Effect of temperature on immatures of Stiretrus decastigmus (Hemiptera: Pentatomidae)

Efeito da temperatura sobre imaturos de Stiretrus decastigmus (Hemiptera: Pentatomidae)

S. Poncio S. T. B. Dequech A. Bolzan C. Güths M. P. Walker V. S. Sturza D. E. Nava About the authors

Abstract

Stiretrus decastigmus (Herrich-Schaeffer) (Hemiptera: Pentatomidae) is an important predator of the insect pest Microtheca ochroloma Stal (Coleoptera: Chrysomelidae). The present study investigated the pre-imaginal development of S. decastigmus at different temperatures. The temperatures were: 20, 25, and 30 °C, with a relative humidity of 70 ± 10% and a photofase of 12 h, and the nymphs were fed larvae of M. ochroloma. We evaluated the duration and viability of the egg and nymphal stages, the duration of each instar, and the predation potential. The incubation time decreased with increasing temperature, and the viability was highest at 25 °C. The duration of the nymphal stage was inversely proportional to the temperature, ranging from 18 days at 30 °C to 40.6 days at 20 °C. The highest S. decastigmus predation rates were found at 20 °C (90.4 larvae) and 30 °C (72.5 larvae). S. decastigmus showed the highest viability and lowest consumption of larvae of M. ochroloma at 25 °C.

Keywords:
Asopinae; Chrysomelidae; biological control; predator

Resumo

Stiretrus decastigmus (Herrich-Schaeffer) (Hemiptera: Pentatomidae) é um importante predador do inseto-praga Microtheca ochroloma Stal (Coleoptera: Chrysomelidae). O objetivo deste trabalho foi estudar o desenvolvimento pré-imaginal de S. decastigmus em diferentes temperaturas. Foram utilizadas as temperaturas de 20, 25, e 30 °C, umidade relativa do ar de 70 ± 10% e fotofase de 12 h, sendo as ninfas alimentadas com larvas de M. ochroloma. Foram avaliados a duração e viabilidade dos estágios de ovo e ninfa, a duração de cada instar e o potencial de predação. O período de incubação diminuiu com o aumento da temperatura e apresentou maior viabilidade a 25 °C. A duração do estágio ninfal foi inversamente proporcional a temperatura com 18 dias a 30 °C e 40,6 dias a 20 °C. A maior taxa de predação de S. decastigmus foi encontrada a 20 °C (90,4 larvas) e 30 °C (72,5 larvas). S. decastigmus teve maior viabilidade e menor consumo de larvas de M. ochroloma a 25 °C.

Palavras-chave:
Asopinae; Chrysomelidae; controle biológico; predador

1 Introduction

Production of vegetables such as species of Brassicaceae is an excellent option for family farms, especially in organic systems (Pinto et al., 2001Pinto, C.M.F., Pereira, J.M. and Paula JUNIOR, T.J., 2001. Agricultura alternativa no contexto mundial. Informe Agropecuário, vol. 22, no. 212, pp. 80-83.). However, the plants are attacked by the insect pest Microtheca ochroloma Stal (Coleoptera: Chrysomelidae), which defoliates the plants during both its larval and adult stages (Fasulo, 2005Fasulo, T.R., 2005 [viewed 23 March 2012]. Yellowmargined leaf beetle, Microtheca ochroloma Stål [online]. Florida: Institute of Food and Agricultural Sciences, University of Florida. EENY-348. Available from: http://edis.ifas.ufl.edu/pdffiles/IN/IN62500.pdf
http://edis.ifas.ufl.edu/pdffiles/IN/IN6...
). The impacts of this pest on crops is well documented in South America, where it is indigenous, and in North America (Ameen and Story, 1997Ameen, A.O. and Story, R.N., 1997. Fecundity and longevity of the yellowmargined leaf beetle (Coleoptera: Chrysomelidae) on crucifers. Journal of Agricultural Entomology, vol. 14, no. 1, pp. 157-162.). The extent of the damage may impel farmers, especially organic producers, to avoid cultivating Brassicaceae (Dequech et al., 2008Dequech, S.T.B., Sausen, C.D., Lima, C.G. and Egewarth, R., 2008. Efeito de extratos de plantas com atividade inseticida no controle de Stal (Col.: Chrysomelidae), em laboratório. Microtheca ochrolomaRevista Biotemas, vol. 21, no. 1, pp. 41-46.).

As an alternative to chemical pesticides, biological control using natural enemies has been increasing in importance in integrated pest management programs (IPM), especially to promote sustainability of agriculture (Parra et al., 2002Parra, J.R.P., Botelho, P.S., Corrêa-Ferreira, B.S. and Bento, J.M.S., 2002. Controle biológico: uma visão inter e multidisciplinar. In: J.R.P. PARRA, P.S. BOTELHO, B.S. CORRÊA-FERREIRA and J.M.S. BENTO, eds. Controle biológico no Brasil: parasitoides e predadores. São Paulo: Manole, pp. 125-142.).

The natural enemy of Microtheca species, Stiretrus decastigmus (Herrich-Schaeffer) (Hemiptera: Pentatomidae), has been recorded in the state of Rio Grande do Sul, southern Brazil, preying on larvae and adults of M. ochroloma (Poncio et al., 2010Poncio, S., Dequech, S.T.B., Sturza, V.S., Lissner, R.A.D., Perlin, L.F., Rosalino, P.K. and Ribeiro, L.P., 2010. Primeiro relato de Stiretrus decastigmus no Brasil predando Microtheca ochroloma.Ciência Rural, vol. 40, no. 5, pp. 1203-1205. http://dx.doi.org/10.1590/S0103-84782010005000069.
http://dx.doi.org/10.1590/S0103-84782010...
) and M. semilaevis Stal (Sturza et al., 2012Sturza, V.S., Poncio, S., Dorfey, C., Dequech, S.T.B., Bolzan, A. and Walker, M., 2012. Ocurrence of Herrich-Schaeffer (Hemiptera: Pentatomidae) preying . Stiretrus decastigmusMicrotheca semilaevis Stal (Coleoptera: Chrysomelidae)Neotropical Entomology, vol. 41, no. 1, pp. 81-82. http://dx.doi.org/10.1007/s13744-011-0013-9. PMid:23950015.
http://dx.doi.org/10.1007/s13744-011-001...
). However, little is known of the biology of this predator, a promising agent for biological control programs targeting this pest. In order to implement biological control, it is necessary to determine the effects of abiotic factors on the development of the predator. The present study examined the effect of different temperatures on the pre-imaginal development of S. decastigmus, with a view toward rearing the species in the laboratory for the purpose of biological control of M. ochroloma.

2 Material and Methods

2.1 Establishment and rearing of Microtheca ochroloma

Adults of M. ochroloma were collected from plots of Chinese cabbage (Brassica chinensis L.) (Brassicaceae) at the Universidade Federal de Santa Maria (UFSM) in the state of Rio Grande do Sul, municipality of Santa Maria, southern Brazil (29° 43’ 28” S, 53° 43’ 19” W, altitude: 95 m). The adults were kept in rearing cages (transparent plastic boxes measuring 30 × 30 × 20 cm), with mesh sides and cover) and fed with Chinese cabbage leaves pre-washed in running water. Water was provided to the insects by capillary action through cotton dental rolls that were placed in plastic containers containing 100 mL of water and changed every two days. The egg masses were removed from the leaves and placed in Petri dishes (diameter = 8.5 cm) with their bottoms covered with filter paper. The larvae from these egg masses were kept in cages similar to those used for adults, but smaller (17.7 × 26.2 × 14.7 cm), and were also fed with leaves of Chinese cabbage, which were replaced daily. After the adults emerged, they were transferred to the larger cages for mating. Part of the insects, in various stages of development, were used to maintain the rearing stock, and part were used for the experiments. The creations were maintained at 23 °C, with a relative humidity of 70 ± 10% and a photofase of 12 h.

2.2 Establishment and rearing of Stiretrus decastigmus

Nymphs and adults of S. decastigmus were collected from plots of Chinese cabbage (Brassica chinensis L.) (Brassicaceae) at the UFSM. The insects were taken to the laboratory and kept in cages (17.7 × 26.2 × 14.7 cm). Their eggs were removed daily and kept in Petri dishes (diameter = 8.5 cm) with the bottoms covered with filter paper moistened with distilled water, until they reached the second instar. The nymphs were then transferred to breeding cages (17.7 × 26.2 × 14.7 cm) because they begin to predate in this stage. Larvae and/or adults of M. ochroloma were used as prey for S. decastigmus nymphs and adults, in laboratory rearing. The creations were maintained at 23 °C, with a relative humidity of 70 ± 10% and a photofase of 12 h.

2.3 Effect of temperature on the immatures of Stiretrus decastigmus

Biological parameters of S. decastigmus were evaluated at temperatures of 20, 25 and 30 °C. Forty eggs of this predator were used per temperature, in a Petri dish (9.0 cm diameter × 1.5 cm height) lined with filter paper moistened with distilled water to reduce egg dehydration. At each temperature, 20 second-instar nymphs were placed in individual cages prepared from plastic pots (350 mL). The experiments began with second-instar nymphs, because the first-instar nymphs do not feed (Zanuncio et al., 1991Zanuncio, J.C., Nascimento, E.C., Santos, G.P. and Araújo, F.S., 1991. Aspectos biológicos do predador (Bergroth, 1891) (Hemiptera: Pentatomidae). Podisus connexivusAnais da Sociedade Entomológica do Brasil, vol. 20, no. 2, pp. 243-249.; Silva et al., 1996Silva, E.N., Santos, T.M. and Ramalho, F.S., 1996. Desenvolvimento ninfal de Stal (Hemiptera: Pentatomidae) alimentado com curuquerê-do-algodoeiro. Supputius cincticepsAnais da Sociedade Entomológica do Brasil, vol. 25, no. 2, pp. 103-108.; Wanderley and Ramalho, 1999Wanderley, M.J.A. and Ramalho, F.S., 1999. Efeitos da temperatura no desenvolvimento de (Stäl) (Heteroptera: Pentatomidae) alimentado com larvas de L. Supputius cincticepsMusca domesticaAnais da Sociedade Entomológica do Brasil, vol. 28, no. 1, pp. 121-129. http://dx.doi.org/10.1590/S0301-80591999000100013.
http://dx.doi.org/10.1590/S0301-80591999...
). The upper opening was closed with voile fabric to allow aeration. An acrylic container (2.5 cm diameter × 4.5 cm height) was placed inside the cage, containing moistened cotton dental rolls to supply water. The nymphs were fed with third- and fourth-instar M. ochroloma larvae, offered to the nymphs in similar proportions ad libitum, and the larvae were left inside the cage until the nymphs reached the final instar.

The duration and survival of the embryo and nymphal stages, the number and duration of instars, the total life-cycle duration, and the number of prey consumed were assessed. The duration and survival were determined daily, when nymph hatching was recorded. The number and durations of instars were determined based on the interval between ecdyses, determined by the presence of molts in the rearing container. The total duration of the nymphal stage was taken as the sum of the duration of each nymphal stage. The overall life cycle was the sum of the durations of the egg and nymphal stages.

2.4 Data analysis

The experiments used a fully randomized design with 20 replications. Data normality was checked with Shapiro-Wilk’s test (k samples) before analysis of variance (ANOVA); means were compared using Tukey’s test (α = 0.05). The ASSISTAT 7.5 Beta (2008) software was used (Silva, 1996Silva, F.A.S., 1996. FASE: the ASSISTAT Software: statistical assistance. In: Proceedings of the 6th International Conference on Computers in Agriculture, 1996, Cancun, Mexico. Cancun: American Society of Agricultural Engineers, pp. 246-298.).

3 Results

The incubation period of S. decastigmus was inversely proportional to the temperature, i.e., 5.00 and 13.66 days at 30 and 20 °C, respectively (d.f. = 2; F = 127.5851; P < 0.001). Eggs kept at 25 °C had the highest survival, and more individuals reached the nymphal stage (95%). At this temperature, the egg incubation period of 8.57 days was intermediate between those at the other temperatures.

The temperature also affected the duration of all nymphal instars (Table 1). Nymphs kept at 20 °C had a longer instar duration than those at 25 and 30 °C. The duration of the final instar was longer at all temperatures. The duration of the nymphal stage varied from 18.00 days at 30 °C to 40.60 days at 20 °C (d.f. = 2; F = 174.4424; P < 0.001). Nymphal survival was highest (85.00%) at 25 °C, lasting 22.70 days, whereas at 20 and 30 °C the duration was 18.0 and 40.6 days, with survival rates of 25 and 20% respectively. The total life cycle of S. decastigmus lasted 23.0, 32.2, and 54.0 days at 30, 25, and 20 °C, respectively (d.f. = 2; F = 215.9122; P < 0.001). The predation rate of S. decastigmus was highest at 20 °C, when each predator nymph preyed on a mean of 90.40 M. ochroloma larvae (d.f. = 3; F = 38.0827; P < 0.001) (Table 2). At all temperatures, consumption was proportional to the increase in size of the nymphs, i.e., the older nymphs consumed more prey (Table 2).

Table 1
Duration (days) of nymphal instars (mean ± SE) and survival of Stiretrus decastigmus (Hemiptera: Pentatomidae) fed on Microtheca ochroloma (Coleoptera: Chrysomelidae) larvae at 20, 25, and 30 °C.
Table 2
Larval consumption (mean ± SE) per instar and total consumption of Microtheca ochroloma (Coleoptera: Chrysomelidae) larvae by the Stiretrus decastigmus (Hemiptera: Pentatomidae) nymph stage fed at 20, 25, and 30 °C.

4 Discussion

The embryonic period of S. decastigmus was relatively long for rearing purposes; the duration of 8.57 days at 25 °C is longer than those reported for other members of Pentatomidae such as Podisus nigrispinus (Dallas) (4.00 days) (Vacari et al., 2007Vacari, A.M., Otuka, A.K. and De-Bortoli, A.S., 2007. Desenvolvimento de (Fabricius, 1794) (Lepidoptera: Crambidae). Podisus nigrispinus (Dallas, 1851) (Hemiptera: Pentatomidae) alimentado com lagartas de Diatraea saccharalisArquivos do Instituto Biológico, vol. 74, no. 3, pp. 259-265.), Podisus distinctus (Dallas) (5.20 days) (Santos et al., 2004Santos, G.P., Zanuncio, T.V., Ribeiro, G.T., Da Silva, E.P. and Zanuncio, J.C., 2004. Influência da temperatura no desenvolvimento ninfal de Podisus distinctus (Dallas) (Heteroptera: Pentatomidae). Revista Cerne, vol. 10, no. 2, pp. 213-221.) and Brontocoris tabidus (Signoret) (3.50 days) (Fernandes et al., 1996Fernandes, L.G., Carvalho, C.F., BUENO, V.H.P. and DINIZ, L.C., 1996. Aspectos biológicos de Brontocoris tabidus Signoret, 1852 e . Podisus nigrispinus Dallas (Hemiptera: Pentatomidae)Revista Cerne, vol. 2, no. 1, pp. 1-10.) and 5.60 days (Jusselino-Filho et al., 2003Jusselino-Filho, P., Zanuncio, J.C., Fragoso, D.B., Serrão, J.E. and Lacerda, M.C., 2003. Biology of (Heteroptera: Pentatomidae) fed with . Brontocoris tabidusMusca domestica (Diptera: Muscidae) larvaeBrazilian Journal of Biology = Revista Brasileira de Biologia, vol. 63, no. 3, pp. 463-468. http://dx.doi.org/10.1590/S1519-69842003000300012. PMid:14758705.
http://dx.doi.org/10.1590/S1519-69842003...
). However, S. decastigmus showed higher survival for the embryonic period than these other predators. Probably longer periods of embryonic development is a characteristic of this species, because when the temperature was high, although this period decreased, it was still longer than those reported for other members of Pentatomidae at lower temperatures (Fernandes et al., 1996Fernandes, L.G., Carvalho, C.F., BUENO, V.H.P. and DINIZ, L.C., 1996. Aspectos biológicos de Brontocoris tabidus Signoret, 1852 e . Podisus nigrispinus Dallas (Hemiptera: Pentatomidae)Revista Cerne, vol. 2, no. 1, pp. 1-10.; Jusselino-Filho et al., 2003Jusselino-Filho, P., Zanuncio, J.C., Fragoso, D.B., Serrão, J.E. and Lacerda, M.C., 2003. Biology of (Heteroptera: Pentatomidae) fed with . Brontocoris tabidusMusca domestica (Diptera: Muscidae) larvaeBrazilian Journal of Biology = Revista Brasileira de Biologia, vol. 63, no. 3, pp. 463-468. http://dx.doi.org/10.1590/S1519-69842003000300012. PMid:14758705.
http://dx.doi.org/10.1590/S1519-69842003...
; Santos et al., 2004Santos, G.P., Zanuncio, T.V., Ribeiro, G.T., Da Silva, E.P. and Zanuncio, J.C., 2004. Influência da temperatura no desenvolvimento ninfal de Podisus distinctus (Dallas) (Heteroptera: Pentatomidae). Revista Cerne, vol. 10, no. 2, pp. 213-221.; Vacari et al., 2007Vacari, A.M., Otuka, A.K. and De-Bortoli, A.S., 2007. Desenvolvimento de (Fabricius, 1794) (Lepidoptera: Crambidae). Podisus nigrispinus (Dallas, 1851) (Hemiptera: Pentatomidae) alimentado com lagartas de Diatraea saccharalisArquivos do Instituto Biológico, vol. 74, no. 3, pp. 259-265.).

As noted by Coursey and Esselbaugh (1962)Coursey, R.M. and Esselbaugh, C.O., 1962. Descriptions of the nymphal stages of some North American Pentatomidae (Hemiptera: Heteroptera). Annals of the Entomological Society of America, vol. 55, no. 3, pp. 323-342. http://dx.doi.org/10.1093/aesa/55.3.323.
http://dx.doi.org/10.1093/aesa/55.3.323...
, pentatomids typically have five instars. The number of instars of S. decastigmus was not affected by the temperature, since the nymphs passed through five instars at all temperatures tested. However, the temperature was a determining factor in the duration of all nymphal instars. For nymphs exposed to temperatures of 20 °C the duration of each instar was longer, and shorter durations predominated in nymphs exposed to 30 °C.

The survival of S. decastigmus nymphs at 25 °C was higher than that of P. nigrispinus reared on Tenebrio molitor L. (Coleoptera: Tenebrionidae) (68%) and Spodoptera frugiperda (J.E. Smith) (Lepidoptera: Noctuidae) (64%) (Oliveira et al., 2004Oliveira, H.N.D., Pratissoli, D., Pedruzzi, E.P. and Espindula, M.C., 2004. Desenvolvimento do predador Podisus nigrispinus alimentado com e Spodoptera frugiperdaTenebrio molitor.Pesquisa Agropecuária Brasileira, vol. 39, no. 10, pp. 947-951. http://dx.doi.org/10.1590/S0100-204X2004001000001.
http://dx.doi.org/10.1590/S0100-204X2004...
), and of P. distinctus reared on Musca domestica (L.) (Diptera: Muscidae) larvae (60%) (Lacerda et al., 2004Lacerda, M.C., Ferreira, A.M.R.M., Zanuncio, T.V., Zanuncio, J.C., Bernardino, A.S. and Espindula, M.C., 2004. Development and reproduction of (Heteroptera: Pentatomidae) fed on larva of . Podisus distinctusBombyx mori (Lepidoptera: Bombycidae)Brazilian Journal of Biology = Revista Brasileira de Biologia, vol. 64, no. 2, pp. 237-242. http://dx.doi.org/10.1590/S1519-69842004000200008. PMid:15462296.
http://dx.doi.org/10.1590/S1519-69842004...
), and T. molitor (76%) (Santos et al., 2004Santos, G.P., Zanuncio, T.V., Ribeiro, G.T., Da Silva, E.P. and Zanuncio, J.C., 2004. Influência da temperatura no desenvolvimento ninfal de Podisus distinctus (Dallas) (Heteroptera: Pentatomidae). Revista Cerne, vol. 10, no. 2, pp. 213-221.). This difference may be related to food quality, since S. decastigmus was fed on prey that, despite being laboratory-reared, is natural; while the studies of these other predators used prey reared on artificial diets.

The nymphal period of 20 days at 25 °C found for S. decastigmus fed with M. ochroloma larvae indicates that this prey species may be appropriate for rearing this predator, because they provide suitable nutritional resources for its development, as reported for another pentatomid predator (Oliveira et al., 2004Oliveira, H.N.D., Pratissoli, D., Pedruzzi, E.P. and Espindula, M.C., 2004. Desenvolvimento do predador Podisus nigrispinus alimentado com e Spodoptera frugiperdaTenebrio molitor.Pesquisa Agropecuária Brasileira, vol. 39, no. 10, pp. 947-951. http://dx.doi.org/10.1590/S0100-204X2004001000001.
http://dx.doi.org/10.1590/S0100-204X2004...
). Since at these temperatures the prey consumption was lowest, this translates to a reduction in production costs. The larger number of prey consumed at 20 °C is related to the longer developmental period at this temperature, since nymphs that take longer to develop require more food. However, this relationship did not obtain at the higher temperature (30 °C), where the development time was reduced; however, the number of prey consumed was higher than that consumed by nymphs kept at 25 °C. Possibly this is related to the accelerated metabolism at higher temperatures, causing the insects to require more energy to reach the next stage.

The total life-cycle duration of S. decastigmus is similar to that of S. cincticeps at 25 °C fed on M. domestica (30.2 days) and T. molitor (30.5 days) (Zanuncio et al., 1992Zanuncio, T.V., Zanuncio, J.C., Vilela, E.F. and Sartório, R.C., 1992. Aspectos biológicos da fase adulta de Stal, 1860 (Hemiptera: Pentatomidae), predador de lagartas desfolhadoras de eucalipto. Supputius cinsticepsInstituto de Pesquisas e Estudos Florestais, vol. 45, no. 1, pp. 35-39.).

The number of M. ochroloma larvae predated by S. decastigmus was higher than that of P. nigrispinus in the laboratory at 28 ± 1 °C, 53 ± 5% RH and a photophase of 14 h, which was 43.10 larvae of Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae) (Vivan et al., 2002Vivan, L.M., Torres, J.B., Veiga, A.F.S.L. and Zanuncio, J.C., 2002. Comportamento de predação e conversão alimentar de . Podisus nigrispinus sobre a traça-do-tomateiroPesquisa Agropecuária Brasileira, vol. 37, no. 5, pp. 581-587. http://dx.doi.org/10.1590/S0100-204X2002000500002.
http://dx.doi.org/10.1590/S0100-204X2002...
) and 15.2 larvae of Plutella xylostella (L.) (Lepidoptera: Pyralidae) at 25 ± 1 °C, 70 ± 10% RH, and a photophase of 12 h (Xavier et al., 2009Xavier, M.R., De-Bortoli, A.S., Vacari, A.M., Laurentis, V.L. and Magalhães, G.O., 2009. Aspectos biológicos e tabela de vida de nigrispinusPlutella (L., 1758) em folha de couve ( . In: Podisus (DALLAS, 1851) alimentado com lagartas de xylostellaBrassicaoleracea L.)Anais do XXI Congresso de Iniciação Científica da Unesp, 2009, Jaboticabal, São Paulo. Jaboticabal: UNESP, pp. 557-560.). This larger amount of prey consumed is likely related to their size and to the amount of nutrients contained, since the larvae of M. ochroloma are smaller than the prey used by these investigators.

In summation, for the purpose of laboratory rearing with a view toward optimizing the production of predators, the temperature of 25 °C was optimum for nymphal development of S. decastigmus, as shown by their higher survival rate and lower consumption of M. ochroloma larvae. With respect to the use of S. decastigmus for the purpose of biological control under field conditions, lower rearing temperatures lead to a higher consumption of larvae and a longer nymphal developmental period.

Acknowledgements

Ayres Menezes de Oliveira Jr. of the “Universidade Estadual de Londrina” for identifying Microtheca, and Aline Barcellos Prates dos Santos from the “Museu de Ciências Naturais da Fundação Zoobotânica do Rio Grande do Sul” for the identification of S. decastimus. The Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) provided a scholarship.

References

  • Ameen, A.O. and Story, R.N., 1997. Fecundity and longevity of the yellowmargined leaf beetle (Coleoptera: Chrysomelidae) on crucifers. Journal of Agricultural Entomology, vol. 14, no. 1, pp. 157-162.
  • Coursey, R.M. and Esselbaugh, C.O., 1962. Descriptions of the nymphal stages of some North American Pentatomidae (Hemiptera: Heteroptera). Annals of the Entomological Society of America, vol. 55, no. 3, pp. 323-342. http://dx.doi.org/10.1093/aesa/55.3.323
    » http://dx.doi.org/10.1093/aesa/55.3.323
  • Dequech, S.T.B., Sausen, C.D., Lima, C.G. and Egewarth, R., 2008. Efeito de extratos de plantas com atividade inseticida no controle de Stal (Col.: Chrysomelidae), em laboratório. Microtheca ochrolomaRevista Biotemas, vol. 21, no. 1, pp. 41-46.
  • Fasulo, T.R., 2005 [viewed 23 March 2012]. Yellowmargined leaf beetle, Microtheca ochroloma Stål [online]. Florida: Institute of Food and Agricultural Sciences, University of Florida. EENY-348. Available from: http://edis.ifas.ufl.edu/pdffiles/IN/IN62500.pdf
    » http://edis.ifas.ufl.edu/pdffiles/IN/IN62500.pdf
  • Fernandes, L.G., Carvalho, C.F., BUENO, V.H.P. and DINIZ, L.C., 1996. Aspectos biológicos de Brontocoris tabidus Signoret, 1852 e . Podisus nigrispinus Dallas (Hemiptera: Pentatomidae)Revista Cerne, vol. 2, no. 1, pp. 1-10.
  • Jusselino-Filho, P., Zanuncio, J.C., Fragoso, D.B., Serrão, J.E. and Lacerda, M.C., 2003. Biology of (Heteroptera: Pentatomidae) fed with . Brontocoris tabidusMusca domestica (Diptera: Muscidae) larvaeBrazilian Journal of Biology = Revista Brasileira de Biologia, vol. 63, no. 3, pp. 463-468. http://dx.doi.org/10.1590/S1519-69842003000300012 PMid:14758705.
    » http://dx.doi.org/10.1590/S1519-69842003000300012
  • Lacerda, M.C., Ferreira, A.M.R.M., Zanuncio, T.V., Zanuncio, J.C., Bernardino, A.S. and Espindula, M.C., 2004. Development and reproduction of (Heteroptera: Pentatomidae) fed on larva of . Podisus distinctusBombyx mori (Lepidoptera: Bombycidae)Brazilian Journal of Biology = Revista Brasileira de Biologia, vol. 64, no. 2, pp. 237-242. http://dx.doi.org/10.1590/S1519-69842004000200008 PMid:15462296.
    » http://dx.doi.org/10.1590/S1519-69842004000200008
  • Oliveira, H.N.D., Pratissoli, D., Pedruzzi, E.P. and Espindula, M.C., 2004. Desenvolvimento do predador Podisus nigrispinus alimentado com e Spodoptera frugiperdaTenebrio molitor.Pesquisa Agropecuária Brasileira, vol. 39, no. 10, pp. 947-951. http://dx.doi.org/10.1590/S0100-204X2004001000001
    » http://dx.doi.org/10.1590/S0100-204X2004001000001
  • Parra, J.R.P., Botelho, P.S., Corrêa-Ferreira, B.S. and Bento, J.M.S., 2002. Controle biológico: uma visão inter e multidisciplinar. In: J.R.P. PARRA, P.S. BOTELHO, B.S. CORRÊA-FERREIRA and J.M.S. BENTO, eds. Controle biológico no Brasil: parasitoides e predadores. São Paulo: Manole, pp. 125-142.
  • Pinto, C.M.F., Pereira, J.M. and Paula JUNIOR, T.J., 2001. Agricultura alternativa no contexto mundial. Informe Agropecuário, vol. 22, no. 212, pp. 80-83.
  • Poncio, S., Dequech, S.T.B., Sturza, V.S., Lissner, R.A.D., Perlin, L.F., Rosalino, P.K. and Ribeiro, L.P., 2010. Primeiro relato de Stiretrus decastigmus no Brasil predando Microtheca ochroloma.Ciência Rural, vol. 40, no. 5, pp. 1203-1205. http://dx.doi.org/10.1590/S0103-84782010005000069
    » http://dx.doi.org/10.1590/S0103-84782010005000069
  • Santos, G.P., Zanuncio, T.V., Ribeiro, G.T., Da Silva, E.P. and Zanuncio, J.C., 2004. Influência da temperatura no desenvolvimento ninfal de Podisus distinctus (Dallas) (Heteroptera: Pentatomidae). Revista Cerne, vol. 10, no. 2, pp. 213-221.
  • Silva, E.N., Santos, T.M. and Ramalho, F.S., 1996. Desenvolvimento ninfal de Stal (Hemiptera: Pentatomidae) alimentado com curuquerê-do-algodoeiro. Supputius cincticepsAnais da Sociedade Entomológica do Brasil, vol. 25, no. 2, pp. 103-108.
  • Silva, F.A.S., 1996. FASE: the ASSISTAT Software: statistical assistance. In: Proceedings of the 6th International Conference on Computers in Agriculture, 1996, Cancun, Mexico. Cancun: American Society of Agricultural Engineers, pp. 246-298.
  • Sturza, V.S., Poncio, S., Dorfey, C., Dequech, S.T.B., Bolzan, A. and Walker, M., 2012. Ocurrence of Herrich-Schaeffer (Hemiptera: Pentatomidae) preying . Stiretrus decastigmusMicrotheca semilaevis Stal (Coleoptera: Chrysomelidae)Neotropical Entomology, vol. 41, no. 1, pp. 81-82. http://dx.doi.org/10.1007/s13744-011-0013-9 PMid:23950015.
    » http://dx.doi.org/10.1007/s13744-011-0013-9
  • Vacari, A.M., Otuka, A.K. and De-Bortoli, A.S., 2007. Desenvolvimento de (Fabricius, 1794) (Lepidoptera: Crambidae). Podisus nigrispinus (Dallas, 1851) (Hemiptera: Pentatomidae) alimentado com lagartas de Diatraea saccharalisArquivos do Instituto Biológico, vol. 74, no. 3, pp. 259-265.
  • Vivan, L.M., Torres, J.B., Veiga, A.F.S.L. and Zanuncio, J.C., 2002. Comportamento de predação e conversão alimentar de . Podisus nigrispinus sobre a traça-do-tomateiroPesquisa Agropecuária Brasileira, vol. 37, no. 5, pp. 581-587. http://dx.doi.org/10.1590/S0100-204X2002000500002
    » http://dx.doi.org/10.1590/S0100-204X2002000500002
  • Wanderley, M.J.A. and Ramalho, F.S., 1999. Efeitos da temperatura no desenvolvimento de (Stäl) (Heteroptera: Pentatomidae) alimentado com larvas de L. Supputius cincticepsMusca domesticaAnais da Sociedade Entomológica do Brasil, vol. 28, no. 1, pp. 121-129. http://dx.doi.org/10.1590/S0301-80591999000100013
    » http://dx.doi.org/10.1590/S0301-80591999000100013
  • Xavier, M.R., De-Bortoli, A.S., Vacari, A.M., Laurentis, V.L. and Magalhães, G.O., 2009. Aspectos biológicos e tabela de vida de nigrispinusPlutella (L., 1758) em folha de couve ( . In: Podisus (DALLAS, 1851) alimentado com lagartas de xylostellaBrassicaoleracea L.)Anais do XXI Congresso de Iniciação Científica da Unesp, 2009, Jaboticabal, São Paulo. Jaboticabal: UNESP, pp. 557-560.
  • Zanuncio, J.C., Nascimento, E.C., Santos, G.P. and Araújo, F.S., 1991. Aspectos biológicos do predador (Bergroth, 1891) (Hemiptera: Pentatomidae). Podisus connexivusAnais da Sociedade Entomológica do Brasil, vol. 20, no. 2, pp. 243-249.
  • Zanuncio, T.V., Zanuncio, J.C., Vilela, E.F. and Sartório, R.C., 1992. Aspectos biológicos da fase adulta de Stal, 1860 (Hemiptera: Pentatomidae), predador de lagartas desfolhadoras de eucalipto. Supputius cinsticepsInstituto de Pesquisas e Estudos Florestais, vol. 45, no. 1, pp. 35-39.

Publication Dates

  • Publication in this collection
    15 Mar 2016
  • Date of issue
    Apr-Jun 2016

History

  • Received
    20 Oct 2014
  • Accepted
    23 Apr 2015
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