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Explaining variations in the diversity of parasitoid assemblages in a biosphere reserve of Mexico: evidence from vegetation, land management and seasonality

Published online by Cambridge University Press:  23 November 2017

A. González-Moreno ,
S. Bordera ,
J. Leirana-Alcocer ,
H. Delfín-González  and
H.S. Ballina-Gómez
A. González-Moreno*
Affiliation:
Instituto Tecnológico de Conkal, Avenida Tecnológico, s/n. C.P. 97345, Conkal, Yucatán, Mexico
S. Bordera
Affiliation:
Departamento de Ciencias Ambientales y Recursos Naturales/Instituto de Investigación CIBIO (Centro Iberoamericano de Biodiversidad), Universidad de Alicante, Apdo. Corr. 99, 03080, Alicante, Spain
J. Leirana-Alcocer
Affiliation:
Campus de Ciencias Biológicas y Agropecuarias, Universidad Autónoma de Yucatán, 97300, Mérida, Yucatán, México
H. Delfín-González
Affiliation:
Campus de Ciencias Biológicas y Agropecuarias, Universidad Autónoma de Yucatán, 97300, Mérida, Yucatán, México
H.S. Ballina-Gómez
Affiliation:
Instituto Tecnológico de Conkal, Avenida Tecnológico, s/n. C.P. 97345, Conkal, Yucatán, Mexico
*
*Author for correspondence Phone: +52 (999) 9124130 (ext.122) E-mail: [email protected]
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Abstract

Insect fauna biodiversity in natural protected areas has not been thoroughly studied. Therefore, the aim of this work was to assess whether and how vegetation types, land management and seasonality influence the diversity of Ichneumonidae (Hymenoptera) in the Ría Lagartos Biosphere Reserve (Mexico). A sampling programme was conducted using Malaise traps from 2008 to 2009 in three vegetation types, each with two conservation zones (core and buffer zones). Three seasons were considered: rainy, dry and north-winds (isolated storms from November to February). A total of 336 species were identified. Rarefaction and Generalized Linear Model indicated higher species richness and abundance, respectively, in the buffer zone of the dry forest; possible explanations for this finding include the intermediate disturbance hypothesis, wherein diversity can be higher in sites where disturbance is not very frequent or very intense, and the ‘enemies hypothesis’, wherein structural complexity and high plant diversity favour increased predators or, in this case, parasitoids. Diversity was higher during the rainy season, which may have been due to the higher availability of resources. Vegetation and management had a positive impact on the Coc (attack cocoons and pupae) and Myc (attack concealed larvae living in the fruiting bodies of mushrooms) parasitoid guilds. Members of the Coc guild are generalist parasitoids, which may be favoured in complex vegetation with a high richness of potential hosts and non-hosts. The Myc guild requires certain environmental conditions that promote fungal growth, such as humidity, that is absent in the other vegetation types of savannah and coastal dune scrubland.

Keywords

Ichneumonidaeprotected areaspecies richnessparasitoid diversityconservationNeotropic
Type
Research Papers
Information
Bulletin of Entomological Research , Volume 108 , Issue 5 , October 2018 , pp. 602 - 615
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Copyright © Cambridge University Press 2017 

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References

Abdala-Roberts, L., González-Moreno, A., Mooney, K. A., Moreira, X., González-Hernández, A. & Parra-Tabla, V. (2016) Effects of tree species diversity and genotypic diversity on leafminers and parasitoids in a tropical forest plantation. Agricultural and Forest Entomology 18(1), 43–51.Google Scholar
Anderson, A. & Purvis, G. (2008) The value of parasitic Hymenoptera as indicators of biological diversity. Strive report series No. 3, Environmental Protection Agency Programme 2007-2013, Dublin, Ireland.Google Scholar
Andrade, J.L., De la Barrera, E., Reyes-García, C., Ricalde, M.F., Vargas-Soto, G. & Cervera, J.C. (2007) El metabolismo ácido de las crasuláceas: diversidad, fisiología ambiental y productividad. Boletin de la Sociedad Botánica de México 81, 37–50.Google Scholar
Askew, R.R. & Shaw, M.R. (1986) Parasitoid communities: their size, structure and development. in Waage, J. & Greathead, D. (Eds). Insect Parasitoids, Vol. 8, London/Orlando, Academic Press, 225–264.Google Scholar
Bordera, S., González-Moreno, A., Sääksjärvi, I. E. & Veijalainen, A. (2010) Three new large-bodied species of Labena (Hymenoptera: Ichneumonidae: Labeninae), with a key to the Neotropical striata species group. Canadian Entomologist 142, 103–119.Google Scholar
Borer, E.T., Seabloom, E.W., Tilman, D. & Novotny, V. (2012) Plant diversity controls arthropod biomass and temporal stability. Ecology letters 15, 1457–1464.Google Scholar
Carignan, V. & Villard, M. (2002) Selecting indicator species to monitor ecological integrity: a review. Environmental Monitoring and Assessment 78, 45–61.Google Scholar
Chay-Hernández, D.A., Delfín-González, H. & Parra-Tabla, V. (2006) Ichneumonoidea (Hymenoptera) community diversity in an agricultural environment in the state of Yucatan, Mexico. Environmental Entomology 35, 1286–1297.Google Scholar
Colwell. (2009) EstimateS: Statistical Estimation of Species Richness and Shared Species from Samples, Version 8.20.Google Scholar
CONANP. (2000) Comision Nacional de Areas Naturales Protegidas 2000 Programa de Manejo Reserva de la Biósfera Ría Lagartos, Yucatán, México. Comisión Nacional de Áreas Naturales Protegidas, Secretaría del Medio Ambiente y Recursos Naturales, México.Google Scholar
Conell, J. (1978) Diversity in tropical rain forests and coral reefs. Science 199, 1302–1310.Google Scholar
Crist, T.O., Veech, J.A., Summerville, K.S. & Gering, J.C. (2003) Partitioning species diversity across landscapes and regions: a hierarchical analysis of alpha, beta and gamma diversity. The American Naturalist 162, 734–743.Google Scholar
Dasch, C.E. (1974) Neotropic Mesochorinae. Memoirs American Entomological Institute 22, 1–509.Google Scholar
Dasch, C.E. (1979) Ichneumon-flies of America north of Mexico: 8. Subfamily Cremastinae. Memoirs of the American Entomological Institute 29, 1–702.Google Scholar
De Rijk, M. (2016) Foraging behaviour by parasitoids in multiherbivore communities. PhD Thesis, Wageningen University, Wageningen, NL, 218p.Google Scholar
Dolphin, K & Quicke, D.J. (2001) Estimating the global species richness of an incompletely described taxon: an example using parasitoid wasps (Hymenoptera: Braconidae). Biological Journal of the Linnean Society 73, 279–286.Google Scholar
Flores, J.S. & Espejel, C.I. (1994) Tipos de Vegetación de la Península de Yucatán. Etnoflora Yucatanense Fasc. 3. México, Universidad Autónoma de Yucatán, UADY.Google Scholar
Fraser, S.E.M., Dytham, C. & Mayhew, P.J. (2007) Determinants of parasitoid abundance and diversity in woodland habitats. Journal of Applied Ecology 44, 352–361.Google Scholar
Fraser, S.E.M., Dytham, C. & Mayhew, P.J. (2008 a) The effectiveness and optimal use of Malaise traps for monitoring parasitoid wasps. Insect Conservation and Diversity 1, 22–31.Google Scholar
Fraser, S.E.M., Dytham, C. & Mayhew, P.J. (2008 b) Patterns in the abundance and distribution of ichneumonid parasitoids within and across habitat patches. Ecological entomology 33, 1–11.Google Scholar
Garbarczyk, H. & Sawoniewicz, J. (1984) Classification of parasitoids into guilds associated with different host groups. Ekologia polska 32, 261–270.Google Scholar
Gauld, I. D. (1987) Some factors affecting the composition of tropical ichneumonid faunas. Biological Journal of the Linnean Society 30, 299–312.Google Scholar
Gauld, I.D. (1988) A survey of the Ophioninae (Hymenoptera: Ichneumonidae) of tropical Mesoamerica with special reference to the fauna of Costa Rica. Bulletin of the British Museum (Natural History) 57, 1–309p.Google Scholar
Gauld, I.D. (1991) The Ichneumonidae of Costa Rica, 1. Memoirs of the American Entomological Institute 47, 1–589.Google Scholar
Gauld, I.D. (1997) The Ichneumonidae of Costa Rica, 2. Memoirs of the American Entomological Institute 57, 1–485.Google Scholar
Gauld, I.D. (2000) The Ichneumonidae of Costa Rica, 3. Memoirs of the American Entomological Institute 63, 1–453.Google Scholar
Gauld, I.D., Ugalde, J.A. & Hanson, P. (1998) Guía de los Pimplinae de Costa Rica (Hymenoptera: Ichneumonidae). Revista de Biología Tropical. International Journal of Tropical Biology and conservation 46, 1–189.Google Scholar
Gauld, I. D., Godoy, C, Sithole, R. & Ugalde, J. (2002) The Ichneumonidae of Costa Rica, 4. Memoirs of the American Entomological Institute 66, 1–768.Google Scholar
Godfray, H.C.J. (1994) Parasitoids Behavioral and Evolutionary Ecology. Princeton, New Jersey, USA, Princeton University Press.Google Scholar
González-Moreno, A. & Bordera, S. (2011) New records of Ichneumonidae (Hymenoptera: Ichneumonoidea) from Mexico. Zootaxa 2879, 1–21.Google Scholar
González-Moreno, A. & Bordera, S. (2012) The Ichneumonidae (Hymenoptera: Ichneumonoidea) from Ria Lagartos Biosphere Reserve, Mexico. Zootaxa 3230, 1–51.Google Scholar
González-Moreno, A., Bordera, S. & Delfín-González, H. (2010) A new species of Endasys Foerster, 1868 (Hymenoptera: Ichneumonidae) from Mexico with additional key to Nearctic species. Zootaxa 2648, 61–68.Google Scholar
González-Moreno, A., Bordera, S., Leirana-Alcocer, J. & Delfín-González, H. (2012) Diurnal flight behaviour of Ichneumonoidea (Insecta: Hymenoptera) related to environmental factors in a tropical dryforest. Environmental Entomology 41, 587–593.Google Scholar
González-Moreno, A., Bordera, S. & Delfín-González, H. (2015) Spatio-temporal diversity of Cryptinae (Hymenoptera, Ichneumonidae) assemblages in a protected area of southeast Mexico. Journal of Insect Conservation 19, 1153–1161. doi: 10.1007/s10841-015-9830-1.Google Scholar
Gotelli, N.J. & Entsminger, G.L.. (2004) EcoSim: Null models software for ecology. Version 7. Acquired Intelligence Inc. & Kesey-Bear. Jericho, VT 05465. http://garyentsminger.com/ecosim/index.htm (accessed June 2011).Google Scholar
Gullan, P. J. & Cranston, P. S. (2000) The Insects. An Outline of Entomology, 2nd edn. Oxford, UK, Blackwell Science.Google Scholar
Haddad, N.M., Bowne, D.R., Cunningham, A., Danielson, B.J., Levery, D.J., Sargent, S. & Spira, T. (2003) Corridor use by diverse taxa. Ecology 84, 609–615.Google Scholar
Haslett, J.R. (2001) Biodiversity and conservation of Diptera in heterogeneous land mosaics: a fly's eye view. Journal of Insect Conservation 5, 71–75.Google Scholar
Hawkins, B.A. (1988) Species diversity in the third and fourth trophic levels: patterns and mechanisms. Journal of Animal Ecology 57, 137–162.Google Scholar
Hawkins, B.A. & Lawton, J.H. (1987) Species richness for parasitoids of British phytophagous insects. Nature 326, 788–790.Google Scholar
Hawkins, B.A., Shaw, M.R. & Askew, R.R. (1992) Relations among assemblage size, host specialization, and climatic variability in North American parasitoid communities. The American Naturalist 139, 58–79.Google Scholar
Henderson, P.A. & Seaby, R.M.H. (2002) Software Species diversity and richness III, version 3.0.2. Pisces Conservation, Lymington.Google Scholar
Hill, M.O. (1979) DECORANA – A Fortran Program for Detrended Correspondence Analysis and Reciprocal Averaging. Ecology and Systematics. 52p. Ithaca, New York, USA, Cornell University.Google Scholar
Hirose, Y. (1994) Determinants of species richness and composition in egg parasitoid assemblages of Lepidoptera. pp. 19–29 in Hawkins, B.A. and Sheehan, W. (Eds) Parasitoid Community Ecology, Vol. 2. Oxford, Oxford University Press.Google Scholar
Hochberg, M.E. & Ives, A.R. (2000) Parasitoid Population Biology. USA, Princeton University Press.Google Scholar
Idris, A.B., Gonzaga, A.D., Zaneedarwaty, N.N., Hasnah, B.T. & Natasha, B.Y. (2001) Does habitat disturbance has adverse effect on the diversity of parasitoid community? Online Journal of Biological Sciencies 1, 1040–1042.Google Scholar
Idris, A.B. & Hainidah, J. (2003) Diversity of Ichneumonid Wasps in the Logged over Forests of Langat Basin in Selangor, Malaysia. Journal of Biological Sciencie 3(2), 259–270.Google Scholar
Inclán, D.J., Cerretti, P. & Marini, L. (2014) Interactive effects of area and connectivity on the diversity of tachinid parasitoids in highly fragmented landscapes. Landscape Ecology 29, 879–889.Google Scholar
Jactel, H. & BrockerhoV, E.G. (2007) Tree diversity reduces herbivory by forest insects. Ecology Letters 10, 835–848.Google Scholar
Janzen, D.H. (1981) The peak in North American Ichneumonid species richness lies between 38° and 42° N. Ecology 62(3), 532–537.Google Scholar
Jervis, M.A., Kidd, N.A.C., Fitton, M.G., Huddleston, T. & Dawah, H.A. (1993) Flower-visiting by hymenopteran parasitoids. Journal of Natural History 27, 67–105.Google Scholar
Kasparyan, D.R. (2007 a) Review of Mexican species of the genus Itoplectis Foerst. (Hymenoptera: Ichneumonidae: Pimplinae) with description of four new species. Russian Entomological Journal 16, 109–114.Google Scholar
Kasparyan, D.R. (2007 b) A new species of Lagoleptus from Mexico (Hymenoptera: Ichneumonidae: Tryphoninae). Zoosystematica Rossica 16, 262.Google Scholar
Kasparyan, D.R. (2007 c) Review of Mexican species of the genus Phytodietus Gravenhorst (Hymenoptera: Ichneumonidae). Zoosystematica Rossica 16, 49–58.Google Scholar
Kasparyan, D.R. & Ruíz-Cancino, E. (2004 a) Adenda a Ichneumonidae (Hymenoptera). pp. 721–723 in Llorente, B.J., Morrone, J.J., Yáñez, O. & Vargas, I.F. (Eds) Biodiversidad, Taxonomía ybiogeografía de artrópodos de México, Vol. IV. México, UNAM-CONABIO.Google Scholar
Kaparyan, D.R. & Ruíz-Cancino, E. (2004 b) Review of Mexican species of the genus Polycyrtus Spinola 1840 (Hymenoptera: Ichenumonidae: Cryptinae) with key to the species of North America. Russian Entomological Journal 12, 311–327.Google Scholar
Kasparyan, D.R. & Ruíz-Cancino, E. (2004 c) Two new species of the genus Phytodietus Gravenhorst, 1829 (Hymenoptera: Ichneumonidae) from Mexico. Russian Entomological Journal 13, 73–76.Google Scholar
Kasparyan, D.R. & Ruíz-Cancino, E. (2004 d) Review of North American species of the genus Lymeon Foerster, 1869 (Hymenoptera: Ichneumonidae: Cryptini). Zoosystematica Rossica 13, 53–79.Google Scholar
Kasparyan, D.R. & Ruíz-Cancino, E. (2005) Avispas parasíticas de plagas y otros insectos. Cryptini de México (Hymenoptera: Ichneumonidae: Cryptinae) Parte I. UAT, Cd. Victoria, Tamaulipas, México.Google Scholar
Kasparyan, D.R. & Ruíz-Cancino, E. (2008) Cryptini de México (Hymenoptera: Ichneumonidae: Cryptinae) Parte II. Serie Avispas parasíticas de plagas y otros insectos. UAT, Cd. Victoria, Tamaulipas, México.Google Scholar
Khalaim, A.I. & Ruiz-Cancino, E. (2009) Mexican species of Labena Cresson (Hymenoptera, Ichneumonidae) with description of a new species. ZooKeys 5, 65–74.Google Scholar
Klein, A. M., Steffan-Dewenter, I., Buchori, D. & Tscharntke, T. (2002) Effects of land-use intensity in tropical agroforestry systems on coffee flower-visiting and trap-nesting bees and wasps. Conservation Biology 16(4), 1003–1014.Google Scholar
Landis, D. A. & Menalled, F. D. (1998) Ecological considerations in the conservation of effective parasitoid communities in agricultural systems. pp. 101–121 in Pedro, Barbosa (Ed.) Conservation Biological Control. San Diego, USA, Academic Press.Google Scholar
LaSalle, J. & Gauld, I.D. (1993) Hymenoptera: their diversity, and their impact on the diversity of other organisms. 197–215. in LaSalle, J. and Gauld, I.D. (Eds) Hymenoptera and Biodiversity. Vol. 8, Wallinford, UK, C.A.B. International.Google Scholar
Legendre, P & Legendre, L. (1998) Numerical Ecology. Amsterdam, The Netherlands, Elsevier.Google Scholar
Leirana-Alcocer, J.L., Hernádez-Betancourt, S., Salinas-Peba, L. & Guerrero-González, L. (2009) Cambios en la estructura y composición de la vegetación relacionados con los años de abandono de tierras agropecuarias en la selva baja caducifolia espinosa de la reserva de Dzilam, Yucatán. Polibotánica 27, 53–70.Google Scholar
Letourneau, D. K. (1987) The enemies hypothesis: tritrophic interactions and vegetational diversity in tropical agroecosystems. Ecology 68(6), 1616–1622.Google Scholar
Lewis, C. N. & Whitfield, J. B. (1999) Braconid wasp (Hymenoptera: Braconid) diversity in forest plots under different silvicultural methods. Environmental Entomology 6, 986–997.Google Scholar
Longino, J.T. (1994) How to measure arthropod diversity in a tropical rainforest. Biology International 28, 3–13.Google Scholar
Magurran, A.E. (2004) Measuring Biological Diversity. UK, Blackwell Publishing.Google Scholar
Mazon, M. & Bordera, S. (2008) Effectiveness of two sampling methods used for collecting Ichneumonidae (Hymenoptera) in the Cabañeros National Park (Spain). European Journal of Entomology 105, 876–888.Google Scholar
Mazon, M. & Bordera, S. (2014) Diversity of Ichneumonidae (Insecta: Hymenoptera) in a protected area of Central Spain: what are we protecting? Insect Conservation and Diversity 7, 432–452. doi: 10.1111/icad.12067.Google Scholar
McCullagh, P. & Nelder, J. A. (1989) Generalized Linear Models. London, UK, Chapman & Hall.Google Scholar
Meagher, R. L., Nuessly, G. S., Nagoshi, R. N. & Hay-Roe, M. M. (2016) Parasitoids attacking fall armyworm (Lepidoptera: Noctuidae) in sweet corn habitats. Biological Control 95, 66–72.Google Scholar
Menalled, F., Marino, C. P., Gage, S. & Landis, A. D. (1999) Does agricultural landscape structure affect parasitism and parasitoid diversity? Ecological Applications 9, 634–641.Google Scholar
Mulder, C., Koricheva, J., Huss-Danell, K., Högberg, P. & Joshi, J. (1999) Insects affect relationships between plant species richness and ecosystem processes. Ecology Letters 2, 237–246.Google Scholar
New, T.R. (2015) Insect Conservation in Urban Environments. 244p. Switzerland, Spriger international Publishing.Google Scholar
Noyes, J.S. (1989) The diversity of Hymenoptera in the tropics with special reference to Parasitica in Sulawesi. Ecological Entomology 14, 197–207.Google Scholar
Östman, Ö., Ekbom, B. & Bengtsson, J. (2001) Landscape heterogeneity and farming practice influence biological control. Basic and Applied Ecology 2(4), 365–371.Google Scholar
Pak, D., Iverson, A. L., Ennis, K. K., Gonthier, D. J. & Vandermeer, J. H. (2015) Parasitoid wasps benefit from shade tree size and landscape complexity in Mexican coffee agroecosystems. Agriculture, Ecosystems & Environment 206, 21–32.Google Scholar
Pérez-Urbina, B., Correa-Sandoval, A., Ruíz-Cancino, E., Kasparyan, D., Coronado-Blanco, J.M. & Horta-Vega, J. (2010) Diversidad de Ichneumonidae (Hymenoptera) en el Cañón del Novillo, Victoria, Tamaulipas, México. Entomotropica 25, 83–97.Google Scholar
Portillo-Quintero, C.A. & Sánchez-Azofeifa, G.A. (2010) Extent and conservation of tropical dry forests in the Americas. Biological Conservation 143, 144–155.Google Scholar
Price, P. W., Bouton, C. E., Gross, P., McPheron, B. A., Thompson, J. N. & Weis, A. E. (1980) Interactions among three trophic levels: influence of plants on interactions between insect herbivores and natural enemies. Annual Review of Ecology and Systematics 11, 41–65.Google Scholar
Price, P. W., Denno, R. F., Eubanks, M. D., Finke, D. L. & Kaplan, I.. (2011) Insect Ecology : Behavior, Populations and Communities. 769p. Cambridge, USA, Cambridge University Press.Google Scholar
Quicke, D. (2015) The Braconid and Ichneumonid Parasitoid Wasps, Biology, Systematics, Evolution and Ecology. Wiley Blackwell.Google Scholar
Rodríguez-Berrío, A. (2006) Estudio de la fauna de Ichneumonidae cenobiontes (Hymenoptera) como potenciales bioindicadores de diversidad en ecosistemas de Montaña Mediterránea p. 228, Thesis, July 2006, Universidad de Alicante.Google Scholar
Root, R.B. (1973) Organization of a plant-arthropod association in simple and diverse habitats: the fauna of collards (Brassica oleracea). Ecological Monographs 43, 95–124.Google Scholar
Roschewitz, I., Hücker, M., Tscharntke, T. & Thies, C. (2005) The influence of landscape context and farming practices on parasitism of cereal aphids. Agriculture, Ecosystems & Environment 108(3), 218–227.Google Scholar
Ruíz-Cancino, E. (2010) Ichneumonidae (Hymenoptera) del Estado de Tamaulipas, México. Serie avispas parasíticas de plagas y otros insectos, No. 6. Tamaulipas, México, Universidad Autónoma de Tamaulipas.Google Scholar
Ruíz-Cancino, E. & Tejada, L.O. (1986) Géneros de Ichneumonidae del Noreste de México. Southwestern Entomologist 11, 37–41.Google Scholar
Ruíz-Cancino, E., Coronado, B.J. & Martínez, R.J. (2002) Contribución al conocimiento de Ichneumonidae (Hymenoptera) del sureste de México. México, Serie Publicaciones Científicas CIDAFF-UATT.Google Scholar
Ruiz-Cancino, E., Kasparyan, D.R., Coronado, B.J., Myartseva, S.N., Trjapitzin, V.A., Hernández, A.S. & García, J.J. (2010) Himenópteros de la Reserva “El Cielo”, Tamaulipas, México. Dugesiana 17, 53–71.Google Scholar
Russell, E. P. (1989) Enemies hypothesis: a review of the effect of vegetational diversity on predatory insects and parasitoids. Environmental Entomology 18(4), 590–599.Google Scholar
Rzedowski, J. (2006) Vegetación de México. First digital edition. México, Comisión Nacional para el Conocimiento y Uso de la Biodiversidad.Google Scholar
Sääksjärvi, I.E., Haataja, S., Neuvonen, S., Gauld, I., Jussila, R. & Salo, J. (2004) High local especies richness of parasitics wasp (Hymenoptera: ichneumonidae: Pimplinae and Rhyssinae) from the lowland rainforest of Peruvian Amazonia. Ecological Entomology 29, 735–743.Google Scholar
Sääksjärvi, I.E., Ruokolainen, K., Tuomisto, H., Haataja, S., Fine, P.V.A., Cárdenas, G., Mesones, I. & Targas, V. (2006) Comparing composition and diversity of parasitoid wasps and plants in an Amazonian rainforest mosaic. Journal of Tropical Ecology 22, 167–176.Google Scholar
Samways, M.J. (2007) Insect conservation: a synthetic management approach. The Annual Review of Entomology 52, 465–487.Google Scholar
Scherber, C., Eisenhauer, N., Weisser, W.W., Schmid, B., Voigt, W., Schulze, E., Roscher, C., Weigelt, A., Allan, E., Beßler, H., Bonkowski, M., Buchmann, N., Buscot, F., Clement, L., Ebeling, A., Engels, C., Fischer, M., Halle, S., Kertscher, I., Klein, A.M., Koller, R., König, S., Kowalski, E., Kummer, V., Kuu, A., Lange, M., Lauterbach, D., Middelhoff, C., Migunova, V.D., Milcu, A., Müller, A., Partsch, S., Petermann, J.S., Renker, C., Rottstock, T., Sabais, A., Scheu, S., Schumacher, J., Temperton, V.M. & Tscharntke, T. (2010) Bottom-up effects of plant diversity on multitrophic interactions in a biodiversity experiment. Nature 468, 553–556.Google Scholar
Shapiro, B.A. & Pickering, J. (2000) Rainfall and parasitic wasp (Hymenoptera: Ichneumonoidea) activity in successional forest stages at Barro Colorado, Nature, Monument, Panama, and La Selva Biological Station, Costa Rica. Agricultural and Forest Entomology 2, 39–47.Google Scholar
Sharkey, M.J. (2007) Phylogeny and classification of hymenoptera. Zootaxa 1668, 521–548.Google Scholar
Sheehan, W. (1986) Response by specialist and generalist natural enemies to agroecosystem diversification: a selective review. Environmental Entomology 15, 456–461.Google Scholar
Skillen, E.L., Pickering, J. & Sharkey, M. J. (2000) Species richness of the Campopleginae and ichneumoninae (hymenoptera: ichneumonidae) along a latitudinal gradient in Eastern North American old- growth forests. Environmental Entomology 29, 460–466.Google Scholar
Sobek, S., Steffan-Dewenter, I., Scerber, C. & Tscharntke, T. (2009) Spatiotemporal changes of beetle communities across a tree diversity gradient. Diversity and Distributions 15, 660–670. doi: 10.1111/j.1472-4642.2009.00570.x.Google Scholar
Speight, M.R., Hunter, M.D. & Watt, A.D. (2008) Ecology of Insects Concepts and Applications. 628p. New York, USA, Wiley-Blacwell.Google Scholar
Stork, N.E., Srivastava, D.S., Eggleton, P., Hodda, M., Lawson, G., Leakey, R.R.B. & Watt, A.D. (2017) Consistency of effects of tropical-forest disturbance on species composition and richness relative to use of indicator taxa. Conservation Biology 31, 924–933. doi: 10.1111/cobi.12883.Google Scholar
Szentkirályi, F. & Kozár, F. (1991) How many species are there in apple insect communities?: testing the resource diversity and intermediate disturbance hypotheses. Ecological Entomology 16, 491–503.Google Scholar
Ter Braak, C.J.F. & Smilauer, P.. (2002) CANOCO Reference Manual and CanoDraw for Windows User'Guide: Software for Canonical Community Ordination (Version 4.5). 500p. Ithaca, New York, USA, Microcomputer Power.Google Scholar
Townes, H. (1969) The genera of Ichneumonidae, Part 1. Memoirs of the American Entomological Institute 11, 1–300.Google Scholar
Townes, H. (1970a) The genera of Ichneumonidae, Part 2. Memoirs of the American Entomological Institute 12, 1–537.Google Scholar
Townes, H. (1970b) The genera of ichneumonidae, part 3. Memoirs of the American Entomological Institute 13, 1–307.Google Scholar
Townes, H. (1971) The genera of Ichneumonidae, Part 4. Memoirs of the American Entomological Institute 17, 1–372.Google Scholar
Townes, H. & Townes, M. (1959) Ichneumon-Flies of America North of Mexico: 1. Subfamily Metopiinae. United States National Museum Bulletin 216. Part 1. Smithsonian Institution.Google Scholar
Townes, H. & Townes, M. (1962) Ichneumon-Flies of America North of Mexico: 3. Subfamily Gelinae, Tribe Mesostenini. United States National Museum Bulletin 216. Part 3. Smithsonian Institution.Google Scholar
Townes, H. & Townes, M. (1966) A catalogue and reclassification of the Neotropic Ichneumonidae. Memoirs of the American Entomological Institute 8, 1–367.Google Scholar
Tscharntke, T., Klein, M., Kruess, A., Steffan-Dewenter, I. & Thies, C. (2005) Landscape perspectives on agricultural intensification and biodiversity - ecosystem service management. Ecology Letters 8, 857–874.Google Scholar
Tylianakis, J.M., Klein, A.M. & Tscharntke, T. (2005) Spatiotemporal variation in the diversity of Hymenoptera across a tropical habitat gradient. Ecology 86(12), 3296–3302.Google Scholar
Veech, J.A. & Crist, T. O. (2009) Partition: software for hierarchical partitioning of species diversity, version 3.0. http://www.users.muohio.edu/cristto/partition.htm.Google Scholar
Vehvilainen, H., Koricheva, J & Ruohomaki, K. (2007) Tree species diversity influences herbivore abundance and damage: meta-analysis of long-termforest experiments. Oecologia 152, 287–298.Google Scholar
Vehvilainen, H., Koricheva, J. & Ruohomaki, K. (2008) Effects of stand tree species composition and diversity on abundance of predatory arthropods. Oikos 117, 935–943.Google Scholar
White, E.P., Adler, P.B., Lauenroth, W.K., Gill, R.A., Greenberg, D., Kaufman, M., Rassweiler, A., Rusak, J.A., Smith, M.D., Steinbeck, J.R., Waide, R.B. & Yao, J. (2006) A comparison of the species time relationship across ecosystems and taxonomic groups. Oikos 112, 185–195.Google Scholar
Zar, J.H. (1984) Biostatistical Analysis. 2nd edn. Englewood Cliffs, NJ: Prentice Hall.Google Scholar
Zhang, Y. & Adams, J. (2011) Top-down control of herbivores varies with ecosystem types. Journal of Ecology 99, 370–372.Google Scholar
Zhao, Z. H., Hui, C., Hardev, S., Ouyang, F., Dong, Z. & Ge, F. (2014) Responses of cereal aphids and their parasitic wasps to landscape complexity. Journal of Economic Entomology 107(2), 630–637.Google Scholar
Zou, Y., Sang, W., Bai, F. & Axmacher, J.C. (2013) Relationships between plant diversity and the abundance and α-diversity of predatory ground beetles (coleoptera: carabidae) in a mature asian temperate forest ecosystem. PLoS ONE 8(12), e82792. doi:10.1371/journal.pone.0082792.Google Scholar
Yu, D.S., van Achterberg, C. & Horstmann, K. (2012) World Ichneumonoidea 2011. Taxonomy, biology, morphology and distribution. Taxapad 2012.Google Scholar