Phytophagy of the predator Podisus nigrispinus (Dallas, 1851) (Hemiptera: Pentatomidae) fed on prey and Brassicaceae

Fitofagia do predador Podisus nigrispinus (Dallas, 1851) (Hemiptera: Pentatomidae) em diferentes brassicáceas

J. F. J. Grigolli M. M. Kubota Grigolli D. G. Ramalho A. L. Martins A. M. Vacari S. A. De Bortoli About the authors

Abstract

The purpose of this study was to investigate the development and reproduction of the zoophytophagous predator Podisus nigrispinus (Dallas) (Heteroptera: Pentatomidae) fed kale, broccoli and cabbage affects its. Nymphs and adults of this predator were fed on larvae of Plutella xylostella (L.) (Lepidoptera: Plutellidae) as prey with kale, cabbage, or broccoli. In the nymph period, the duration and prey consumption were similar with all the Brassicacea cultivar. However, nymph viability was higher for predators with broccoli leaves. The mean weight of 5th-instar nymphs, newly emerged females and the sex ratio were similar among the Brassicacea cultivars, while newly emerged males were heavier with kale and broccoli leaves. The supply of broccoli leaves resulted in greater oviposition, higher number of eggs per egg mass and longer longevity of P. nigrispinus males and females. Furthermore, the consumption of P. xylostella larvae by adult predators was higher with these cultivars. The net reproductive rate (R0) and mean generation time (T) were highest for predators with prey and broccoli leaves. The reproductive parameters of P. nigrispinus were enhanced when fed on P. xylostella larvae with and broccoli leaves, which can be an alternative diet in laboratory rearing of this predator.

Keywords:
biological control; mass rearing; predatory stinkbug; zoophytophagous

Resumo

O objetivo deste estudo foi verificar o desenvolvimento e reprodução do zoofitófago Podisus nigrispinus (Dallas) (Heteroptera: Pentatomidae) em couve, brócolis e repolho. Ninfas e adultos deste predador foram alimentados com lagartas de Plutella xylostella (L.) (Lepidoptera: Plutellidae) como presa e receberam folhas de couve, repolho ou brócolis. Durante o período ninfal, a duração do período e o consumo de presas foram semelhantes com as diferentes cultivares de brassicácea. Porém, a viabilidade ninfal foi maior para predadores com folhas de brócolis. O peso de ninfas de quinto instar e de fêmeas recém-emergidas e a razão sexual de P. nigrispinus foram semelhantes entre as cultivares de brassicáceas, enquanto que o peso de machos recém-emergidos foi maior com folhas de couve e brócolis. Folhas de brócolis proporcionaram maiores número de oviposições, ovos por postura e longevidade de machos e fêmeas de P. nigrispinus. Além disso, o consumo de lagartas de P. xylostella por adultos desse predador fora maiores com esta cultivar. A taxa líquida de reprodução (R0) e o tempo médio de geração (T) foram maiores para predadores com presa e folhas de brócolis. Podisus nigrispinus alimentados com lagartas de P. xylostella e folhas de brócolis apresentaram melhores parâmetros reprodutivos, podendo ser uma alternativa para a criação deste predador em laboratório.

Palavras-chave:
controle biológico; criação massal; percevejo predador; zoofitófago

1 Introduction

Podisus nigrispinus (Dallas, 1851) (Hemiptera: Pentatomidae) is an important biological control agent in several crops (Medeiros et al., 2000MEDEIROS, R.S., RAMALHO, F.S., LEMOS, W.P. and ZANUNCIO, J.C., 2000. Age-dependent fecundity and life-fertility tables for . Podisus nigrispinus (Dallas) (Heteroptera, Pentatomidae)Journal of Applied Entomology, vol. 124, no. 7-8, pp. 319-324. http://dx.doi.org/10.1046/j.1439-0418.2000.00482.x.
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). It can be found in Central and South America (Thomas, 1992THOMAS, D.B., 1992. Taxonomic synopsis of the Asopinae Pentatomidae (Heteroptera) of the Western Hemisphere. Lanham: Entomological Society of America. 156 p.), especially in the Neotropics (De Clercq, 2000DE CLERCQ, P., 2000. Predaceous stink bugs (Pentatomidae, Asopinae). In: C.W. SCHAEFER, A.R. PANIZZI. Heteroptera of economic importance. Cambridge: Cambridge University, pp. 737-789.). In Brazil, P. nigrispinus was reported in several States, e.g., Espírito Santo, Maranhão, Minas Gerais, Mato Grosso do Sul, Pará, and São Paulo (Oliveira et al., 2011OLIVEIRA, H.N., ESPINDULA, M.C., DUARTE, M.M., PEREIRA, F.F. and ZANUNCIO, J.C., 2011. Development and reproduction of (Hemiptera: Pentatomidae) fed with . Podisus nigrispinusThyrinteina arnobia (Lepidoptera: Geometridae) reared on guava leavesBrazilian Archives of Biology and Technology, vol. 54, no. 3, pp. 429-434. http://dx.doi.org/10.1590/S1516-89132011000300001.
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). Podisus species have a generalist feeding habit, but mainly on lepidopteran larvae (Oliveira et al., 2004aOLIVEIRA, H.N., ESPINDULA, M.C., PRATISSOLI, D. and PEDRUZZI, E.P., 2004a. Ganho de peso e comportamento de oviposição de Podisus nigrispinus utilizando lagartas de Spodoptera frugiperda e larvas de como presas. Tenebrio molitorCiência Rural, vol. 34, no. 6, pp. 1945-1948. http://dx.doi.org/10.1590/S0103-84782004000600043.
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).

Due to the ease of rearing this stinkbug in the laboratory, these insects are produced and released in biological control programs of defoliating larvae (Zanuncio et al., 2002ZANUNCIO, J.C., GUEDES, R.N.C., OLIVEIRA, H.N. and ZANUNCIO, T.V., 2002. Uma década de estudos com percevejos predadores: conquistas e desafios. In: J.R.P. PARRA, P.S.M. BOTELHO, B.S. CORRÊA-FERREIRA, J.M.S. BENTO. Controle biológico no Brasil: parasitoide e predadores. São Paulo: Manole, pp. 405-505.). Alternative preys and artificial diets are used to mass rearing this predator P. nigrispinus (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, 1851) (Hemiptera: Pentatomidae)Cerne, vol. 2, no. 1, pp. 1-10.; Zanuncio et al., 1996aZANUNCIO, J.C., SAAVEDRA, J.L.D., OLIVEIRA, H.N., DEGHEELE, D. and DE CLERCQ, P., 1996a. Development of the predatory stinkbug (Signoret) (Heteroptera: Pentatomidae) on different proportions of an artificial diet and pupae of . Brontocoris tabidusTenebrio molitor L. (Coleoptera: Tenebrionidae)Biocontrol Science and Technology, vol. 6, no. 4, pp. 619-625. http://dx.doi.org/10.1080/09583159631253.
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; Saavedra et al., 1997SAAVEDRA, J.L.D., ZANUNCIO, J.C., ZANUNCIO, T.V. and GUEDES, R.N., 1997. Prey capture ability of . Podisus nigrispinus (Dallas) (Heteroptera: Pentatomidae) reared for successive generations on meridic dietsJournal of Applied Entomology, vol. 12, no. 1-5, pp. 327-330. http://dx.doi.org/10.1111/j.1439-0418.1997.tb01414.x.
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; Zanuncio et al., 1996bZANUNCIO, T.V., ZANUNCIO, J.C., SAAVEDRA, J.L.D. and LOPES, E.D., 1996b. Desenvolvimento de (Dallas) (Heteroptera: Pentatomidae) com . Podisus nigrispinusZophobas confusa Gebien (Coleoptera: Tenebrionidae) comparado a duas outras presas alternativasRevista Brasileira de Zoologia, vol. 13, no. 1, pp. 159-164. http://dx.doi.org/10.1590/S0101-81751996000100016.
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), in view of the difficulties of using natural prey in the laboratory.

The prey availability and quality can influence the development of P. nigrispinus (Valicente and O’Neil 1993VALICENTE, F.H. and O’NEIL, R.J., 1993. Effects of two host plants on selected life history characteristics of (Say) (Heteroptera, Pentatomidae). 1 - Without access to prey. Podisus maculiventrisEnvironmental Entomology, vol. 23, pp. 1254-1259.; De Clercq et al., 1998DE CLERCQ, P., MERLEVEDE, F. and TIRRY, L., 1998. Unnatural prey and diets for rearing (Heteroptera, Pentatomidae). Podisus maculiventrisBiological Control, vol. 12, no. 2, pp. 137-142. http://dx.doi.org/10.1006/bcon.1998.0611.
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; Molina-Rugama et al., 1998aMOLINA-RUGAMA, A.J., ZANUNCIO, J.C., PRATISSOLI, D. and CRUZ, I., 1998a. Efeito do intervalo de alimentação na reprodução e na longevidade do predador . Podisus nigrispinus (Dallas) (Heteroptera: Pentatomidae)Anais da Sociedade Entomológica do Brasil, vol. 27, no. 1, pp. 77-84. http://dx.doi.org/10.1590/S0301-80591998000100010.
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; Mourão et al., 2003MOURÃO, S.A., ZANUNCIO, J.C., MOLINA-RUGAMA, A.J., VILELA, E.F. and LACERDA, M.C., 2003. Efeito da escassez de presa na sobrevivência e reprodução do predador Supputius cincticeps (Stal) (Heteroptera: Pentatomidae). Neotropical Entomology, vol. 32, no. 3, pp. 469-473. http://dx.doi.org/10.1590/S1519-566X2003000300014.
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). However, this predator can also feed on plants without damaging them (Naranjo and Stimac, 1985NARANJO, S.E. and STIMAC, J.L., 1985. Development, survival, and reproduction of . Geocoris punctipes (Hemiptera, Lygaeidae): effects of plant feeding on soybean and associated weedsEnvironmental Entomology, vol. 14, no. 4, pp. 523-530. http://dx.doi.org/10.1093/ee/14.4.523.
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; Ruberson et al., 1986RUBERSON, J.R., TAUBER, J.M. and TAUBER, C.A., 1986. Plant feeding by (Heteroptera, Pentatomidae): effect on survival, development, and pre oviposition period. Podisus maculiventrisEnvironmental Entomology, vol. 15, no. 4, pp. 894-897. http://dx.doi.org/10.1093/ee/15.4.894.
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; Naranjo and Stimac, 1987NARANJO, S.E. and STIMAC, J.L., 1987. Plant influences on predation and oviposition by . Geocoris punctipes (Hemiptera, Lygaeidae) in soybeansEnvironmental Entomology, vol. 16, no. 1, pp. 182-189. http://dx.doi.org/10.1093/ee/16.1.182.
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; De Clercq and Degheele, 1992DE CLERCQ, P. and DEGHEELE, D., 1992. Development and survival of (Say) and (Fab.) (Heteroptera, Pentatomidae) at various constant temperatures. Podisus maculiventrisPodisus sagittaCanadian Entomologist, vol. 124, no. 01, pp. 125-133. http://dx.doi.org/10.4039/Ent124125-1.
http://dx.doi.org/10.4039/Ent124125-1...
; Lemos et al., 2001LEMOS, W.P., MEDEIROS, R.S., RAMALHO, F.S. and ZANUNCIO, J.C., 2001. Effects of plant feeding on the development, survival, and reproduction of . Podisus nigrispinus (Dallas) (Heteroptera, Pentatomidae)International Journal of Pest Management, vol. 27, no. 2, pp. 89-93. http://dx.doi.org/10.1080/09670870151130499.
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). This feeding behavior allows the classification of the insect as zoophytophagous (Coll and Guershon, 2002COLL, M. and GUERSHON, M., 2002. Omnivory in terrestrial arthropods: mixing plant and prey diet. Annual Review of Entomology, vol. 47, no. 1, pp. 267-297. PMid:11729076. http://dx.doi.org/10.1146/annurev.ento.47.091201.145209.
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; Azevedo et al., 2007AZEVEDO, D.O., ZANUNCIO, J.C., ZANUNCIO JUNIOR, J.S., MARTINS, G.F., MARQUES-SILVA, S., SOSSAI, M.F. and SERRÃO, J.E., 2007. Biochemical and morphological aspects of salivary glands of the predator . Brontocoris tabidus (Heteroptera: Pentatomidae)Brazilian Archives of Biology and Technology, vol. 50, no. 3, pp. 469-477. http://dx.doi.org/10.1590/S1516-89132007000300013.
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), since the combined use of plants and prey can improve their biological characteristics (Lemos et al., 2001LEMOS, W.P., MEDEIROS, R.S., RAMALHO, F.S. and ZANUNCIO, J.C., 2001. Effects of plant feeding on the development, survival, and reproduction of . Podisus nigrispinus (Dallas) (Heteroptera, Pentatomidae)International Journal of Pest Management, vol. 27, no. 2, pp. 89-93. http://dx.doi.org/10.1080/09670870151130499.
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; Oliveira et al., 2002OLIVEIRA, J.E.M., TORRES, J.B., CARRANO-MOREIRA, A.F. and BARROS, R., 2002. Efeito das plantas do algodoeiro e do tomateiro, como complemento alimentar, no desenvolvimento e na reprodução do predador . Podisus nigrispinus (Dallas) (Heteroptera: Pentatomidae)Neotropical Entomology, vol. 31, no. 1, pp. 101-108. http://dx.doi.org/10.1590/S1519-566X2002000100014.
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).

There are at least three hypotheses to explain the zoophytophagous habit in predators: (1) equivalence - plants can provide nutrients when prey is absent or scarce; (2) facilitation – plants provides essential nutrients complementary to predation; and (3) independence - plant material provides essential nutrients absent in the prey (Lalonde et al., 1999LALONDE, R.G., MCGREGOR, R.R., ROITBERGER, B.D. and GILLESPIE, D.R., 1999. Plant-feeding by arthropod predators contributes the stability of predator-prey population dynamics. Oikos, vol. 87, no. 3, pp. 603-609. http://dx.doi.org/10.2307/3546827.
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; Eubanks and Denno, 2000EUBANKS, M. and DENNO, R.F., 2000. Host plants mediate omnivore-herbivore interactions and influence prey suppression. Ecology, vol. 81, pp. 936-947.; Gillespie and McGregor, 2000GILLESPIE, D.R. and MCGREGOR, R.R., 2000. The functions of plant feeding in the omnivorous predator . Dicyhus hesperus: water places limits on predationEcological Entomology, vol. 25, no. 4, pp. 380-386. http://dx.doi.org/10.1046/j.1365-2311.2000.00285.x.
http://dx.doi.org/10.1046/j.1365-2311.20...
; Sinia et al., 2004SINIA, A., ROITBERG, B., MCGREGOR, R.R. and GILLESPIE, D.R., 2004. Prey feeding increases water stress in the omnivorous predator Dicyphus hesperus.Entomologia Experimentalis et Applicata, vol. 110, no. 3, pp. 243-248. http://dx.doi.org/10.1111/j.0013-8703.2004.00145.x.
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).

Dietary habits can change the life cycle of insects, since well-fed individuals reproduce more and more frequently (Lenski, 1984LENSKI, R.E., 1984. Food limitation and competition: a field experiment with two species. CarabusJournal of Animal Ecology, vol. 53, no. 1, pp. 203-216. http://dx.doi.org/10.2307/4352.
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; Molina-Rugama et al., 1997MOLINA-RUGAMA, A.J., ZANUNCIO, J.C., TORRES, J.B., ZANUNCIO, T.V., 1997. Longevidad y fecundidad de . Podisus nigrispinus (Heteroptera: Pentatomidae) alimentado com Musca domestica (Diptera: Muscidae) y frijolRevista de Biologia Tropical = Journal of Tropical Biology, vol. 45, pp. 1125-1130.; Chapman, 1998CHAPMAN, R.F., 1998. Reproductive system: female. In: R.F. CHAPMAN. The insects: structure and function. Cambridge: Cambridge University, pp. 295-324.; Molina-Rugama et al., 1998bMOLINA-RUGAMA, A.J., ZANUNCIO, J.C., ZANUNCIO, T.V. and OLIVEIRA, M.L.R., 1998b. Reproductive strategy of . Podisus rostralis (Stal) (Heteroptera: Pentatomidae) females under different feeding intervalsBiocontrol Science and Technology, vol. 8, no. 4, pp. 583-588. http://dx.doi.org/10.1080/09583159830090.
http://dx.doi.org/10.1080/09583159830090...
; Lemos et al., 2001LEMOS, W.P., MEDEIROS, R.S., RAMALHO, F.S. and ZANUNCIO, J.C., 2001. Effects of plant feeding on the development, survival, and reproduction of . Podisus nigrispinus (Dallas) (Heteroptera, Pentatomidae)International Journal of Pest Management, vol. 27, no. 2, pp. 89-93. http://dx.doi.org/10.1080/09670870151130499.
http://dx.doi.org/10.1080/09670870151130...
). The objective of this study was to evaluate the development and reproduction of P. nigrispinus in three different Brassicacea cultivars to improve laboratory rearing of this predator.

2 Material and Methods

The experiment was carried out in the Laboratory of Biology and Rearing of Insects (LBCI) of the Department of Plant Protection, FCAV/UNESP, in Jaboticabal, São Paulo, Brazil in an air-conditioned room at 25±1 ºC, relative humidity of 70±10% and 12-hour photoperiod (12 h light and 12 hours dark). The treatments consisted of three Brassicacea species: kale Brassica oleracea var. acephala (kales ‘Manteiga’ hybrid HS-20), cabbage Brassica oleracea var. capitata (cabbage ‘Bob Cat’) and broccoli Brassica oleracea var. italic (broccoli 'Piracicaba'). In the tests, the predatory stinkbug P. nigrispinus was fed ad libitum on prey Plutella xylostella (L.) (Lepidoptera: Plutellidae) larvae. The mass-reared insects used in the experiment were from the LBCI, FCAV/UNESP, Jaboticabal, São Paulo, Brazil.

2.1 Biological parameters of Podisus nigrispinus nymphs feeding on Plutella xylostella larvae as prey and Brassicaceae

A completely randomized design with six replications was used to evaluate P. nigrispinus nymph stage. Transparent plastic cylindrical 1000 mL containers (diameter 15 cm, height 10 cm), covered with plastic lid were used. Two tubes (1.5 cm3) were fixed to the lid, one to provide water and the other to fix a Brassicacea (cabbage, kales or broccoli) leaf.

Each container represented one replication, in which 10 predatory second-instar P. nigrispinus nymphs (<24 h old) were placed, which were initially fed with 20 fourth-instar P. xylostella larvae and a leaf of one of the Brassicaceae. As the nymphs developed, the number of larvae available increased, avoiding lack of prey, as well as cannibalism. The sterilization of the containers and exchange of water, leaves and containers, as well as evaluations were performed every 48 hours.

The following biological parameters were evaluated in the nymph stage: duration of each stage, duration of the nymph stage, nymph viability and nymph consumption. In addition, 10 to 24 h-old 5th- instar nymphs were weighed per treatment.

2.2 Biological parameters of Podisus nigrispinus adults feeding on Plutella xylostella larvae as prey and Brassicaceae

After adult emergence, 10 pairs were formed per treatment, and one couple per container was placed in a transparent 1000 mL plastic container (diameter 15 cm, height 10 cm), and covered with a plastic lid. Two tubes (1.5 cm3) were fixed to the lid, one to provide water and the other to fix a Brassicacea (cabbage, kales or broccoli) leaf. Per container, 50 fifth instar P. xylostella larvae were offered as prey. The experimental design used was completely randomized with three treatments (kales, cabbage, and broccoli) and 10 replications.

The following biological characteristics were evaluated: weight of newly emerged males and females (<24 h old), longevity of males and females, oviposition period, and total daily number of eggs per female, egg viability and egg incubation period.

2.3 Fertility life table of Podisus nigrispinus

The biological parameters of P. nigrispinus determined in three different Brassicaceae were used to establish a life fertility table (Birch, 1948BIRCH, L.C., 1948. The intrinsic rate of natural increase of an insect population. Journal of Animal Ecology, vol. 17, no. 1, pp. 15-26. http://dx.doi.org/10.2307/1605.
http://dx.doi.org/10.2307/1605...
; Silveira Neto et al., 1976SILVEIRA NETO, S., NAKANO, O., BALDIN, D. and VILLANOVA, N.A., 1976. Manual de ecologia dos insetos. São Paulo: Agronômica Ceres. 419 p.; Price, 1984PRICE, P.W., 1984. Insect ecology. 2nd ed. New York: John Willey. 607 p.).

From the values of age ranges (x), specific fertility (mx) and survival probability (lx) of the life and fertility tables, the net reproductive rate (R0), the generation time (T), the intrinsic growth rate (rm), finite increase rate (λ) and the population doubling time (Dt) (Krebs, 1994KREBS, C.J., 1994. Ecology: the experimental analysis of distribution and abundance. New York: Harper & Row. 801 p.) were calculated, where R0= ∑(lxmx); T = ∑(xlxmx)/∑(lxmx); rm= lnR0/T; λ= erm; and Dt= ln (2)/rm.

2.4 Data analysis

The data of biological parameters were subjected to Taylor's Power Law (Taylor, 1984TAYLOR, L.R., 1984. Accessing and interpreting the spatial distributions of insect populations. Annual Review of Entomology, vol. 29, no. 1, pp. 321-357. http://dx.doi.org/10.1146/annurev.en.29.010184.001541.
http://dx.doi.org/10.1146/annurev.en.29....
) for homogenization of the means and reduction of the variances to indicate the best data transformation using arcsinx/100 for the parameters sex ratio and egg viability. Analysis of variance (SAS INSTITUTE, 2000SAS INSTITUTE, 2000. SAS/C OnlineDocTM: version 8. Cary: SAS Institute, Inc.) was used and the means of the Brassicacea treatments were compared by Tukey’s test at 5% significance.

The population parameters of the fertility life table were estimated (Maia et al., 2000MAIA, A.H., LUIZ, A.J.B. and CAMPANHOLA, C., 2000. Statistical inference on associated fertility life parameters using Jackknife technique: computational aspects. Journal of Economic Entomology, vol. 93, no. 2, pp. 511-518. PMid:10826207. http://dx.doi.org/10.1603/0022-0493-93.2.511.
http://dx.doi.org/10.1603/0022-0493-93.2...
), using SAS (SAS INSTITUTE, 2000SAS INSTITUTE, 2000. SAS/C OnlineDocTM: version 8. Cary: SAS Institute, Inc.) software, based on the jackknife method for estimating the parameters, confidence intervals, and to allow treatment comparisons.

3 Results

The duration of the second (F2;15= 0.26; P>0.05), third (F2;15= 3.64; P>0.05), fourth (F2;15= 2.13; P>0.05), and fifth (F2;15= 0.43; P>0.05) instars and the nymph period (F2;15= 0.38; P>0.05) of P. nigrispinus fed on P. xylostella larvae on different Brassicaceae were similar. However, nymph viability (F2;15= 4.09; P<0.05) of this predator on broccoli (80.00%) was longer then on kale (56.67%) and cabbage (61.67%), whereas nymph prey consumption (F2;15= 1.75) was similar between treatments, 29.18 (cabbage) to 41.75 (kale) P. xylostella larvae per nymph of the predator (Table 1).

Table 1
Duration of nymph stages (days), nymph period (days), nymph survival (%), and prey consumption (mean ± SE) by Podisus nigrispinus (Heteroptera: Pentatomidae) nymphs fed on Plutella xylostella (Lepidoptera: Plutellidae) larvae with leaves of three Brassicacea cultivars. Jaboticabal, São Paulo, Brazil, 2012.

The mean weight of fifth-instar nymphs (F2;15= 0.68; P>0.05) and newly emerged females (F2;15= 0.45; P>0.05) as well as the sex ratio (F2;10= 1.04; P>0.05) of insects were similar in all treatments. However, newly emerged males (F2;27= 4.23; P<0.05) on cabbage and broccoli had higher mean weight. The mean weight of fifth- instar nymphs was similar between treatments, varying from 17.71 mg (kales and cabbage) to 19.70 mg (broccoli). The weight of newly emerged predator males was higher on kales (33.49 mg) and broccoli (28.61 mg) than on cabbage (23.58 mg), while no differences were observed in the mean weight of newly emerged females, 39.02 mg (cabbage) to 43.35 mg (broccoli). The sex ratio of this predator was similar in the three treatments, 0.44 (broccoli) to 0.68 (cabbage) (Table 2).

Table 2
Weight of fifth instar nymphs and of newly emerged males and females (mg) and sex ratio (mean ± SE) of Podisus nigrispinus (Heteroptera: Pentatomidae) fed on Plutella xylostella (Lepidoptera: Plutellidae) larvae with leaves of three Brassicacea cultivars. Jaboticabal, São Paulo, Brazil, 2012.

The parameters eggs per female (F2;27= 6.41; P<0.01), number of ovipositions (F2;27= 6.59; P<0.01) and eggs per egg mass (F2;27= 3.56; P<0.05) differed between treatments with higher for P. nigrispinus nymphs fed on broccoli. The incubation period (F2;27= 0.70; P>0.05) and viability (F2;27= 1.85; P>0.05) were not different between treatments (Table 3).

Table 3
Number of eggs per female, number of egg mass per female, egg incubation period (days), egg viability (%), and number of eggs per egg mass (mean ± SE) of Podisus nigrispinus (Heteroptera: Pentatomidae) fed on Plutella xylostella (Lepidoptera: Plutellidae) larvae with leaves of three Brassicacea cultivars. Jaboticabal, São Paulo, Brazil, 2012.

The number of eggs per female of this predator (F2;27= 3.56; P<0.05) reared on broccoli was 2.38 folds higher than on kale and 2.44 folds higher than on cabbage, indicating that broccoli provided better conditions for oviposition of P. nigrispinus. The number of ovipositions (F2;27= 6.59; P<0.01) was higher on broccoli (13.10) than on kale (5.80) and cabbage (2.90). The number of eggs per egg mass was higher on broccoli (35.76) compared to kale (23.12) and cabbage (17.74). However, the egg viability (F2;27= 1.85; P>0.05) was similar between treatments, i.e., 55.60% (kale), 59.69% (broccoli) and 63.79% (cabbage). This pattern was similar to that of the incubation period (F2;27= 0.70; P>0.05), 5.05 days (cabbage), 5.12 days (kale) and 5.34 days (broccoli) (Table 3).

The consumption of adult predators (F2;29= 8.19; P<0.01), male (F2;29= 15.80; P<0.01) and female (F2;29= 18.42 ; P<0.01) longevities differed, with higher values of the predator with broccoli (Table 4).

Table 4
Consumption of Plutella xylostella (Lepidoptera: Plutellidae) larvae and longevity (days) of Podisus nigrispinus (Heteroptera: Pentatomidae) adults and longevity (days) of P. nigrispinus males and females (mean ±S E) fed on P. xylostella larvae with leaves of three Brassicacea cultivars. Jaboticabal, São Paulo, Brazil, 2012.

The consumption of P. nigrispinus adults on broccoli t (306.21 larvae) was higher than with kale (182.21 larvae) and cabbage (172.50 larvae). Female longevity was longer on broccoli (37.86 days) than on kale (17.43 days) and cabbage (23.00 days). Male longevity was highest on broccoli (42.29 days) than on kale (25.00 days), that was higher than on cabbage (8.00 days) (Table 4).

The Brassicaceae affected population parameters of the life table of P. nigrispinus. The net reproductive rate (R0) (75.3 females/female) and generation time (T) (37.6 days) of this predator were higher with broccoli. The intrinsic population increase rate (rm), finite population increase rate (λ) and the time required for population doubling (TD) were similar between the Brassicacea cultivars (Table 5).

Table 5
Fertility life table parameters (mean ± SE) of Podisus nigrispinus (Heteroptera: Pentatomidae) fed on Plutella xylostella (Lepidoptera: Plutellidae) larvae with leaves of three Brassicacea cultivars. Jaboticabal, São Paulo, Brazil, 2012.

4 Discussion

Development and reproduction of P. nigrispinus varied with Brassicacea cultivar. The plant material can have positive effects on the development of predatory stinkbugs even under adverse situations (Lemos et al., 2001LEMOS, W.P., MEDEIROS, R.S., RAMALHO, F.S. and ZANUNCIO, J.C., 2001. Effects of plant feeding on the development, survival, and reproduction of . Podisus nigrispinus (Dallas) (Heteroptera, Pentatomidae)International Journal of Pest Management, vol. 27, no. 2, pp. 89-93. http://dx.doi.org/10.1080/09670870151130499.
http://dx.doi.org/10.1080/09670870151130...
). Thus, the reproduction and population growth rates of this insect are high when fed on prey and plants (Guedes et al., 2007GUEDES, B.A.M., ZANUNCIO, J.C., RAMALHO, F.S. and SERRAO, J.E., 2007. Midgut morphology and enzymes of the obligate zoophytophagous stinkbug . Brontocoris tabidus (Signoret, 1863) (Heteroptera: Pentatomidae)The Pan-Pacific Entomologist, vol. 83, no. 1, pp. 66-74. http://dx.doi.org/10.3956/0031-0603-83.1.66.
http://dx.doi.org/10.3956/0031-0603-83.1...
).

Podisus nigrispinus feeding on prey with broccoli had improved biological parameters what agrees with that found with Eucalyptus urophylla with reduced nymph mortality and increased adult longevity and the number of eggs per female and P. nigrispinus nymphs. This indicates that this predator can be fed with both prey and Eucalyptus in the field as well as in the laboratory (Holtz et al., 2011HOLTZ, A.M., ALMEIDA, G.D., FADINI, M.A.M., ZANUNCIO, J.C., ZANUNCIO-JÚNIOR, J.S. and ANDRADE, G.S., 2011. Phytophagy on eucalyptus plants increases the development and reproduction of the predator . Podisus nigrispinus (Hemiptera: Pentatomidae)Acta Scientiarum: Agronomy, vol. 33, no. 2, pp. 231-235.).

Results obtained in the present study could be explained because plant material can compensate a possible low nutritional quality of the prey by supplying water and nutrients that would increase weight, reproduction and longevity of these predators (Guedes et al., 2007GUEDES, B.A.M., ZANUNCIO, J.C., RAMALHO, F.S. and SERRAO, J.E., 2007. Midgut morphology and enzymes of the obligate zoophytophagous stinkbug . Brontocoris tabidus (Signoret, 1863) (Heteroptera: Pentatomidae)The Pan-Pacific Entomologist, vol. 83, no. 1, pp. 66-74. http://dx.doi.org/10.3956/0031-0603-83.1.66.
http://dx.doi.org/10.3956/0031-0603-83.1...
). The development and reproduction of Supputius cincticeps (Stal) and Brontocoris tabidus Signoret (Hemiptera: Pentatomidae) was also improved when fed on T. molitor pupae on eucalyptus plants with exclusively prey (Zanuncio et al., 2000ZANUNCIO, J.C., ZANUNCIO, T.V., GUEDES, R.N.C. and RAMALHO, F.S., 2000. Effect of feeding on three Eucalyptus species on the development of (Heteroptera: Pentatomidae) fed with . Brontocoris tabidusTenebrio molitor (Coleoptera: Tenebrionidae)Biocontrol Science and Technology, vol. 10, pp. 443-450. http://dx.doi.org/10.1080/09583150050115025.
http://dx.doi.org/10.1080/09583150050115...
).

The duration of nymph period with kale (18.90), cabbage (18.74) and broccoli (18.23) were similar to that reported for the nymph period of P. nigrispinus fed only on Spodoptera frugiperda (J.E. Smith) (Lepidoptera: Noctuidae) and on pupae of T. molitor, respectively, 21.6 and 20.4 days (Oliveira et al., 2004bOLIVEIRA, H.N., PRATISSOLI, D., PEDRUZZI, E.P. and ESPINDULA, M.C., 2004b. Desenvolvimento do predador alimentado com Podisus nigrispinusSpodoptera frugiperda e Tenebrio molitor.Pesquisa Agropecuaria Brasileira, vol. 39, no. 10, pp. 947-951. http://dx.doi.org/10.1590/S0100-204X2004001000001.
http://dx.doi.org/10.1590/S0100-204X2004...
).

The weight of fifth-instar nymphs and of newly emerged males and females in the three treatments were lower than that of fifth-instar nymphs and males and females P. nigrispinus fed on Thyrinteina arnobia (Stoll, 1792) (Lepidoptera: Geometridae) with guava leaves (Oliveira et al., 2011OLIVEIRA, H.N., ESPINDULA, M.C., DUARTE, M.M., PEREIRA, F.F. and ZANUNCIO, J.C., 2011. Development and reproduction of (Hemiptera: Pentatomidae) fed with . Podisus nigrispinusThyrinteina arnobia (Lepidoptera: Geometridae) reared on guava leavesBrazilian Archives of Biology and Technology, vol. 54, no. 3, pp. 429-434. http://dx.doi.org/10.1590/S1516-89132011000300001.
http://dx.doi.org/10.1590/S1516-89132011...
). The higher weight of females than males was due to the biomass accumulated by females from the fifth-instar stage, necessary for reproduction. The weight gain of the females was also related to the ovary development and egg formation (Oliveira et al., 1999OLIVEIRA, H.N., ZANUNCIO, J.C., SOSSAI, M.F. and PRATISSOLI, D., 1999. Body weight increment of Podisus nigrispinus (Stal) (Heteroptera: Pentatomidae), fed on L. (Diptera: Muscidae). Tenebrio molitor L. (Coleoptera: Tenebrionidae) or Musca domesticaBrenesia, vol. 51, pp. 77-83.; Oliveira et al., 2002OLIVEIRA, J.E.M., TORRES, J.B., CARRANO-MOREIRA, A.F. and BARROS, R., 2002. Efeito das plantas do algodoeiro e do tomateiro, como complemento alimentar, no desenvolvimento e na reprodução do predador . Podisus nigrispinus (Dallas) (Heteroptera: Pentatomidae)Neotropical Entomology, vol. 31, no. 1, pp. 101-108. http://dx.doi.org/10.1590/S1519-566X2002000100014.
http://dx.doi.org/10.1590/S1519-566X2002...
).

The mean number of eggs per P. nigrispinus female fed with P. xylostella and broccoli (467.90) was higher than with T. arnobia larvae on guava trees (314.90) (Oliveira et al., 2011OLIVEIRA, H.N., ESPINDULA, M.C., DUARTE, M.M., PEREIRA, F.F. and ZANUNCIO, J.C., 2011. Development and reproduction of (Hemiptera: Pentatomidae) fed with . Podisus nigrispinusThyrinteina arnobia (Lepidoptera: Geometridae) reared on guava leavesBrazilian Archives of Biology and Technology, vol. 54, no. 3, pp. 429-434. http://dx.doi.org/10.1590/S1516-89132011000300001.
http://dx.doi.org/10.1590/S1516-89132011...
), Alabama argillacea (Hüebner, 1818) (Lepidoptera: Noctuidae) on cotton (348.10) (Oliveira et al., 2002OLIVEIRA, J.E.M., TORRES, J.B., CARRANO-MOREIRA, A.F. and BARROS, R., 2002. Efeito das plantas do algodoeiro e do tomateiro, como complemento alimentar, no desenvolvimento e na reprodução do predador . Podisus nigrispinus (Dallas) (Heteroptera: Pentatomidae)Neotropical Entomology, vol. 31, no. 1, pp. 101-108. http://dx.doi.org/10.1590/S1519-566X2002000100014.
http://dx.doi.org/10.1590/S1519-566X2002...
), and with T. molitor (296.66; 325.00) (Oliveira et al., 2004bOLIVEIRA, H.N., PRATISSOLI, D., PEDRUZZI, E.P. and ESPINDULA, M.C., 2004b. Desenvolvimento do predador alimentado com Podisus nigrispinusSpodoptera frugiperda e Tenebrio molitor.Pesquisa Agropecuaria Brasileira, vol. 39, no. 10, pp. 947-951. http://dx.doi.org/10.1590/S0100-204X2004001000001.
http://dx.doi.org/10.1590/S0100-204X2004...
; Espindula et al., 2006ESPINDULA, M.C., OLIVEIRA, H.N., CAMPANHARO, M., PASTORI, P.L. and MAGEVSKI, G.C., 2006. Influência da massa corporal sobre características reprodutivas e longevidade de fêmeas de (Dallas) (Heteroptera: Pentatomidae). Podisus nigrispinusIdesia, vol. 24, pp. 19-25.), Diatraea saccharalis (Fabricius, 1794) (Lepidoptera: Pyralidae) (97.12) (Vacari et al., 2007VACARI, A.M., OTUKA, A.K. and BORTOLI, S.A., 2007. Desenvolvimento de Podisus nigrispinus (Dallas, 1851) (Hemiptera: Pentatomidae) alimentado com lagartas de (Fabricius,1794) (Lepidoptera: Crambidae). Diatraea saccharalisArquivos do Instituto Biologico, vol. 74, pp. 259-265.) and T. arnobia (57.00) on Eucalyptus (Holtz et al., 2006HOLTZ, A.M., ZANUNCIO, J.C., MARINHO, J.S., PRATISSOLI, D., PALLINI, A. and PEREIRA, C.J., 2006. Características biológicas de adultos de Podisus nigrispinus e (Hemiptera: Pentatomidae) alimentados com . Supputius cincticepsThyrinteina arnobia (Lepidoptera: Geometridae)Idesia, vol. 24, pp. 41-418.; Holtz et al., 2007HOLTZ, A.M., ZANUNCIO, J.C., OLIVEIRA, C.L., PRATISSOLI, D., PALLINI, A., MARINHO, J.S. and VIANNA, U.R., 2007. Potencial reprodutivo e de sobrevivência de Podisus nigrispinus Dallas (Heteroptera: Pentatomidae) sobre L. (Coleoptera: Tenebrionidae). Thyrinteina arnobia Stoll Lepidoptera: Geometridae) e Tenebrio molitorFloresta, vol. 37, no. 1, pp. 63-70. http://dx.doi.org/10.5380/rf.v37i1.7842.
http://dx.doi.org/10.5380/rf.v37i1.7842...
). This high number of eggs suggests that the prey P. xylostella and broccoli leaf may have higher nutritional values for the predator P. nigrispinus.

In the field, plant-derived substances can be an alternative or complementing the diet of predatory bugs (Crum et al., 1998CRUM, D.A., WEISER, L.A. and STAMP, N.E., 1998. Effects of prey scarcity and plant material as a dietary supplement on an insect predator. Oikos, vol. 83, no. 3, pp. 549-557. http://dx.doi.org/10.2307/3546775.
http://dx.doi.org/10.2307/3546775...
), allowing them to maintain their longevity (Valicente and O’Neil, 1995VALICENTE, F.H. and O’NEIL, R.J., 1995. Effect of host plants and feeding regimes on selected life history characteristics of . Podisus maculiventris (Say) (Heteroptera: Pentatomidae)Biological Control, vol. 5, no. 3, pp. 449-461. http://dx.doi.org/10.1006/bcon.1995.1054.
http://dx.doi.org/10.1006/bcon.1995.1054...
; Zanuncio et al., 2004ZANUNCIO, J.C., LACERDA, M.C., ZANUNCIO JÚNIOR, J.C., ZANUNCIO, T.V., SILVA, M.C. and ESPINDULA, M.C., 2004. Fertility and life table and rate of population growth of the predator Supputius cincticeps (Heteroptera: Pentatomidae) on plant of in the field. Eucalyptus cloezianaAnnals of Applied Biology, vol. 144, no. 3, pp. 357-361. http://dx.doi.org/10.1111/j.1744-7348.2004.tb00351.x.
http://dx.doi.org/10.1111/j.1744-7348.20...
). The use of plants as dietary supplement may or may not lead to a better establishment of predatory bug populations, depending on the composition of the agroecosystems (Oliveira et al., 2002OLIVEIRA, J.E.M., TORRES, J.B., CARRANO-MOREIRA, A.F. and BARROS, R., 2002. Efeito das plantas do algodoeiro e do tomateiro, como complemento alimentar, no desenvolvimento e na reprodução do predador . Podisus nigrispinus (Dallas) (Heteroptera: Pentatomidae)Neotropical Entomology, vol. 31, no. 1, pp. 101-108. http://dx.doi.org/10.1590/S1519-566X2002000100014.
http://dx.doi.org/10.1590/S1519-566X2002...
). Food source may affect the development and reproduction of these species since the nutritional value of plants depends on their species and natural enemies (Wackers, 2004WACKERS, F.L., 2004. A comparison of nectar and honeydew sugars with respect to their utilization by the hymenopteran parasitoid Cotesia glomerata.Journal of Insect Physiology, vol. 47, no. 9, pp. 1077-1084. PMid:11472770. http://dx.doi.org/10.1016/S0022-1910(01)00088-9.
http://dx.doi.org/10.1016/S0022-1910(01)...
). The greater viability of nymphs on broccoli leaves indicates that this Brassicacea has a positive influence on the rearing of P. nigrispinus.

The use of predatory bugs in biological control programs can reduce the use of insecticides and the environmental impacts they cause. The mass rearing of insects is important to provide natural enemies for research and commercial purposes. The use of P. xylostella and broccoli leaves has proved promising in rearing the predator with longer longevity and better reproductive parameters.

Acknowledgements

The authors gratefully acknowledge the scholarships granted by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) and the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) and thank the Universidade Estadual Paulista for the infrastructure.

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Publication Dates

  • Publication in this collection
    13 Mar 2017
  • Date of issue
    Nov 2017

History

  • Received
    08 Oct 2015
  • Accepted
    16 May 2016
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