Parasitism rate and viability of
Trichogramma maxacalii
(Hym.: Trichogrammatidae) parasitoid of the
Eucalptus
defoliator
Euselasia apison
(Lep.: Riodinidae), on
eggs of
Anagasta kuehniella
(Lep.: Pyralidae)
Harley Nonato de Oliveira
a,*, Jose Cola Zanuncio
a,
Dirceu Pratissoli
b, Ivan Cruz
caDepartamento de Biologia Animal, Universidade Federal de Vic,osa, 36571-000 Vic,osa, Minas Gerais, Brazil bDepartamento de Fitossanidade, Universidade Federal do EspõÂrito Santo, 29500-000 Alegre, EspõÂrito Santo, Brazil
cCNPMS/EMBRAPA, C. Postal 151, 35701-970, Sete Lagoas, Minas Gerais, Brazil
Received 7 January 1999
Abstract
Parasitism rates and viability of individuals of two populations of Trichogramma maxacalii (Hymenoptera: Trichogrammatidae) were evaluated in twoEucalyptusplantations in the Counts of RibeiraÄo Preto, State of SaÄo Paulo and Nova Era, State of Minas Gerais, Brazil. These parasitoids were reared on eggs of the hostAnagasta kuehniella(Lepidoptera: Pyralidae) with or without honey and were exposed to eggs of the host after 0, 6, 12, 24, 36, 48 and 60 h after emergence. Each recently emerged parasitoid female was placed in a 4.0 cm0.7 cm glass tube with a blue 3.5 cm0.5 cm cartoon with 40 glued non-viable eggs ofA.kuehniellaand parasitism was permitted during 24 h. Viability ofT. maxacalii(above 96.0%) was not affected by the presence of food, by the origin of the parasitoid population, or by the period in which it was kept without eggs of the host. However, parasitism rate was higher than 75.0% and lower than 65.0%, for parasitoids with or without honey, respectively. Individuals of the population from SaÄo Paulo showed higher parasitism rates when they received eggs of the host at longer periods after its emergence. Parasitism was higher for the population from Minas Gerais when eggs of the host were provided soon after emergence. Parasitism behaviour in these two populations shows that they can be combined to obtain a better ef®ciency ofT. maxacaliiin programs of mass release againstEuselasia apisaon(Dalman) (Lepidoptera: Riodinidae) in
Eucalyptusplantations.#2000 Elsevier Science B.V. All rights reserved.
Keywords:Trichogrammatidae; Parasitoids;Eucalyptus
1. Introduction
Parasitoids, specially those attacking eggs such as Trichogrammatidae, Scelionidae and Encyrtidae
spe-*Corresponding author.
E-mail address: [email protected] (H.N. de Oliveira)
cies, are important insect biological control agents (Jones, 1988; Lasalle and Gauld, 1993).
TheTrichogrammagenus, with about 100 species and wide geographical distribution, has been used in biological control programs in different cultures against pests in the Lepidoptera, Megaloptera, Coleoptera, Hymenoptera, Neuroptera, Diptera and Heteroptera (Morrison, 1985; Parra et al., 1989).
Studies with Trichogramma in Brazil started in 1946 with the importation and multiplication of Tri-chogramma minutum(Riley) (Hymenoptera: Tricho-grammatidae) against the sugarcane borer Diatraea saccharalis(Fabricius) (Lepidoptera: Pyralidae) (Pra-tissoli, 1986) and substantial progress with species of this genus has followed.
Monitoring of eight Lepidoptera defoliator pests of Eucalyptus in the State of Minas Gerais, Brazil showed that ®ve of them are parasited by Tricho-gramma spp. (Moraes et al., 1983a; Brun et al., 1984). Moraes et al. (1983b) found Trichogramma demoraesi (Nagaraja) and Trichogramma soaresi (Nagaraja) in areas planted withEucalyptus. Voegele and Pointel (1980) describedTrichogramma maxaca-lii in Euselasia euploea eucerus (Hewitson) (Lepi-doptera: Riodinidae). Brun et al. (1984) described Trichogramma manicobai and Trichogramma caia-posi as egg parasitoids of Erinnyis ello (L.) (Lepi-doptera: Sphingidae) and Trichogramma acacioi in eggs of Psorocampa denticulata(Schaus) (Lepidop-tera: Notodontidae). The increase in the number of studies withTrichogrammaled to the description of six species of egg parasitoids ofEucalyptusdefoliators (Pratissoli, 1995).
Factors such as humidity, light and, especially, temperature, can affect the length of the development cycle, sex ratio, longevity and parasitism rate of egg parasitoids (Calvin et al., 1984; Gou, 1988). For this reason, many parameters can be used to select species and/or varieties ofTrichogramma, including parasit-ism rate (Ashley et al., 1974). The objective of this research was to evaluate the parasitism rate of indi-viduals of two populations of the egg parasitoid T. maxacaliiof theEucalyptusdefoliatorEuselasia api-saon(Dalman) (Lepidoptera: Riodinidae). This para-sitoid was maintained with or without honey and received Anagasta kuehniella(Zeller) (Lepidoptera: Pyralidae) eggs at different periods after its emer-gence.
2. Materials and methods
This work was conducted in the Laboratory of `Fitos-sanidade do Centro AgropecuaÂrio da Universidade Fed-eral do EspõÂrito Santo (CAUFES)', in Alegre, State of EspõÂrito Santo, Brazil, with two populations ofT. max-acaliicollected inEucalyptusplantations in the Counts of RibeiraÄo Preto, State of SaÄo Paulo (Population 1) and Nova Era, State of Minas Gerais (Population 2), Brazil in eggs of theEucalyptusdefoliatorE. apisaon.Parasitism rate and viability of individuals of these two populations were studied in eggs of the host A. kuehniella when provided or deprived of honey as food. Additionally, we wanted to test if parasitism rate and viability of T. maxacaliiwas affected by the length of the time until the parasitoid received eggs of this host supplied after 0, 6, 12, 24, 36, 48 and 60 h from emergence. This factorial experiment was conducted in a controlled room with temperature of 2518C, relative humidity of 7010% and photoperiod of 14 h.
Newly emerged T.maxacaliifemales were indivi-dualized in 4.0 cm0.7 cm glass tubes, closed with plastic ®lm. For each of the intervals without exposure to eggs a total of 20 tubes was used, 10 being with food and 10 without food. In each glass tube a female of the parasitoid was placed with a blue 3.5 cm0.5 cm cardboard containing 40 glued eggs ofA.kuehniella collected, glued and turned non-viable with a germi-cidal light applied 50 min before they were offered to the parasitoid. Egg parasitism was allowed during 24 h, after which the cardboard pieces were removed from the tubes. The female parasitoids were main-tained in the tubes to evaluate their longevity. The cardboard with eggs were placed in 23.0 cm4.0 cm closed plastic bags, maintained in the same room, until emergence of the parasitoid brood.
The experiment was set up in a completely rando-mised design, with subdivided blocks, in a 22 factorial (two populations and two feeding types) and subparcels of seven periods (0, 6, 12, 24, 36, 48 and 60 h), with 10 replications. Data were analysed using analysis of variance, `t' test at 5% probability level and regression analysis.
3. Results and discussion
(Table 1). Independent of the time that parasitoids were left without eggs of the host or food its viability ranged from 96.1 to 96.7% in eggs ofA. kuehniella. These values were similar for individuals of both populations of T. maxacalii showing that they are appropriate for mass rearing.
Viability ofT.maxacalii was above 96.0% which can be considered high because Navarro (1993) reported that values above 72.0% in mass rearing facilities ofTrichogrammacan be considered appro-priate. This viability is also higher than that reported by Piao et al. (1992) who obtained 75.3% of adult emergence for several species of this genus.
Viability ofTrichogrammaspecies can be different according to the type of host used because Laing and Eden (1990) showed rates above 89.0% forT. minutum reared withSitrotoga cerealella(Oliv.) (Lepidoptera: Gelechiidae). On the other hand, this parasitoid did not display good viability rates withA. kuehniellaeggs. This same species ofTrichogrammareared by Corri-gan and Laing (1994) in eggs ofLambdina ®scellaria (GueneÂe) (Lepidoptera: Geometridae),Manduca sexta (L.) (Lepidoptera: Sphingidae) orChoristoneura fumi-ferana (Clemens) (Lepidoptera: Tortricidae) showed viability of 85.3, 74.0 and 81.1%, respectively. Finally, Houseweart et al. (1982) found viability of 71.3% for this parasitoid in eggs ofC. fumiferana.
Viability of Trichogramma galloi (Zucchi) was 90.5% in eggs ofD. saccharalis (CoÃnsoli and Parra, 1994); Trichogramma distinctum (Zucchi) showed 80.7 and 31.0% viability in eggs of A. kuehniella
and D. saccharalis, respectively (Lopes and Parra, 1991), while two varieties ofTrichogramma pretiosum (Riley) showed parasitism rate higher than 86.0% in eggs of A. kuehniella (Sa and Parra, 1994). These results show the importance of a good host for mass rearing egg parasitoids and also to develop tests aim-ing to evaluate its viability rate.
Parasitism rate was affected by the presence of food and by the interaction between parasitoid varieties and the time in which adults of T. maxacalii were left without eggs of the host (Table 1). Fed parasitoids displayed signi®cantly higher rate of parasitism (76.91.4%) than non-fed ones (63.11.7%). Overall parasitism rate was 76.9% which represented 30.7 eggs parasited during 24 h for each fed female of T. maxacalii.
Parasitism rates of T. maxacalii were different than that reported by Santa-CecõÂlia et al. (1987) who found no signi®cant differences for this rate for T. demoraesi fed or not with honey, in eggs of A. kuehniella. This shows that parasitism potential is directly related to the species and/or varieties of the parasitoid (Lopes, 1988; Pinto and Tavares, 1992). It also means that it is important to feedT. maxacaliito obtain higher parasitism rates. Besides, parasitism rates of these insects were similar to that found by Tironi (1992), approximately 80.0% forT. pretiosum in eggs of A. kuehniella and higher than that of Lopes and Parra (1991), 42.9% for T. distinctum in eggs of the same host. On the other hand, fed Tricho-gramma buesi (VoegeleÂ) had parasitism rate up to Table 1
Analysis of variance of parasitism rate and viability ofTrichogramma maxacalii(Hymenoptera: Trichogrammatidae) on eggs ofAnagasta kuehniella(Lepidoptera: Pyralidae) at 2518C, 7010% of relative humidity and photophase of 14 h
Source of variation Degrees of freedom Medium square
parasitism rate Viability
Population 1 0.91a 12.93a
Feeding 1 10347.84b 2.96a
PopulationFeeding 1 565.25a 1.22a
Errora 36 339.14 78.40
Time 6 199.73a 87.59a
PopulationTime 6 978.58b 47.99a
FeedingTime 6 513.59a 69.80a
PopulationFeedingTime 6 478.17a 94.44a
Errorb 181 271.15 56.71
36.4% in eggs of Pieris rapae (L.) (Lepidoptera: Pieridae) (Abbas, 1989) showing that a parasitoid can present lower parasitism rate due to its host. It is important to obtain a higher parasitism rate because Navarro (1993) considers that an ideal parasitism rate in mass rearing egg parasitoids in laboratory, in Colombia, should be at least 76.0%.
The interaction between population and time (Table 1, Fig. 1) showed signi®cant differences in the parasitism rate for each population. Such differences are impor-tant for both laboratory and ®eld insects because when combined they can reach a higher parasitism rate of eggs of Lepidoptera pests than the amount they can show alone. On the other hand since such ef®ciency can be affected by the presence of food it is recom-mended to maintain the understorey vegetation under Eucalyptus trees in programs of forest management aiming to increase amount of food and shelter for parasitoids liberated.
higher survival rate in polycultures where they can ®nd larger supply of pollen and nectar.
Parasitism rate of Population 1 increased signi®-cantly with age ofT. maxacaliiadults, but this rate was higher during the ®rst hours after emergence and decreased with time for individuals of Population 2 (Fig. 1). Decreasing parasitism rate with age increase for fed or not egg parasitoids was also reported by Santa-CecõÂlia et al. (1987), but at larger time intervals. This might be due to the fact that these authors worked with T. demoraesi which presents longer longevity thanT. maxacalii.
Parasitism rate by Trichogramma evanescens (Westwood) and Trichogramma brassicae (Bed-zdenko) also decreased, signi®cantly, between 24 and 96 h after their emergence (Fleury and Boule-treau, 1993). Leatemia et al. (1995) found that T. minutum displays higher parasitism rate when it received eggs sooner after its emergence, reaching its highest value (69.6%), during the ®rst 48 h of age. Highest parasitism rate ofTrichogramma atopovirilia (Oatman and Platner) in eggs of Helicoverpa zea (Boddie) (Lepidoptera: Noctuidae) was observed dur-ing the ®rst 24 h, when 22 eggs of this insect were parasited by each female of this parasitoid (Resende and Ciociola, 1995).
Different results for the number of eggs parasited reported in the literature can be related to individual species and also to the geographical origin of the Trichogramma(Lopes and Parra, 1991).
Populations of T. maxacaliifrom RibeiraÄo Preto, State of SaÄo Paulo and of Nova Era, State of Minas Gerais, Brazil can be used for mass production and liberated individually or combined, in programs of biological control ofE. apisaoninEucalyptus planta-tions. Since their parasitism rate are different over time, one population can complement the other if its individuals are liberated, simultaneously. This concept agrees with that reported by other authors, because Hassan (1997) showed that the combination of two parasitoids populations can increase their ef®ciency for pest control.
Acknowledgements
To `Coordenac,aÄo de Aperfeic,oamento de Pessoal de NõÂvel Superior (CAPES)', to `Conselho Nacional de
Desenvolvimento Cientõ®co e TecnoloÂgico (CNPq)' and to `Fundac,aÄo de Amparo a Pesquisa do Estado de Minas Gerais (FAPEMIG)' for grants. To Dr. Rene I. Alfaro, from the Paci®c Forest Research Centre for reviewing the manuscript.
References
Abbas, M.S.T., 1989. Studies on Trichogramma buesi as a biocontrol agent againstPieris rapaein Egypt. Entomophaga 34 (4), 447±451.
Ashley, T.P., Allen, J.C., Gonzales, D., 1974. Successful para-sitization of Heliothis zea and Trichoplusia ni eggs by
Trichogramma. Environ. Entomol. 3 (2), 319±322.
Brun, P.G., Moraes, G.W.G., Soares, L.A., 1984. TreÃs espeÂcies novas de Trichogrammatidae parasitoÂides de lepidoÂpteros desfolhadores de mandioca e eucalipto. Pesq. Agropec. Bras. 19 (7), 805±810.
Calvin, D.D., Knapp, M.C., Welch, S.M., 1984. Impact of environmental factors onTrichogramma pretiosum reared on Southwestern corn borer eggs. Environ. Entomol. 13 (3), 774± 780.
CoÃnsoli, F.L., Parra, J.R.P., 1994. Efeito do fotoperõÂodo na biologia deTrichogramma galloi Zucchi. An. Soc. Entomol. Bras. 23 (3), 467±472.
Corrigan, J.D., Laing, J.E., 1994. Effects of the rearing host species and the host species attacked on performance byTrichogramma minutum Riley (Hymenoptera: Trichogrammatidae). Environ. Entomol. 23 (3), 755±760.
Fleury, F., Bouletreau, M., 1993. Effects of temporary host deprivation on the reproductive potential of Trichogramma brassicae. Entomol. Exp. Appl. 68, 203±210.
Gou, X., 1988. Bionomics of Trichogramma ostriniae Pang et Chang. In: Proceedings of International Symposium on Trichogramma and other egg parasitoids, vol. 2, 1986, Ghangzhou, INRA, Paris, pp. 191±195.
Hassan, S.A., 1997. Selec,aÄo de espeÂcies deTrichogrammapara uso em programas de controle bioloÂgico. In: Parra, J.R.P., Zucchi, R.A. (Eds.), Trichogrammae o controle bioloÂgico aplicado, FEALQ, Piracicaba, pp. 183±205.
Houseweart, M.W., Southard, S.G., Jennings, D.T., 1982. Avail-ability and acceptAvail-ability of spruce budworm to parasitism by the egg parasitoid, Trichogramma minutum (Hym.: Tricho-grammatidae). Can. Entomol. 114 (8), 657±666.
Jones, W.A., 1988. A world review of the parasitoids for the Southern green stink bug, Nezara viridula (L.) (Hetero-ptera: Pentatomidae). Ann. Entomol. Soc. Am. 81 (2), 262± 273.
Laing, J.E., Eden, G.M., 1990. 2.0 Mass-production of Tricho-gramma minutumRiley on factitious host eggs. Mem. Entomol. Soc. Can. 153, 10±24.
Leatemia, J.A., Laing, J.E., Corrigan, J.E., 1995. Production of exclusively male progeny by mated, honey-fedTrichogramma minutumRiley (Hym., Trichogrammatidae). J. Appl. Entomol. 119 (8), 561±566.
Lopes, J.R.S., Parra, J.R.P., 1991. Efeito da idade de ovos do hospedeiro natural e alternativo no desenvolvimento e parasitismo de duas espeÂcies deTrichogramma. Rev. Agric. 66 (3), 221±244. Lopes, J.R.S., 1988. Estudos bioetoloÂgicos deTrichogramma galloi
Zucchi, 1988 (Hym.: Trichogrammatidae) para o controle de
Diatraea saccharalis(Fabr., 1794) (Lep.: Pyralidae). ESALQ, Piracicaba, 141 pp. (Tese M.S.)
Moraes, G.W.G., Brun, P.G., Soares, L.A., 1983a. O controle bioloÂgico dos lepidoÂpteros desfolhadores de eucaliptos em Minas Gerais. Inf. Agrop. 9 (104), 23±30.
Moraes, G.W.G., Brun, P.G., Soares, L.A., 1983b. Insetos x insetos; nova alternativa para o controle de pragas. CieÃncia Hoje 6 (1), 70±77.
Morrison, R.K., 1985. Trichogrammaspp. In: Singh, P., Moore, R.F. (Eds.). Handbook of Insect Rearing, vol. 1, Elsevier, Amsterdam, pp. 413±417.
Navarro, M.A., 1993. ProduccõÂon, uso y manejo en Colombia, El
Trichogrammaspp., Palmira, ICA, 184 pp.
Parra, J.R.P., Lopes, J.R.S., Serra, H.J.P., Zucchi, R.A., 1989. Metodologia de criac,aÄo deAnagasta kuehniella(Zeller, 1879) para produc,aÄo massal de Trichogramma spp.. An. Soc. Entomol. Bras. 18 (2), 403±415.
Piao, Y.F., Lin, H., Shi, G.R., 1992. Quality control of the physique of mass-rearedTrichogramma. Plant Protection 18 (3), 28±29. Pinto, F., Tavares, J., 1992. Longevity and parasitic capacity of the Azorean type ofTrichogramma cordubensis Vargas; Cabello (Hym., Trichogrammatidae). In: Proceeding of International Symposium on Trichogramma and other egg parasitoids, vol. 3, San Antonio, INRA, Paris, pp. 89±91.
Pratissoli, D., 1986. Seletividade de treÃs espeÂcies deTrichogramma
a ovos esteÂreis de lepidoÂpteros em condic,oÄes de laboratoÂrio ESAL Lavras, 77 pp. (Tese M.S.)
Pratissoli, D., 1995. Bioecologia de Trichogramma pretiosum
Riley, 1879 nas trac,as Scrobipalpuloides absoluta (Meyrick, 1917) ePhthorimaea operculella(Zeller, 1873) em tomateiro. ESALQ, Piracicaba, 135 pp. (Tese D.S.)
Resende, D.L.M.C., Ciociola, A.I., 1995. Capacidade de para-sitismo de Trichogramma atopovirilia Oatman; Platner, 1983 (Hymenoptera: Trichogrammatidae) em ovos de Helicov-erpa zea (Boddie, 1850) (Lepidoptera: Noctuidae) em difer-entes temperaturas. Cienc. e Agrotec. Lavras 20 (4), 421± 424.
Risch, S.J., 1981. Insect herbivore abundance in tropical mono-cultures and polymono-cultures: an experimental test of two hypotheses. Ecology 62, 1325±1340.
SaÂ, L.A., Parra, J.R.P., 1994. Biology and parasitism of
Trichogramma pretiosum Riley (Hym., Trichogrammatidae) onEphestia kuehniella(Zeller) (Lep., Pyralidae) andHeliothis zea(Boddie) (Lep., Noctuidae) eggs. J. Appl. Ent. 118, 38± 43.
Santa-CecõÂlia, L.V.C., Matioli, J.C., Sousa, B., 1987. Aspectos da biologia de Trichogramma demoraesi Nagaraja, 1983 e contribuic,oÄes ao manejo de criac,oÄes massais deste parasitoÂide em ovos de Anagasta kuehniella (Zeller, 1879). An. E.S.A. ``Luiz de Queiroz'' 44, 1607±1625.
Tironi, P., 1992. Aspectos bioecoloÂgicos de Trichogramma pretiosum Riley, 1879 eTrichogramma atopovirilia Oatman; Platner, 1983 (Hym.: Trichogrammatidae), como agentes de controle bioloÂgico deHelicoverpa zea(Boddie, 1850) (Lep.: Noctuidae). ESAL, Lavras, 74 pp. (Tese M.S.)
VoegeleÂ, J., Pointel, J.G., 1980. Une nouvelle espeÁce de Trichogramme,Trichogramma maxacalii(Hym., Trichogram-matidae). Ann. Soc. Ent. Fr. 16 (5), 599±603.
