
Mason, W.R.M. 1968. New Canadian Cryptinae (Ichneumonidae: Hymenoptera). The Canadian Entomologist, 100: 1723.CrossRefGoogle Scholar
Meltofte, H., Christensen, T.R., Elberling, B., Forchhammer, M.C., Rasch, M. 2008. High-Arctic ecosystem dynamics in a changing climate: ten years of monitoring and research at Zackenberg Research Station, Northeast Greenland. Advances in Ecological Research, Volume 40. Academic Press – Elsevier, New York, NY, United States of America.Google Scholar
Memmott, J.Godfray, H.C.J. 1993. Parasitoid Webs. In Hymenoptera and biodiversity. Edited by J. LaSalle and I.D. Gauld. CAB International, Wallingford, United Kingdom. Pp. 217234.Google Scholar
Mills, N.J. 1992. Parasitoid guilds, life-styles, and host ranges in the parasitoid complexes of tortricoid hosts (Lepidoptera, Tortricoidea). Environmental Ecology, 21: 230239.Google Scholar
Morewood, W.D.Wood, D.M. 2002. Host utilization by Exorista thula Wood (sp. n.) and Chetogena gelida (Coquillett) (Diptera: Tachinidae), parasitoids of arctic Gynaephora species (Lepidoptera: Lymantriidae). Polar Biology, 25: 575582.CrossRefGoogle Scholar
Morris, R.J., Lewis, O.T., Godfray, H.C.J. 2004. Experimental evidence for apparent competition in a tropical forest food web. Nature, 428: 310313.CrossRefGoogle Scholar
Nielsen, I.C. 1910. A catalogue of the insects of north-east Greenland with descriptions of some larvae. Meddelelser om Grønland, 43: 5570.Google Scholar
Nixon, G.E.J. 1970. A revision of the N.W. European species of Microplitis Förster (Hymenoptera: Braconidae). Bulletin of the British Museum (Natural History), Entomology, 25: 130.Google Scholar
Novotny, V., Drozd, P., Miller, S.E., Kulfan, M., Janda, M., Basset, Y., et al. 2006. Why are there so many species of herbivorous insects in tropical rainforests? Science, 313: 11151118.CrossRefGoogle ScholarPubMed
Noyes, J.S. 2002. Interactive catalogue of world Chalcidoidea 2001. CD-ROM, 2nd edition. Taxapad, Vancouver, Canada.Google Scholar
Oksanen, L.Oksanen, T. 2000. The logic and realism of the hypothesis of exploitation ecosystems. The American Naturalist, 155: 703723.CrossRefGoogle ScholarPubMed
Oliver, D.R. 1963. Entomological studies in the Lake Hazen area, Ellesmere Island, including the lists of species of Arachnida, Collembola, and Insecta. Arctic, 16: 175180.CrossRefGoogle Scholar
Papp, J. 1989. Contribution to the braconid wasps of Greenland, Denmark (Hymenoptera: Braconidae). Folia Entomologica Hungarica, 100: 95104.Google Scholar
Quicke, D.L.J. 1997. Parasitic wasps. Chapman and Hall, London, United Kingdom.Google Scholar
Roininen, H., Danell, K., Zinovjev, A., Vikberg, V., Virtanen, R. 2002. Community structure, survival and mortality factors in Arctic populations of Eupontania leaf gallers. Polar Biology, 25: 605611.CrossRefGoogle Scholar
Roman, A. 1933. Schlupfwespen aus Ost-Grönland. Skrifter om Svalbard og Ishavet, 53: 513.Google Scholar
Roman, A. 1934. East Greenland Ichneumonids. Annals and Magazine of Natural History, Series 10, 14: 606611.CrossRefGoogle Scholar
Rougerie, R., Smith, M.A., Fernández-Triana, J., Lopez-Vaamonde, C., Ratnasingham, S., Hebert, P.D.N. 2011. Molecular analysis of parasitoid linkages (MAPL): gut contents of adult parasitoid wasps reveal larval host. Molecular Ecology, 20: 179186.CrossRefGoogle ScholarPubMed
Santos, A.M.C.Quicke, D.L.J. 2011. Large-scale diversity patterns of parasitoid insects. Entomological Science, 14: 371382.CrossRefGoogle Scholar
Santos, A.M.C., Quicke, D., Borges, P.A.V., Hortal, J. 2011. Species pool structure determines the level of generalism of island parasitoid faunas. Journal of Biogeography, 38: 16571667.CrossRefGoogle Scholar
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: 117142.Google Scholar
Schwarz, M.Shaw, M.R. 2000. 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 3. Tribe Phygadeuontini, subtribes Chiroticina, Acrolytina, Hemitelina and Gelina (excluding Gelis), with descriptions of new species. Entomologist's Gazette, 51: 147186.Google Scholar
Schwenke, W. 1999. Revision der europäischen Mesochorinae (Hymenoptera, Ichneumonoidea, Ichneumonidae). Spixiana Supplement, 26: 1124.Google Scholar
Schwenke, W. 2000. Eine neue Mesochorus-Art aus Käfern, mit einer Betrachtung der aus Käfern bekannten Mesochorinae (Hymenoptera, Ichneumonidae, Mesochorinae). Entomofauna, 21: 4956.Google Scholar
Shaw, M.R. 1994. Parasitoid host ranges. In Parasitoid community ecology. Edited by B.A. Hawkins and W. Sheehan. Oxford University Press, Oxford, United Kingdom. Pp. 111144.CrossRefGoogle Scholar
Shaw, M.R.Huddleston, T. 1991. Classification and biology of braconid wasps (Hymenoptera: Braconidae). Handbooks for the Identification of British Insects, 7: 1126.Google Scholar
Smith, M.A., Fernández-Triana, J., Roughley, R., Hebert, P.D.N. 2009. DNA barcode accumulation curves for understudied taxa and areas. Molecular Ecology Resources, 9 (Suppl. 1), 208216.CrossRefGoogle ScholarPubMed
Southwood, T.R.E.Henderson, P.A. 2000. Ecological methods, 3rd edition. Blackwell, Oxford, United Kingdom.Google Scholar
Tack, A., Gripenberg, S., Roslin, T. 2011. Can we predict indirect interactions from quantitative food webs? – An experimental approach. Journal of Animal Ecology, 80: 108118.CrossRefGoogle ScholarPubMed
Timms, L.L., Bennett, A.M.R., Buddle, C.M., Wheeler, T.A. In press. Assessing five decades of change in a high Arctic parasitoid community. Ecography, in press. doi: 10.1111/j.1600-0587.2012.00278.xCrossRefGoogle Scholar
Townes, H.K. 1983. Revisions of twenty genera of Gelini (Ichneumonidae). Memoirs of the American Entomological Institute, 35: 1281.Google Scholar
Townes, H.K.Townes, M. 1959. Ichneumon-flies of American north of Mexico: 1. Subfamily Metopiinae. Bulletin of the United States National Museum, 216: 1318.CrossRefGoogle Scholar
Townes, H.K.Townes, M. 1962. Ichneumon-flies of American north of Mexico: 3. Subfamily Gelinae, tribe Mesostenini. Bulletin of the United States National Museum, 216: 1602.CrossRefGoogle Scholar
Tscharntke, T.Hawkins, B.A. 2002. Multitrophic level interactions. Cambridge University Press, Cambridge, United Kingdom.CrossRefGoogle Scholar
Tschorsnig, H.-P.Herting, B. 1994. Die Raupenfliegen (Diptera: Tachinidae) Mitteleuropas: Bestimmungstabellen und Angaben zur Verbreitung und Ökologie der einzelnen Arten. Stuttgarter Beiträge zur Naturkunde, Serie A (Biologie), 506: 1170.Google Scholar
van Achterberg, C. 2006. The Braconidae (Hymenoptera) of Greenland. Zoologische Mededelingen (Leiden), 80: 1362.Google Scholar
van der Wal, R.Hessen, D.O. 2009. Analogous aquatic and terrestrial food webs in the high Arctic: the structuring force of a harsh climate. Perspectives in Plant Ecology, Evolution and Systematics, 11: 231240.CrossRefGoogle Scholar
van Veen, F.J.F., Morris, R.J., Godfray, H.C.J. 2006. Apparent competition, quantitative food webs, and the structure of phytophagous insect communities. Annual Review of Entomology, 51: 187208.CrossRefGoogle ScholarPubMed
Veijalainen, A., Sääksjärvi, I.E., Erwin, T.L., Gómez, I.C., Longino, J.T. 2013. Subfamily composition of Ichneumonidae (Hymenoptera) from western Amazonia: insights into diversity of tropical parasitoid wasps. Insect Conservation and Diversity, 6: 2837 . doi: 10.1111/j.1752-4598.2012.00185.x.CrossRefGoogle Scholar
Wahl, D.B.Sharkey, M.J. 1993. Superfamily Ichneumonoidea. In Hymenoptera of the world: an identification guide to families. Edited by H. Goulet and J.T. Huber. Research Branch, Agriculture Canada, Ottawa, Ontario, Canada. Pp. 358509.Google Scholar
Whitfield, J.B. 1997. Subfamily Microgastrinae. In Manual of the New World genera of the family Braconidae (Hymenoptera). Edited by R.A. Wharton, M. Marsh, and M.J. Sharkey. Special publication of the International Society of Hymenopterists, 1: 332–364.Google Scholar
Whitfield, J.B.Wharton, R.A. 1997. Subfamily Hormiinae. In Manual of the New World genera of the family Braconidae (Hymenoptera). Edited by R.A. Wharton, M. Marsh, and M.J. Sharkey. Special publication of the International Society of Hymenopterists, 1: 284–301.Google Scholar
Wright, D.H. 1983. Species-energy theory – an extension of species-area theory. Oikos, 41: 496506.CrossRefGoogle Scholar
Yu, D.S., van Achterberg, C., Horstmann, K. 2005. World Ichneumonoidea 2004 – taxonomy, biology, morphology and distribution. DVD/CD. Taxapad, Vancouver, Canada.Google Scholar