KAPITTEL 6 SENTRALE FUNN OG ANALYSE
6.2.1 Innplassering ansatte
Fêmeas de P. elaesis e T. diatraeae reduzem a imunidade do hospedeiro alternativo, A. gemmatalis. O maior número de parasitóides por pupa provoca uma diminuição no número de hemócitos circulantes na hemolinfa desse hospedeiro alternativo, provavelmente devido a maior injeção de substância tóxica do trato reprodutivo com a oviposição, o que garante um ambiente adequado ao desenvolvimento das formas imaturas do parasitóide. Por outro lado, as idades dos parasitóides e hospedeiro alternativo também influenciam nesta interação.
Palmistichus elaeisis na idade de 72 horas e T. diatraeae com 24 horas possuem
maior propabilidade de sucesso reprodutivo pela maior capacidade de oviposição, indicada pela presença de ovócitos bem formados nos ovários de fêmeas destes parasitóides e maior inibição de hemócitos circulantes na hemolinfa de A. gemmatalis. O envelhecimento pode contribuir com a menor eficiência na produção desses parasitóides, devido a absorção de ovócitos e menor inibição da defesa do hospedeiro. Vale ressaltar que a absorção de ovócitos nesses parasitóides pode ser uma estratégia reprodutiva pela falta de hospedeiros disponíveis ou pela exigência de recursos energéticos. No entanto, a absorção de ovócitos também pode indicar indiretamente uma redução da capacidade dos parasitóides em superar as defesas de seus hospedeiros, sugerindo menor desempenho no parasitismo.
Palmistichus elaeisis e T. diatraeae afetaram a quantidade dos hemócitos do
hospedeiro. Entretanto, a idade do hospedeiro de maneira geral, não influenciou a sua defesa contra o parasitismo através de hemócitos ou encapsulação. Pupas mais novas são melhores para o desenvolvimento de P. elaeisis e T. diatreae em criação em laboratório. Por outro lado, as causa para esse melhor desenvolvimeto não é explicado
pelas análises de número de hemócitos e encapsulação. A semelhança entre o número de hemócitos e encapsulação entre pupas com 24 e 48 horas de idade pode ser respondida pelo custo adaptativo que pupas de A. gemmatalis teriam se fossem utilizados recursos para ativar e manter uma maior produção de células de defesa ou de fatores humorais. A organização dos tecidos e órgãos dessas pupas poderia atuar indiretamente como uma defesa, resultado em menor sucesso reprodutivo de P. elaesisis e T. diatraeae em pupas de A. gemmatalis.
Em conclusão, os parasitóides P. elaeisis e T. diatraeae suplantam a resposta imune do hospedeiro alternativo, A. gemmatalis, quando em maiores densidades e nas idades de maior fecundidade, sem efeito da idade do hospedeiro.
REFERÊNCIAS
Abdel-Latief, M. & M. Hilker. 2007. Innate immunity: eggs of Manduca sexta are able to respond to parasitism by Trichogramma evanescens. Insect Biochemistry and Molecular Biology 38: 136-145.
Amaya, K.E., S. Asgari, R. Jung, M. Hongskula & N.E. Beckage. 2005. Parasitization of Manduca sexta larvae by the parasitoid wasp Cotesia congregate induces an impaired host immune response. Journal of Insect Physiology 51: 505-512. Andrade, G.S., D. Pratissoli, J.B. Torres, R. Barros, L.P. Dalvi & H.B. Zago. 2009.
Parasitismo de ovos de Heliothis virescens por Trichogramma spp. pode ser afetado por cultivares de algodão. Acta Scientiarum. Agronomy 31: 569-573. Andrade, G.S.; Pratissoli, D.; Barros, R.; Zago, H.B. ; Pereira, A.I.A.; Dalvi, L.P.
Screening of two Trichogramma species, native to southeastern Brazil, for the control of tobacco budworm. Revista Colombiana de Entomología, v. 36, n.1, p. 16-19, 2010.
Asgari, S., O. Schmidt & U. Theopold. 1997. A polydnavirus-encoded protein of an endoparasitoid wasp is an immune suppressor. Journal of General Virology 78: 3061-3070.
Asgari, S., U. Theopold, C. Wellby & O. Schmidt. 1998. A protein with protective properties against the cellular defense reactions in insects. Proceedings of the National Academy of Sciences of the United States of America 95: 3690-3695. Bae, S. & Y. Kim. 2004. Host physiological changes due to parasitism of a braconid
wasp, Cotesia plutellae, on diamondback moth, Plutella xylostella. Comparative Biochemistry and Physiology, Part A 138: 39-44.
Barboriak D.P., A.O. Padua, G.E. York & J.R. MacFall. 2005. Creation of DICOM: aware applications using ImageJ. Journal of Digital Imaging 18: 91-99.
Bascuña-Garcia, A.P., C. Lara, A. Córdoba-Aguilar. 2010. Immune investment impairs growth, female reproduction and survival in the house cricket, Acheta domesticus. Journal of Insect Physiology 56: 204-211.
Beck, M., U. Theopold & O. Schmidt. 2000. Evidence for serine protease inhibitor activity in the ovarian calyx fluid of the endoparasitoid Venturia canescens. Journal of Insect Physiology 46: 1275-1283.
Beckage, N.E. & D.B. Gelman. 2004. Wasp parasitoid disruption of host development: implications for new biologically based strategies for insect control. Annual Review of Entomology 49: 299-330.
Bennett, F.D., H. Glenn, M. Yaseen & R.M. Baranowski. 1987. Records of Trichospilus
diatraeae, an Asian parasite (Hymenoptera: Eulophidae) from the Caribbean and
Florida. Florida Entomologist 70: 184-186.
Bodin, A., B. Jaloux, J.P. Delbecque, F. Vannier, J.P. Monge & N. Mondy. 2009. Reproduction in a variable environment: How does Eupelmus vuilleti, a parasitoid wasp, adjust oogenesis to host availability? Journal of Insect Physiology 55: 643-648.
Bodin, A., B. Jaloux, N. Mandon, F. Vannier, J.P. Delbecque, J.P. Monge & N. Mondy. 2007. Host-induced ecdysteroids in the stop-and-go oogenesis in a synovigenic parasitoid wasp. Archives of Insect Biochemistry and Physiology 65: 103-111. Borges, A.R., P.N. Santos, A.F. Furtado & R.C.B.Q. Figueiredo. 2008. Phagocytosis of
latex beads and bacteria by hemocytes of the triatomine bug Rhodnius prolixus (Hemiptera: Reduvidae). Micron 39: 486-494.
Cai, J., G.Y. Ye &C. Hu 2004. Parasitism of Pieris rapae (Lepidoptera: Pieridae) by a pupal endoparasitoid, Pteromalus puparum (Hymenoptera: Pteromalidae): effects of parasitization and venom on host hemocytes. Journal of Insect Physiology 50: 315- 322.
Carton, Y., M. Poirié & A.J. Nappi. 2008. Insect immune resistance to parasitoids. Insect Science 15: 67-87.
Cerenius, L., B.L. Lee & K. Söderhäll. 2008. The proPO-system: pros and cons for its role in invertebrate immunity. Trends in Immunology 29: 263-71.
Chapman RF. 1998. The insects: structure and function. 4 th edition, Elsevier.
Cheng T.C., Y.L. Zhang, C. Liu, P.Z. Xu, Z.H. Gao, Q.Y. Xia & Z.H. Xiang. 2008. Identification and analysis of toll-related genes in the domesticated silkworm,
Bombyx mori. Developmental and Comparative Immunology 32: 464-475.
Cotter S.C., L.E.B. Kruuk & K. Wilson. 2004. Costs of resistance: genetic correlations and potential trade-offs in an insect immune System. Journal of Evolutionary Biology 17: 421-429.
Cullen, R., K.D. Warner, M. Jonsson & S.D. Wratten. 2008. Economics and adoption of conservation biological control. Biological Control 45: 272-280.
Dong, S.Z., G.Y. Ye, P.C. Yao, Y.L. Huang, X.X. Chen, Z.C. Shen & C. Hu 2008. Effects of starvation on the vitellogenesis, ovarian development and fecundity in the ectoparasitoid, Nasonia vitripennis (Hymenoptera: Pteromalidae). Insect Science 15: 429-440.
Er, A., F. Uçkan, D.B. Rivers, E. Ergin & O. Sak. 2010. Effects of parasitization and envenomation by the endoparasitic wasp Pimpla turionellae (Hymenoptera: Ichneumonidae) on hemocyte numbers, morphology, and viability of its host
Galleria mellonella (Lepidoptera: Pyralidae). Annals of the Entomological Society
of America 103: 273-282.
Falabella, P., L. Riviello, M.L. De Stradis, C. Stigliano, P. Varricchio, A. Grimaldi, M. Eguileor, F. Graziani, S. Gigliotti & F. Pennacchio. 2009. Aphidius ervi teratocytes release an extracellular enolase. Insect Biochemistry and Molecular Biology 39: 801-813.
Firlej, A., E. Lucas, D. Coderre & G. Boivin. 2007. Teratocytes growth pattern reflects host suitability in a host – parasitoid assemblage. Physiological Entomology 32: 181–187.
Freitak, D., I. Ots, A. Vanatoa & P. Hõrak. 2003. Immune response isenergetically costly in white cabbage butterfly pupae. Proceedings of the Royal Society B (Suppl.) 270: 220-222.
Gershman S.N., C.A. Barnett, A.M. Pettinger, C.B. Weddle, J. Hunt, S.K. Sakaluk. 2010. Give 'til it hurts: trade-offs between immunity and male reproductive effort in the decorated cricket, Gryllodes sigillatus. Journal of Evolutionary Biology 23: 829-839.
Greene, G.L., N.C. Leppla & W.A. Dickerson. 1976. Velvetbean caterpillar: A rearing procedure and artificial diet. Journal of Economic Entomology 69: 487-488. Greene, G.L., N.C. Leppla & W.A. Dickerson. 1976. Velvetbean caterpillar: A rearing
procedure and artificial diet. Journal of Economic Entomology 69: 487-488.
Hegazi, E. & W. Khafagi. 2008. The effects of host age and superparasitism by the parasitoid, Microplitis rufiventris on the cellular and humoral immune response of
Spodoptera littoralis larvae. Journal of Invertebrate Pathology 98: 79-84.
Hoch G., L. F. Solter & A. Schopf. 2004. Hemolymph melanization and alterations in hemocyte numbers in Lymantria dispar larvae following infections with different
entomopathogenic microsporidia. Entomologia Experimentalis et Applicata 113: 77-86.
Holtz, A.M., A. Pallini, M. Venzon, J.C. Zanuncio, D. Pratissoli, W.F. Barbosa & G.S. Andrade. 2010. Antibiosis of Eucalyptus plants on Podisus nigrispinus. Phytoparasitica 38: 133-139.
Huang, F., M. Shi, Y.Y. Yang, J.Y. Li & X.X. Chen. 2009. Changes in hemocytes of
Plutella xylostella after parasitism by Diadegma semiclausum. Archives of Insect
Biochemistry and Physiology 70: 177-187.
Huebner, E. 1981. Oocyte-follicle cell interaction durign normal oogenesis and atresia in an insect. Journal of Ultrastructural Research 74: 95-104.
Ibrahim, A.M.A. & Y. Kim 2006. Parasitism by Cotesia plutellae alters the hemocyte population and immunological function of the diamondback moth, Plutella
xylostella. Journal of Insect Physiology 52: 943-950.
Ishii, K, H. Hamamoto, M. Kamimura, K. Sekimizu. 2008. Activation of the silkworm cytokine by bacterial and fungal cell wall components via a reactive oxygen species-triggered mechanism. Journal of Biological Chemistry 283: 2185-2191. Jervis, M.A., G.E. Heimpel, P.N. Ferns, J.A. Harvey & N.A.C. Kidd. 2001. Life-history
strategies in parasitoid wasps: a comparative analysis of ‘ovigeny’. Journal of Animal Ecology 70: 442-458.
Jervis, M.A., J. Ellers & J.A. Harvey. 2008. Resources acquisition, allocation, and utilisation in parasitoid reproductive strategies. Annual Review of Entomology 53: 361-385.
Jiravanichpaisal, P., B.L. Lee & K. Söderhäll. 2006. Cell-mediated immunity in arthropods: Hematopoiesis, coagulation, melanization and opsonization. Immunobiology 211: 213-236.
Jonsson, M., S.D. Wratten, D.A. Landis & G.M. Gurr. 2008. Recent advances in conservation biological control of arthropods by arthropods. Biological Control 45: 172-175.
Kaeslin, M, R. Pfister-Wilhelm, D. Molina & B. Lanzrein. 2005. Changes in the haemolymph proteome of Spodoptera littoralis induced by the parasitoid Chelonus
inanitus or its polydnavirus and physiological implications. Journal of Insect
Physiology 51: 975–988.
Lavine, M.D. & M.R. Strand. 2002. Insect hemocytes and their role in immunity. Insect Biochemistry and Molecular Biology 32: 1295-1309.
Li, B. & N. Mills. 2004. The influence of temperature in size as an indicator of host quality for the development of a solitary koinobiont parasitoid. Entomologia Experimentalis et Applicata 110: 249-256.
Li, Y., J.F. Lu, C.J. Feng, X. Ke & W.J. Fu 2007. Role of venom and ovarian proteins in immune suppression of Ostrinia furnacalis (Lepidoptera: Pyralidae) larvae parasitized by Macrocentrus cingulum (Hymenoptera: Braconidae), a polyembryonic parasitoid. Insect Science 14: 93-100.
Lukianchuk, J.L. & S. M. Smith. 1997. Influence of plant structural complexity on the foraging success of Trichogramma minutum: a comparison of search on artificial and foliage models. Entomologia Experimentalis et Applicata 84: 221-228. Mabiala-Moundoungou, A.D.N., G. Doury, P. Eslin, A. Cherqui & G. Prevost. 2010.
Deadly venom of Asobara japonica parasitoid needs ovarian antidote to regulate host physiology. Journal of Insect Physiology 56: 35-41.
Martins, G.F. & J.E. Serrão. 2004. Changes in the reproductive tract of Melipona
quadrifasciata anthidioides (Hymenoptera: Apidae: Meliponini) queen after
Mendel Z., A. Protasov, D. Blumberg, D. Brand, N. Saphir, Z. Madar & J. La Salle. 2007. Release and recovery of parasitoids of the eucalyptus gall wasp Ophelimus
maskelli in Israel. Phytoparasitica 35: 330-332.
Moreira, M.D., M.C.F. Santos, E.B. Beserra, J.B. Torres & R.P. Almeida 2009. Parasitismo e superparasitismo de Trichogramma pretiosum Riley (Hymenoptera: Trichogrammatidae) em ovos de Sitotroga cerealella (Oliver) (Lepidoptera: Gelechiidae). Neotropical Entomology 38: 237-242.
Nadeem S., M.Ashfaq, M. Hamed & S. Ahmed 2010. Optimization of short and long term storage duration for Trichogramma chilonis (Ishii) (Hymenoptera: Trichogrammatidae) at low temperatures. Pakistan Journal of Zoology 42: 63-67. Nalini, M., A.M.A. Ibrahim, I. Hwang & Y. Kim. 2009. Altered actin polymerization of
Plutella xylostella (L.) in response to ovarian calyx components of an
endoparasitoid Cotesia plutellae (Kurdjumov). Physiological Entomology 34: 110-118.
Nappi A.J. & E. Ottaviani. 2000. Cytotoxicity and cytotoxic molecules in invertebrates. Bioessays 22: 469-480.
Nappi, A.J. & B.M. Christensen. 2005. Melanogenesis and associated cytotoxic reactions: applications to insect innate immunity. Insect Biochemistry and Molecular Biology 35: 443-459.
Narayanan, K. 2004. Insect defence: its impact on microbial control of insect pest. Current Science 86: 800-814.
Neto, F.C.M., J.C. Zanuncio, I. Cruz, R.N.C. Guedes & M.C. Picanço. 2005. Progeny production and parasitism by Campoletis flavicincta (Hym.: Ichneumonidae) as affected by female ageing. Biological Agriculture & Horticulture 22: 369-378.
Oliveira, H.N., T.V. Zanuncio, J.C. Zanuncio & J.E. Serrão. 2008. The eucalypt defoliator Thyrinteina arnobia (Lepidoptera: Geometridae) protects its eggs from parasitism. Biological Letters 45: 23-28.
Papaj, D.R. 2000. Ovarian dynamics and host use. Annual Review of Entomology 45: 423-448.
Paranhos, B.J., M.D.Z Costa, S.M. Ovruski, R.M. Alves, L. Blummer & J.M.M. Walderi. 2008. Offspring in response to parental female densities in the fruit fly parasitoid Diachasmimorpha longicaudata (Hymenoptera: Braconidae: Opiinae). Florida Entomologist 91: 628-635.
Paron, M.R., E. Berti-Filho. 2000. Capacidade reprodutiva de Trichospilus diatraeae (Hymenoptera: Eulophidae) em pupas de diferentes hospedeiros (Lepidoptera). Scientia Agricola 57: 355-358.
Pastori P.L., L.B. Monteiro, M. Botton & D. Pratissoli. 2007. Parasitism capacity of
Trichogramma pretiosum Riley (Hymenoptera : Trichogrammatidae) reared under
different temperatures on Bonagota salubricola (Meyrick) (Lepidoptera : Tortricidae) eggs. Neotropical Entomology 36: 926-931.
Pech, L.L. & M.R. Strand, 1996. Granular cells are required for encapsulation of foreign targets by insect haemocytes. Journal of Cell Science 109, 2053–2060. Pennacchio, F. & M.R. Strand. 2006. Evolution of developmental strategies in parasitic
Hymenoptera. Annual Review of Entomology 51: 233-58.
Pereira F.P., R. Barros, D. Pratissoli, J.R.P. Parra. 2004. Biologia e exigências térmicas de Trichogramma pretiosum Riley e T. exiguum Pinto & Platner (Hymenoptera: Trichogrammatidae) criados em ovos de Plutella xylostella (L.) (Lepidoptera: Plutellidae). Neotropical Entomology 33: 231-236.
Pereira, F.F. & J. C. Zanuncio. 2005. Palmistichus elaeisis, uma alternativa de controle para a lagarta parda do eucalipto. Manejo Integrado de Plagas & Agroecologia 76: 89-91.
Pereira, F.F., J.C. Zanuncio, J.E. Serrao, H.N. Oliveira, K. Fávero & E.L.V. Grance 2009. Progênie de Palmistichus elaeisis Delvare & LaSalle (Hymenoptera: Eulophidae) parasitando pupas de Bombyx mori L. (Lepidoptera: Bombycidae) de diferentes idades. Neotropical Entomology 38: 660-664.
Pereira, F.F., J.C. Zanuncio, J.E. Serrão, P.L. Pastori & F.S. Ramalho. 2009. Reproductive performance of Palmistichus elaeisis (Hymenoptera: Eulophidae) with previously refrigerated pupae of Bombyx mori (Lepidoptera: Bombycidae). Brazilian Journal of Biology 69: 865-869.
Pereira, F.F., J.C. Zanuncio, M. T. Tavares, P.L. Pastori, G.C. Jacques & E.F. Vilela. 2008. New record of Trichospilus diatraeae as a parasitoid of the eucalypt defoliator Thyrinteina arnobia in Brazil. Phytoparasitica 36: 304-306.
Pereira, F.F., T.V. Zanuncio, J.C. Zanuncio, D. Pratissoli & M.T. Tavares. 2008. Species of Lepidoptera defoliators of eucalypt as new hosts for the polyphagous parasitoid Palmistichus elaeisis (Hymenoptera: Eulophidae). Brazilian Journal of Biology, 51: 259-262.
Pereira, F.F., J.C. Zanuncio, J.E. Serrão, T.V. Zanuncio, D. Pratissoli & P.L Pastori. 2010. The density of females of Palmistichus elaeisis Delvare and LaSalle (Hymenoptera: Eulophidae) affects their reproductive performance on pupae of
Bombyx mori L. (Lepidoptera: Bombycidae). Anais da Academia Brasileira de
Pfister-Wilhelm, R. & B. Lanzrein. 2009. Stage dependent influences of polydnaviruses and the parasitoid larva on host ecdysteroids. Journal of Insect Physiology 55: 707- 715.
Poirié, M., Y. Carton & A. Dubuffet. 2009. Virulence strategies in parasitoid Hymenoptera as an example of adaptive diversity. Comptes Rendus Biologies 332: 311-320.
Pratissoli D., A.F. Bueno, R.C.O.F. Bueno, J.C. Zanuncio & R.A. Polanczyk. 2009.
Trichogramma acacioi parasitism capacity at different temperatures and factitious
hosts. Revista Brasileira de Entomologia 53: 151-153.
Pratissoli, D., J.C. Zanuncio, U.R. Vianna, J.S. Andrade, T.B.M. Pinon & G.S. Andrade. 2005. Thermal requirements of Trichogramma pretiosum and T. acacioi (Hym.: Trichogrammatidae), parasitoids of the avocado defoliator Nipteria
panacea (Lep.: Geometridae), in eggs of two alternative hosts. Brazilian Archives
of Biology and Technology 48: 523-523.
Pratissoli, D., R.T. Thuler, G.S. Andrade, L.C.M. Zanotti & A.F. Silva. 2005. Estimativa de Trichogramma pretiosum para controle de Tuta absoluta em tomateiro estaqueado. Pesquisa Agropecuária Brasileira 40: 715-718.
Pruijssers, A.J., P. Falabella, J.H. Eum, F. Pennacchio, M.R. Brown & M.R. Strand 2009. Infection by a symbiotic polydnavirus induces wasting and inhibits metamorphosis of the moth Pseudoplusia includens. Journal of Experimental Biology 212: 2998-3006.
Rantala M.J. J. Honkavaara & J. Suhonen. 2010. Immune system activation interacts with territory-holding potential and increases predation of the damselfly Calopteryx
Rantala, M.J & R. Kortet. 2004. Male dominance and immunocompetence in the field cricket (Gryllus bimaculatus). Behavioral Ecology 15: 187-191.
Rantala, M.J. & D.A. Roff. 2007. Inbreeding and extreme outbreeding cause sex differences in immune defence and life history traits in Epirrita autumnata. Heredity 98: 329-336.
Rasband, W.S., ImageJ, U. S. National Institutes of Health, Bethesda, Maryland, USA, http://rsb.info.nih.gov/ij/, 1997-2009.
Reed, D.A., K.A. Luhring, C.A. Stafford, A.K. Hansen, J.G. Millar, L.M. Hanks & T.D. Paine. 2007. Host defensive response against an egg parasitoid involves cellular encapsulation and melanization. Biological Control 41: 214-222.
Renault, S., A. Petit, F. Bénédet, S. Bigot & Y. Bigot. 2002. Effects of the Diadromus
pulchellus ascovirus, DpAV-4, on the hemocytic encapsulation response and
capsule melanization of the leek-moth pupa, Acrolepiopsis assectella. Journal of Insect Physiology 48: 297-302.
Ribeiro, C. & M. Brehélin. 2006. Insect haemocytes: What type of cell is that? Journal of Insect Physiology 52: 417-429.
Richards, E.H. & J.P. Edwards. 2000. Parasitism of Lacanobia oleracea (Lepidoptera) by the ectoparasitoid, Eulophus pennicornis, is associated with a reduction in host haemolymph phenoloxidase activity. Comparative Biochemistry and Physiology B-Biochemistry & Molecular Biology 127: 289-298.
Rosenheim, J.A., S.J. Jepsen, C.E. Matthews, D.S. Smith & M.R. Rosenheim. 2008. Time limitation, egg limitation, the cost of oviposition, and lifetime reproduction by an insect in nature. The American Naturalist 172: 486-496.
Russo, J., M. Brehélin, Y. Carton. 2001. Haemocyte changes in resistant and susceptible strains of D. melanogaster caused by virulent and avirulent strains of the parasitic wasp Leptopilina boulardi. Journal of Insect Physiology 47: 167-172.
Schmid-Hempel, P. 2003. Variation in immune defence as a question of evolutionary ecology. Proceedings of The Royal Society of London Series B-Biological Sciences 270: 357-366.
Schmidt, O.; U. Theopold, N.E. Beckage. Insect and vertebrate immunity: key similarities versus differences. In: Beckage, N.E (Ed.). Insect Immunology, cap. 1, p. 1-23, 2008.
Shelby, K.S. & B.A. Webb. 1999. Polydnavirus-mediated suppression of insect immunity. Journal of Insect Physiology 45: 507-514.
Silva-Torres, C., I.T. Ramos Filho, J. B. Torres & R. Barros. 2009. Superparasitism and host size effects in Oomyzus sokolowskii, a parasitoid of diamondback moth. Entomologia Experimentalis et Applicata 133: 65-73.
Soares, M.A., C.T. Gutierrez, J.C. Zanuncio, R.P.P. Pedrosa & A.S. Lorenzon. 2009. Superparasitismo de Palmistichus elaeisis (Hymenoptera: Eulophidae) y comportamiento de defensa de dos hospederos. Revista Colombiana de Entomología 35: 62-67.
Soares, M.A., G.L.D. Leite, J.C. Zanuncio, S.L. Rocha, V.G.M. Sa, J.E. Serrão. 2007. Flight capacity, parasitism and emergence of five Trichogramma (Hymenoptera: Trichogrammatidae) species from forest areas in Brazil. Phytoparasitica 35: 314- 318.
Souza E. A., C.A. Neves, L.A.O. Campos, J.C. Zanuncio & Serrão, J.E. 2007. Effect of mating delay on the ovary of Melipona quadrifasciata anthidioides (Hymenoptera: Apidae) queens. Micron 38: 471-477.
Souza, D.J., A. Bezier, D. Depoix, J.M. Drezen & A. Lenoir. 2009. Blochmannia endosymbionts improve colony growth and immune defence in the ant Camponotus
fellah. BMC Microbiology 9: 29.
Souza, D.J., J. Van Vlaenderen, Y. Moret & A. Lenoir. 2008. Immune response affects ant trophallatic behaviour. Journal of Insect Physiology 54: 828-832.
Stanley, D.W. & J.S. Miller. 2006. Eicosanoid actions in insect cellular immune functions. Entomologia Experimentalis et Applicata 119: 1-13.
Stefanini, M., C. DeMartino, & L. Zamboni, 1967. Fixation of ejaculated spermatozoa for electron microscopy. Nature 216: 173-174.
Strand M.R. & L.L. Pech. 1995. Immunological basis for compatibility in parasitoid host relationships. Annual Review of Entomology 40: 31-56.
Strand M.R. 2008. The insect cellular immune response. Insect Science 15: 1-14.
Suzuki M. & T. Tanaka. 2007. Development of Meteorus pulchricornis and regulation of its noctuid host, Pseudaletia separata. Journal of Insect Physiology Journal of Insect Physiology 53: 1072-1078.
Tena, A., A. Kapranas, F. Garcia-Mari, & R.F. Luck. 2008. Host discrimination, superparasitism and infanticide by a gregarious endoparasitoid. Animal Behaviour 76: 789-799.
Teramoto, T. & T. Tanaka 2004. Mechanism of reduction in the number of the circulating hemocytes in the Pseudaletia separata host parasitized by Cotesia
kariyai. Journal of Insect Physiology 50: 1103-1111.
Theopold, U., O. Schmidt, K. Söderhäll & M.S. Dushay. 2004. Coagulation in arthropods: defense, wound closure and healing. Trends in Immunology 25: 289- 294.
Uckan, F., S. Sinan, S. Savasci & E. Ergin. 2004. Determination of venom components from the endoparasitoid wasp Pimpla turionellae L. (Hymenoptera: Ichneumonidae). Annals of The Entomological Society of America 97: 775-780. Vainikka, A, M.J. Rantala, O. Seppälä & J. Suhonen. 2007. Do male mealworm beetles,
Tenebrio molitor, sustain the honesty of pheromone signals under immune challenge?
Acta Ethologica 10: 63-72
van Alphen & M.E. Visser. 1990. Superparasitism as an adaptive strategy for insect parasitoids, Annual Review of Entomology 35: 59-79.
Vass, E. & A. J. Nappi. 1998. Prolonged oviposition decreases the ability of the parasitoid Leptopilina boulardi to suppress the cellular immune response of its host Drosophila melanogaster. Experimental Parasitology 89: 86-91.
Vass, E., A.J. Nappi & Y. Carton, 1993. Comparative study of immune competence and host susceptibility in Drosophila melanogaster parasitized by Leptopilina boulardi and Asobara tabida. Journal of Parasitology 79: 106-112.
Wang, X.G., H. Nadel, M.W. Johnson, K.M. Daane, K. Hoelmer, V.M. Walton, C.H Pickett,. & K.R. Sime. 2009. Crop domestication relaxes both top-down and bottom-up effects on a specialist herbivore. Basic and Applied Ecology 10: 216- 227.
Wu M.L., G.Y. Ye, J.Y. Zhu, X.X. Chen & C. Hu. 2008. Isolation and characterization of an immunosuppressive protein from venom of the pupa-specific endoparasitoid
Pteromalus puparum. Journal of Invertebrate Pathology 99:186-191.
Yamamoto, D., R. Henderson, L.S. Corley & K. Iwabuchi. 2007. Intrinsic, inter-specific competition between egg, egg-larval, and larval parasitoids of plusiine loopers. Ecological Entomology 32: 221-228.
Zanuncio, J.C., F.F. Pereira, G.C. Jacques, M.T. Tavares & J.E. Serrão. 2008. Tenebrio
molitor Linnaeus (Coleoptera: Tenebrionidae), a new alternative host to rear the
pupae parasitoid Palmistichus elaeisis Delvare & LaSalle (Hymenoptera: Eulophidae). Coleopterists Bulletin 62: 64-66.
Zhang, G.M., O. Schmidt & S.A. Asgari. 2004. Novel venom peptide from an endoparasitoid wasp is required for expression of polydnavirus genes in host hemocytes. Journal of Biological Chemistry 279: 41580-41585.