Abstract
This study provides the first survey of the parasitoid fauna reared in flower heads of Asteraceae in the Brazilian cerrado. We investigated the relative importance of herbivore richness and plant species commonness to differences in parasitoid species richness among the plant species. A total of 15,372 specimens from 192 morphospecies belonging to 103 genera of Hymenoptera were reared from the flower heads of 74 Asteraceae species. Chalcidoidea and Ichneumonoidea were the most common superfamilies, with Eulophidae and Braconidae as the main families of parasitoid wasps. Singletons and doubletons accounted for 45% of total parasitoid species richness. The number of parasitoid species per plant species ranged from 1 to 67, and the variation in parasitoid species richness among plants was mainly explained by the number of sites in which the plants were recorded. This study shows that there is a highly diversified fauna of Hymenoptera parasitoids associated with flower heads of Asteraceae in the Brazilian cerrado. Our findings suggest that the accumulation of parasitoid species on plants is mainly determined by the regional commonness of plant species rather than the number of herbivore species associated with the plants.
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Almeida AM, Fonseca CR, Prado PI, Almeida-Neto M, Diniz S, Kubota U, Braun MR, Raimundo RLG, Anjos LA, Mendonça TG, Futada SM, Lewinsohn TM (2006) Assemblages of endophagous insects on Asteraceae in São Paulo cerrados. Neotropical Entomol 35:458–468
Almeida-Neto M, Prado PI, Kubota U, Bariani JM, Aguirre GH, Lewinsohn TM (2010) Invasive grasses and native Asteraceae in the Brazilian cerrado. Plant Ecol 209:109–122
Almeida-Neto M, Prado PIP, Lewinsohn TM (2011) Phytophagous insect fauna tracks host plant responses to exotic grass invasion. Oecologia 165:1051–1062
Antonelli A, Sanmartín I (2011) Why are there so many plant species in the neotropics? Taxon 60:403–414
Araújo W, Santos B, Gomes-Klein V (2011) Insect galls from Serra dos Pireneus, GO, Brazil. Biota Neotropical 11:357–365
Arbuckle JL (2003) Amos 5 (computer software). Smallwaters, Chicago
Boucek Z (1988) Australasian Chalcidoidea (Hymenoptera). A biosystematic revision of genera of fourteen families, with a reclassification of species. p 832
Boucek Z, Delavare G (1992) On the new world Chalcididae (Hymenoptera). Mem Am Entol Inst 53:1–446
Brown KS, Gifford DR (2002) Lepidoptera in the cerrado landscape and the conservation of vegetation, soil and topographical mosaics. In: Oliveira PS, Marquis RJ (eds) The Cerrados of Brazil: ecology and natural history of a neotropical savanna. Columbia University Press, New York, pp 201–217
Buffington M (2004) Taxonomic notes on Nordlandiella Diaz and Ganaspidium Weld (Hymenoptera: Figitidae: Eucoilinae). Proc Entomol Soc of Wash 106:192–198
Buffington ML, Ronquist F (2006) Familia Figitidae. In: Fernández F, Sharkey MJ (eds) Introducción a los Hymenoptera de la Región Neotropical. Serie Entomología Colombiana. Sociedad Colombiana de Entomología, Bogotá, pp 811–823
Burks BBD (1971) A synopsis of the genera of the family Eurytomidae (Hymenoptera: Chalcidoidea). Trans Am Entomol Soc 97:1–89
Camargo AJA, Becker VO (1999) Saturniidae (Lepidoptera) from the Brazilian cerrado: composition and biogeographic relationships. Biotropica 31:696–705
Dias BFS (1996) Cerrados: uma caracterização. In: Dias BF (ed) Alternativas de desenvolvimento dos cerrados: manejo e conservação dos recursos naturais renováveis, 1st edn. Fundação Pró-Natureza, Brasília, pp 11–25
Dias ATC, Trigo JR, Lewinsohn TM (2010) Bottom-up effects on a plant-endophage-parasitoid system: the role of flower-head size and chemistry. Aust Ecol 35:104–115
Diaz N, Gallardo F (2000) Cynipoidea parasitoids of dung-flies in Brazil. II (Insecta: Hymenoptera). Anais da Sociedade Entomológica do Brasil 29:469–474
Diniz S, Prado PI, Lewinsohn TM (2010) Species richness in natural and disturbed habitats: Asteraceae and flower-head insects (Tephritidae: Diptera). Neotropical Entomol 39:163–171
Dyer L (2007) Tropical tritrophic interactions: nasty hosts and ubiquitous cascades. In: Carson W, Schnitzer S (eds) Tropical forest community ecology. Blackwell Science, Oxford, pp 275–293
Fernández F, Sharkey MJ (2006) Introducción a los Hymenoptera de la región neotropical. Serie entomología colombiana. Sociedad colombiana de entomología, Bogotá, p 894
Filgueiras TS (2002) Herbaceous plant communities. In: Oliveira PS, Marquis RJ (eds) The cerrados of Brazil: ecology and natural history of a neotropical savanna. Columbia University Press, New York, pp 121–139
Flores AFH, Penteado-Dias AM (2011) Five new species of the genus Sphelodon (Hymenoptera: Ichneumonidae) from Brazil with a key to the neotropical species. Rev Biol Tropical 59:1621–1635
Fonseca CR (2009) The silent mass extinction of insect herbivores in biodiversity hotspots. Conserv Biol 23:1507–1515
Fonseca CR, Prado PI, Almeida-Neto M, Kubota U, Lewinsohn TM (2005) Flower-heads, herbivores, and their parasitoids: food web structure along a fertility gradient. Ecol Entomol 30:36–46
Gagné RJ (1994) The gall midges of the neotropical region. Cornell University Press, Ithaca, 357
Gauld I (1997) Ichneumonidae of Costa Rica, 2. Mem Am Entomol Inst 57:1–485
Gauld I (2000) Ichneumonidae of Costa Rica 3. Mem Am Entomol Inst 63:1–453
Gering J, DeRennaux KA, Crist TO (2007) Scale dependence of effective specialization: its analysis and implications for estimates of global insect species richness. Divers Distrib 13:115–125
Gibson G (1995) Parasitic wasps of the subfamily Eupelminae: classification and revision of the world genera (Hymenoptera: Chalcidoidea: Eupelmidae). Mem Entomol Int 5:426
Gibson GAP, Huber JT, Woolley JB (1997) Annotated keys to the genera of nearctic Chalciodoidea (Hymenoptera). NRC Research Press, Ottawa, 794
Gordh G, Moczar L (1990) A catalog of the world Bethylidae (Hymenoptera: Aculeata). Mem Am Entomol Inst 46:1–364
Grace JB (2006) Structural equation modeling and natural systems. Cambridge University Press, Cambridge, 349
Guimarães JA, Gallardo FE, Diaz NB (2005) Contribution to the systematic of Odontosema Kieffer (Hymenoptera: Cynipoidea: Figitidae). Trans Am Entomol Soc 3:1–5
Hayat M (1983) The genera of Aphelinidae (Hymenoptera) of the world. Syst Entomol 8:63–102
Johnson NF (1987) Systematics of new world Trissolcus, a genus of pentatomid egg-parasites (Hymenoptera: Scelionidae). J Nat Hist 21:285–304
Kelly CK, Southwood TR (1999) Species richness and resource availability: a phylogenetic analysis of insects associated with trees. Proc Natl Acad Sci U S A 96:8013–8016
Köppen W (1948) Climatologia: con un estudio de los climas de la tierra. Fondo de Cultura Económica, México, p 478
Lewinsohn T (1988) Composição e tamanho de faunas associadas à capítulos de compostas. PhD Thesis, Universidade Estadual de Campinas, Campinas
Lewinsohn T (1991) Insects in flower heads of Asteraceae in southeast Brazil: a tropical case study in species richness. In: Price P, Lewinsohn T, Fernandes G, Benson W (eds) Evolutionary ecology of plant-animal interactions: tropical and temperate perspectives. Wiley, New York, pp 525–559
Lewinsohn TM, Novotny V, Basset Y (2005) Insects on plants: diversity of herbivore assemblages revisited. Annu Rev Ecol Syst 36:597–620
Lewis OT, Memmott J, LaSalle J, Lyal CHC, Whitefoord C, Godfray HCJ (2002) Structure of a diverse tropical forest insect-parasitoid community. J Anim Ecol 71:855–873
Lin N, Huber J, LaSalle J (2007) The Australian genera of Mymaridae (Hymenoptera: Chalcidoidea). Zootaxa 1596:1–111
Lomolino MV (2004) Conservation biogeography. In: Lomolino MV (ed) Directions in the geography of nature. Sinauer Associates, Sunderland, pp 293–296
MacCallum RC, Browne MW, Sugawara HM (1996) Power analysis and determination of sample size for covariance structure modeling. Psychol Methods 1:130–149
Masner L (1993) Superfamily Platygastroidea (pp. 558–565). In: Goulet H, Huber J (eds) Hymenoptera of the world: an identification guide to families. Research Branch. Agriculture Canada, Ottawa, p 668
Masner, L. (2006) Superfamilia Ceraphronoidea. In: Fernández F, Sharkey MJ (eds.) Introducción a los Hymenoptera de la región Neotropical. Sociedad Colombiana de Entomología y Univerdidad Nacional de Colombia, Bogotá D.C. 894 pp 785–792
Myers N, Mittermeier RA, Mittermeier CG, Fonseca GA, Kent J (2000) Biodiversity hotspots for conservation priorities. Nature 403:853–858
Nascimento AR, Penteado-Dias AM (2011) New species of Chelonus (Microchelonus) Szépligeti, 1908 (Hymenoptera: Braconidae: Cheloninae) from Brazil. Braz J Biol 71:511–515
Novotny V, Basset Y (2000) Rare species in communities of tropical insect herbivores: pondering the mystery of singletons. Oikos 89: 564–572
Noyes JS (1980) A review of the genera of neotropical Encyrtidae (Hymenoptera: Chalcidoidea). Bull Br Mus 41:107–253
Ødegaard F, Diserud OH, Engen S, Aagaard K (2000) The magnitude of local host specificity for phytophagous insects and its implications for estimates of global species richness. Conserv Biol 14:1182–1186
Ovruski S, Wharton R, Rull J, Guillén L (2007) Aganaspis alujai (Hymenoptera: Figitidae: Eucoilinae), a new species attacking Rhagoletis (Diptera: Tephritidae) in the neotropical region. Fla Entomol 90:626–634
Perre P, Loyola RD, Lewinsohn TM, Almeida-Neto M (2011) Insects on urban plants: contrasting the flower head feeding assemblages on native and exotic hosts. Urban Ecosyt 14:01–12
Prado PI, Lewinsohn TM (2002) The fauna of Tephritidae (Diptera) from capitula of Asteraceae in Brazil. Proc Entomol Soc Wash 104:1007–1028
Prado PI, Lewinsohn TM (2004) Compartments in insect–plant associations and their consequences for community structure. J Anim Ecol 73:1168–1178
Preacher KJ, Coffman DL (2006) Computing power and minimum sample size for RMSEA [Computer software]. Available from http://quantpsy.org/
Quinlan J (1986) A key to the Afrotropical genera of Eucoilidae (Hymenoptera), with a revision of certain genera. Bull Br Mus Entomol 52:243–366
Rezende AV, Walter BMT, Fagg CW, Felfili JM, Júnior MCS, Nogueira PE, Mendonça RC, Filgueiras TS, Sano SM, Almeida SP, Ribeiro JF (2008) Cerrado: ecologia e flora, Vol. 2. Embrapa Informação Tecnologica, Brasília, p 876
Rott AS, Godfray HCJ (2000) The structure of a leafminer-parasitoid community. J Anim Ecol 69:274–289
Salvo A, Valladares G (1998) Taxonomic composition of parasitoid communities (Hymenoptera, Parasitica) of agromyzid leafminers (Diptera, Agromyzidae) in Argentina. Stud Neotropical Fauna Environ 33:116–123
Salvo A, Valladares GR, Cagnolo L (2013) Parasitic assemblages on leafminers? A comparison of structure and function among host orders. Stud Neotropical Fauna Environ 46:11–22
Sandonato DL, Onody HC, Penteado-Dias A (2010) Fauna de Campopleginae (Hymenoptera, Ichneumonidae) em hortas orgânicas em Araraquara e São Carlos, SP, Brasil. Biota Neotropical 10:117–121
Sano SM, de Almeida SP, Ribeiro JF (2008) Cerrado: ecologia e flora, vol 1. Embrapa Informação Tecnológica, Brasília, 406
Shipley B (2000) Cause and correlation in biology: a user’s guide to path analysis, structural equations, and causal inference. Oxford University Press, Oxford, p 317
Triapitsyn S (2006) Hymenoptera: egg parasitoids of Proconiine sharpshooters (Hemiptera: Cicadellidae) in the nearctic region, with description of two new species of Gonatocerus. Zootaxa 38:1–38
Urso-Guimarães M, Scareli-Santos C, Bonifácio-Silva A (2003) Occurrence and characterization of entomogen galls in plants from natural vegetation areas in Delfinópolis, MG, Brazil. Braz J Biol 63:705–715
Valladares G, Salvo A (2001) Community dynamics of leafminers (Diptera: Agromyzidae) and their parasitoids (Hymenoptera) in a natural habitat from central Argentina. Acta Oecol 22:301–309
Warming E (1973) Lagoa Santa, contribuição para a geografia fitobiológica. In: Warming E, Ferri M (eds) Lagoa Santa e a vegetação dos cerrados brasileiros. Itatiaia, Belo Horizonte, pp 1–282
Wharton R, Marsh P, Sharkey M (1997) Manual of the new world genera of the family Braconidae (Hymenoptera). International Society of Hymenopterists p 439
Zwölfer H, Romstöck-Völkl M (1991) Biotypes and the evolution of niches in phytophagous insects on Cardueae hosts. In: Price PW, Lewinsohn TM, Fernandes GW, Benson WW (eds) Plant–animal interactions: evolutionary ecology in tropical and temperate regions. Wiley, New York, p 639
Acknowledgments
We are grateful to various colleagues for their valuable help with field work and to Marina R. Braun, Sérgio Vanin, José R. Mermudes, João Semir, Roberto L. Esteves, and Mara Magenta for providing or confirming identification of insects and plants. This study was supported by FAPESP grant no. 98/05085-2 to TML within the BIOTA-FAPESP Program, no. 04/15482-1 to T.M. Lewinsohn, and no. 03/02541-0 and 06/56889-2 to M. Almeida-Neto. A.R. Nascimento was supported by the CAPES Grant. MAN, CRF, TML, and APD received research productivity grants from CNPq.
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Nascimento, A.R., Almeida-Neto, M., Almeida, A.M. et al. Parasitoid Wasps in Flower Heads of Asteraceae in the Brazilian Cerrado: Taxonomical Composition and Determinants of Diversity. Neotrop Entomol 43, 298–306 (2014). https://doi.org/10.1007/s13744-014-0218-9
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DOI: https://doi.org/10.1007/s13744-014-0218-9