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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 brassicaceas.

1. Introduction

Podisus nigrispinus (Dallas, 1851) (Hemiptera: Pentatomidae) is an important biological control agent in several crops (Medeiros et al., 2000). It can be found in Central and South America (Thomas, 1992), especially in the Neotropics (De Clercq, 2000). In Brazil, P. nigrispinus was reported in several States, e.g., Espirito Santo, Maranhao, Minas Gerais, Mato Grosso do Sul, Para, and Sao Paulo (Oliveira et al., 2011). Podisus species have a generalist feeding habit, but mainly on lepidopteran larvae (Oliveira et al., 2004a).

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., 2002). Alternative preys and artificial diets are used to mass rearing this predator P. nigrispinus (Fernandes et al., 1996; Zanuncio et al., 1996a; Saavedra et al., 1997; Zanuncio et al., 1996b), 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 1993; De Clercq et al., 1998; Molina-Rugama et al., 1998a; Mourao et al., 2003). However, this predator can also feed on plants without damaging them (Naranjo and Stimac, 1985; Ruberson et al., 1986; Naranjo and Stimac, 1987; De Clercq and Degheele, 1992; Lemos et al., 2001). This feeding behavior allows the classification of the insect as zoophytophagous (Coll and Guershon, 2002; Azevedo et al., 2007), since the combined use of plants and prey can improve their biological characteristics (Lemos et al., 2001; Oliveira et al., 2002).

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., 1999; Eubanks and Denno, 2000; Gillespie and McGregor, 2000; Sinia et al., 2004).

Dietary habits can change the life cycle of insects, since well-fed individuals reproduce more and more frequently (Lenski, 1984; Molina-Rugama et al., 1997; Chapman, 1998; Molina-Rugama et al., 1998b; Lemos et al., 2001). 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, Sao Paulo, Brazil in an air-conditioned room at 25 [+ or -] 1 [degrees]C, relative humidity of 70 [+ or -] 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, Sao 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 [cm.sup.3]) 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 [cm.sup.3]) 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 ofP nigrispinus determined in three different Brassicaceae were used to establish a life fertility table (Birch, 1948; Silveira Neto et al., 1976; Price, 1984).

From the values of age ranges (x), specific fertility (mx) and survival probability ([l.sub.x]) of the life and fertility tables, the net reproductive rate ([R.sub.0]), the generation time (T), the intrinsic growth rate ([r.sub.m]), finite increase rate (X) and the population doubling time (Dt) (Krebs, 1994) were calculated, where [R.sub.0] = [SIGMA]([l.sub.x][m.sub.x]); T = [SIGMA](x[l.sub.x][m.sub.x])/[SIGMA]([l.sub.x][m.sub.x]); [r.sub.m] = ln[R.sub.0]/T; [lambda] = [e.sup.rm]; and Dt = ln (2)/[r.sub.m].

2.4. Data analysis

The data of biological parameters were subjected to Taylor's Power Law (Taylor, 1984) for homogenization of the means and reduction of the variances to indicate the best data transformation using arcsin [square root of (x/100)] for the parameters sex ratio and egg viability. Analysis of variance (SAS INSTITUTE, 2000) 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., 2000), using SAS (SAS INSTITUTE, 2000) software, based on the jackknife method for estimating the parameters, confidence intervals, and to allow treatment comparisons.

3. Results

The duration of the second ([F.sub.2;15] = 0.26; P>0.05), third ([F.sub.2;15] = 3.64; P>0.05), fourth ([F.sub.2;15] = 2.13; P>0.05), and fifth ([F.sub.2;15] = 0.43; P>0.05) instars and the nymph period ([F.sub.2;15] = 0.38; P>0.05) of P. nigrispinus fed on P. xylostella larvae on different Brassicaceae were similar. However, nymph viability ([F.sub.2;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 (F215 = 1.75) was similar between treatments, 29.18 (cabbage) to 41.75 (kale) P. xylostella larvae per nymph of the predator (Table 1).

The mean weight of fifth-instar nymphs (F = 0.68; P>0.05) and newly emerged females ([F.sub.2;15] = 0.45; P>0.05) as well as the sex ratio ([F.sub.2;10] = 1.04; P>0.05) of insects were similar in all treatments. However, newly emerged males ([F.sub.2;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).

The parameters eggs per female ([F.sub.2;27] = 6.41; P<0.01), number of ovipositions ([F.sub.2;27] = 6.59; P<0.01) and eggs per egg mass ([F.sub.2;27] = 3.56; P<0.05) differed between treatments with higher for P. nigrispinus nymphs fed on broccoli. The incubation period ([F.sub.2;27] = 0.70; P>0.05) and viability ([F.sub.2;27] = 1.85; P>0.05) were not different between treatments (Table 3).

The number of eggs per female of this predator ([F.sub.2;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 ([F.sub.2;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 ([F.sub.2;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 ([F.sub.2;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 ([F.sub.2;29] = 8.19; P<0.01), male ([F.sub.2;29] = 15.80; P<0.01) and female ([F.sub.2;29] = 18.42; P<0.01) longevities differed, with higher values of the predator with broccoli (Table 4).

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 ([R.sub.0]) (75.3 females/female) and generation time (T) (37.6 days) of this predator were higher with broccoli. The intrinsic population increase rate ([r.sub.m]), finite population increase rate (X) and the time required for population doubling (TD) were similar between the Brassicacea cultivars (Table 5).

4. Discussion

Development and reproduction ofP 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., 2001). Thus, the reproduction and population growth rates of this insect are high when fed on prey and plants (Guedes et al., 2007).

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., 2011).

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., 2007). 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., 2000).

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., 2004b).

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., 2011). 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., 1999; Oliveira et al., 2002).

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., 2011), Alabama argillacea (Huebner, 1818) (Lepidoptera: Noctuidae) on cotton (348.10) (Oliveira et al., 2002), and with T. molitor (296.66; 325.00) (Oliveira et al., 2004b; Espindula et al., 2006), Diatraea saccharalis (Fabricius, 1794) (Lepidoptera: Pyralidae) (97.12) (Vacari et al., 2007) and T. arnobia (57.00) on Eucalyptus (Holtz et al., 2006; Holtz et al., 2007). 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., 1998), allowing them to maintain their longevity (Valicente and O'Neil, 1995; Zanuncio et al., 2004). 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., 2002). 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, 2004). 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.


The authors gratefully acknowledge the scholarships granted by the Coordenacao de Aperfeicoamento de Pessoal de Nivel Superior (CAPES) and the Conselho Nacional de Desenvolvimento Cientifico e Tecnologico (CNPq) and thank the Universidade Estadual Paulista for the infrastructure.


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J. F J. Grigolli (a), *, M. M. Kubota Grigolli (b), D. G. Ramalho (c), A. L. Martins (d), A. M. Vacari (b), S. A. De Bortoli (b)

(a) Fundacao MS, CP 137, CEP 79150-000, Maracaju, MS, Brazil

(b) Faculdade de Ciencias Agrarias e Veterinarias--FCAV, Universidade Estadual Paulista--UNESP, Via de Acesso Prof. Paulo Donato Castellane, s/n, CEP 14884-900, Jaboticabal, SP, Brazil

(c) Faculdade de Filosofia, Ciencias e Letras de Ribeirao Preto--FFCLRP, Universidade de Sao Paulo--USP, Avenida Bandeirantes, 3900, Monte Alegre, CEP 14040-901, Ribeirao Preto, SP, Brazil

(d) Universidade Federal do Parana--UFPR, CP 19020, CEP 81531-980, Curitiba, PR, Brazil

* e-mail:

Received: October 8, 2015--Accepted: May 16, 2016--Distributed: November 31, 2017
Table 1. Duration of nymph stages (days), nymph period (days), nymph
survival (%), and prey consumption (mean [+ or -] SE) by Podisus
nigrispinus (Heteroptera: Pentatomidae) nymphs fed on Plutella
xylostella (Lepidoptera: Plutellidae) larvae with leaves of three
Brassicacea cultivars. Jaboticabal, Sao Paulo, Brazil, 2012.

Treatament   Nymph Stages
                  2[degrees]                   3[degrees]

Kales        4.14 [+ or -] 0.22 (a)   2.73 [+ or -] 0.98 (a)
Cabbage      4.10 [+ or -] 0.75 (a)   4.18 [+ or -] 1.47 (a)
Broccolis    3.95 [+ or -] 0.47 (a)   2.57 [+ or -] 0.54 (a)

Treatament   Nymph Stages
                 4[degrees]                     5[degrees]

Kales        4.12 [+ or -] 1.10 (a)   5.90 [+ or -] 1.12 (a)
Cabbage      3.10 [+ or -] 0.46 (a)   5.36 [+ or -] 1.01 (a)
Broccolis    3.87 [+ or -] 0.61 (a)   5.85 [+ or -] 0.73 (a)

Treatament   Nymphal                   Nymph
             Period                    Survival

Kales        18.90 [+ or -] 1.65 (a)   56.67 [+ or -] 18.05 (b)
Cabbage      18.74 [+ or -] 1.42 (a)   61.67 [+ or -] 14.41 (b)
Broccolis    18.23 [+ or -] 1.00 (a)   80.00 [+ or -] 12.65 (a)

Treatament   Prey

Kales        41.75 [+ or -] 13.72 (a)
Cabbage      29.18 [+ or -] 8.04 (a)
Broccolis    31.55 [+ or -] 9.49 (a)

Means followed by the same letter per column did not differ by Tukey's
test (P<0.05).

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

Treatament   Weight
             5th-instar                Males

Kales        17.71 [+ or -] 2.94 (a)   33.49 [+ or -] 7.58 (a)
Cabbage      17.71 [+ or -] 4.57 (a)   23.58 [+ or -] 9.65 (b)
Broccolis    19.70 [+ or -] 4.03 (a)   28.61 [+ or -] 4.86 (ab)

Treatament   Weight                     Sex Ratio (1)

Kales        41.49 [+ or -] 8.50 (a)    0.52 [+ or -] 0.24 (a)
Cabbage      39.02 [+ or -] 13.88 (a)   0.68 [+ or -] 0.22 (a)
Broccolis    43.35 [+ or -] 7.05 (a)    0.44 [+ or -] 0.31 (a)

Means followed by the same letter per column did not differ by Tukey's
test (P<0.05). (1) Original data. Data were transformed to arcsin
[square root of (x/100)] for statistical analysis (Taylor, 1984).

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 [+ or -] SE) of Podisus nigrispinus (Heteroptera:
Pentatomidae) fed on Plutella xylostella (Lepidoptera: Plutellidae)
larvae with leaves of three Brassicacea cultivars. Jaboticabal, Sao
Paulo, Brazil, 2012.

Treatament   Eggs/Female                 Clutches

Kales        196.10 [+ or -] 57.53 (b)   5.80 [+ or -] 1.77 (b)
Cabbage      191.90 [+ or -] 38.10 (b)   2.90 [+ or -] 2.46 (b)
Broccolis    467.90 [+ or -] 87.12 (a)   13.10 [+ or -] 4.96 (a)

Treatament   Incubation Period        Viability (1)

Kales        5.12 [+ or -] 0.80 (a)   55.60 [+ or -] 11.42 (a)
Cabbage      5.05 [+ or -] 0.73 (a)   63.79 [+ or -] 13.03 (a)
Broccolis    5.34 [+ or -] 0.86 (a)   59.69 [+ or -] 9.75 (a)

Treatament   Eggs/Clutch

Kales        23.12 [+ or -] 0.54 (b)
Cabbage      17.74 [+ or -] 0.04 (b)
Broccolis    35.76 [+ or -] 0.89 (a)

Means followed by the same letter per column did not differ by Tukey's
test (P<0.05). (1) Original data. Data were transformed to arcsin
[square root of (x/100)] for statistical analysis (Taylor 1984).

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 [+ or -] SE) fed on P. xylostella larvae with leaves of
three Brassicacea cultivars. Jaboticabal, Sao Paulo, Brazil, 2012.

Treatament   Consumption       Longevity (days)
                               Male             Female
Kales        182.21 [+ or -]   25.00 [+ or -]   17.43 [+ or -]
             21.29 (b)         4.41 (b)         1.81 (b)
Cabbage      172.50 [+ or -]   8.00 [+ or -]    23.00 [+ or -]
             30.34 (b)         4.31 (c)         2.94 (b)
Broccolis    306.21 [+ or -]   42.29 [+ or -]   37.86 [+ or -]
             31.09 (a)         6.90 (a)         1.89 (a)

Means followed by the same letter per column did not differ by Tukey's
test (P<0.05).

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

Parametro (1)                  Kales

[R.sub.0] (female/female)      57.1 [+ or -] 14.08 (b) (2)
T (days)                       29.1 [+ or -] 6.89 (b)
[r.sub.m] (femeas/femea*dia)   0.139 [+ or -] 0.0406 (a)
A (females/females/day)        1.149 [+ or -] 0.0463 (a)
TD (days)                      4.9 [+ or -] 1.62 (a)

Parametro (1)                  Cabbage

[R.sub.0] (female/female)      47.6 [+ or -] 15.96 (b)
T (days)                       28.8 [+ or -] 7.49 (b)
[r.sub.m] (femeas/femea*dia)   0.139 [+ or -] 0.0272 (a)
A (females/females/day)        1.149 [+ or -] 0.0312 (a)
TD (days)                      4.9 [+ or -] 0.98 (a)

Parametro (1)                  Broccolis

[R.sub.0] (female/female)      75.3 [+ or -] 13.90 (a)
T (days)                       37.6 [+ or -] 7.23 (a)
[r.sub.m] (femeas/femea*dia)   0.115 [+ or -] 0.0159 (a)
A (females/females/day)        1.122 [+ or -] 0.0179 (a)
TD (days)                      5.9 [+ or -] 0.79 (a)

(1) [R.sub.0] = [SIGMA]([l.sub.x][m.sub.x]), for the number of eggs
per female per generation, where [l.sub.x] = proportion of mated
females alive at age x; [m.sub.x] = age-specific fecundity rates
multiplied by the sex ratio (0.52, 0.68, and 0.43 sex ratio on kale,
cabbage, and broccoli, respectively); T =
[SIGMA](x[l.sub.x][m.sub.x])/[SIGMA]([l.sub.x][m.sub.x]); [r.sub.m] =
ln [R.sub.0]/T; and [lambda] = [e.sup.rm]; (2) Means [+ or -] IC
followed by the same letter per row do not differ from each other by
the "t" paired comparison test by the Jackknife method.
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Title Annotation:Original Articlekkkkkk ao
Author:Grigolli, J.F.J.; Grigolli, M.M. Kubota; Ramalho, D.G.; Martins, A.L.; Vacari, A.M.; De Bortoli, S.A
Publication:Brazilian Journal of Biology
Date:Nov 1, 2017
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