Life history and cost analysis for continuous rearing of Perillus bioculatus (Heteroptera: Pentatomidae) on a zoophytogenous artificial diet

The impact of a zoophytogenous, insect-free artificial diet on the developmental rate, life history parameters, and fertility was examined over 11 consecutive generations for domesticated Perillus biocullatus (F.) (Heteroptera: Pentatomidae). This study showed that when fed an insect-free artificial diet during both the nymphal and adult stages, developmental times were prolonged, and the net reproductive rates (R0) and the intrinsic rates of increase (r(m)) were significantly lower than when fed larval Trichoplusia ni at both nymphal and adult stages. Moreover, the cost to rear P. bioculatus on the artificial diet approached 1.1 times the cost of rearing P. bioculatus on natural prey. These results demonstrate the effectiveness and potential cost-savings of the zoophytogenous artificial diet for rearing a beneficial pentatomid.     

Life table parameters, reproductive rate, intrinsic rate of increase, and estimated cost of rearing Podisus maculiventris (Heteroptera: Pentatomidae) on an artificial diet.

The impact of an insect-free artificial diet provided at nymphal and/or adult stage upon the developmental rate, life table parameters, and fertility table parameters was examined for Podisus maculiventris (Say). This study showed that when fed an insect-free artificial diet during both the nymphal and adult stage, developmental time was prolonged, preoviposition period was extended, and reproductive rate (R0) and intrinsic rate of increase (r) were significantly lower than when fed larval insect prey at both nymphal and adult stages. Additionally, feeding larval prey to adults reared as nymphs on an artificial diet significantly increased the proportion of fertile females, the number of eggs laid by mated females, the reproductive rate and intrinsic rate of increase, but the mean generation time was not significantly different. Likewise, feeding artificial diet to adults reared on larval prey resulted in a significant reduction in reproductive rate and intrinsic rate of increase. The "realized" cost to rear P. maculiventris on the artificial diet was calculated (as the cost to double the population size) using raw material cost, fertility table parameters and doubling time values. Raw material cost for rearing P. maculiventris colony on Trichoplusia ni (Hübner) (Lepidoptera: Noctuidae) was only 1.4 times higher than the cost of artificial diet raw materials required to rear the same size colony. However, the realized cost of rearing was 3.5 times higher when rearing on artificial diet because of the prolonged developmental time and reduced reproductive output. The cost efficiency of rearing a beneficial insect on an artificial diet that decreases the intrinsic rate of increase of a colony is discussed, as well as the advantages and disadvantages of supplementing adult diets with natural prey at the reproductive stage.     

Toxicity of Selected Insecticides to the Spined Soldier Bug, Podisus maculiventris (Heteroptera: Pentatomidae)

Susceptibility of Podisus maculiventris to the insect growth regulator teflubenzuron, the carbamate methomyl, the pyrethroid deltamethrin, and the bioinsecticide Bacillus thuringiensis subsp. kurstaki (Bactospeine) was evaluated in the laboratory. Newly-moulted fourth instars and seven-day-old female adults were exposed to formulated materials of each compound via ingestion for 48 h. Teflubenzuron was highly toxic to fourth instars (LC 50 = 14.7 mg a.i. l -1 ) of the predator, but proved to be harmless to female adults. Both fourth instars and females suffered the highest mortality when they were exposed to methomyl (LC 50 = 5.4 and 10.6 mg a.i. l -1 , respectively). Deltamethrin was relatively safe for the predator in either stage; however, fourth instars were more tolerant to the pyrethroid than females (LC 50 = 158.8 and 43.4 mg a.i. l -1 , respectively). Neither fourth instars nor females were affected by B. thuringiensis at 10 000 mg formulated material l -1 . Reproductive capacity of the predator was also examined when applying field concentrations of teflubenzuron (200 mg a.i. l -1 ) or deltamethrin (12.5 mg a.i. l -1 ) via ingestion. Treatment with deltamethrin only prolonged preoviposition period. A marked decline in egg hatch was observed when the insects were exposed to teflubenzuron compared with the control (7 vs 63%, respectively). Fourth and fifth instars that had ingested sublethal doses of teflubenzuron demonstrated longer developmental times than did those of the control. Ingestion experiments suggest that use of deltamethrin and B. thuringiensis may be compatible with releases of P. maculiventris . In contrast, populations of the predator may be harmed when methomyl or teflubenzuron are applied.     

Suppression of Colorado potato beetle infestation by pheromone-mediated augmentation of the predatory spined soldier bug, Podisus maculiventris (Say) (Heteroptera: Pentatomidae)

1 Hardware and protocols were tested to enable individual growers and insectary operators to mass-produce predatory spined soldier bugs (SSBs), Podisus maculiventris (Say) (Heteroptera: Pentatomidae: Asopinae), for augmentative biological control. Using pheromone-based technology, an average of 1775 female SSBs (potentially as many as 1.6 million offspring) were captured each year during 2–3 weeks in early spring. 2 Data for the first 2 years of a 3-year project to use SSB for biological suppression of the Colorado potato beetle (CPB), Leptinotarsa decemlineata (Say) (Coleoptera: Chrysomelidae), verified earlier research showing that augmentation of SSB (～5 nymphs/plant) can significantly suppress CPB infestations. In the third year, wild SSBs were transferred directly from pheromone traps to mid-plot nursery cages having a mesh size chosen to retain the adult predators but allow their offspring to escape. Pheromone dispensers were placed peripherally to promote dispersal of young predators and immigration of new wild spined soldier bug adults. Pheromone-mediated augmentation using porous nursery cages and pheromone dispensers was less labour-intensive than earlier methods, and resulted in significantly improved potato yield. 3 Trapping SSB adults early in the spring protects them from parasitization by tachinid flies and scelionid wasps that use the pheromone to facilitate host-finding. The compatibility of pheromone-mediated predator augmentation/conservation with implementation of transgenic plants, imidacloprid insecticide, and other biocontrol methods is discussed.     

Comparison of susceptibility of pest Euschistus servus and predator Podisus maculiventris (Heteroptera: Pentatomidae) to selected insecticides

Susceptibility of the brown stink bug, Euschistus serous (Say), and the spined soldier bug, Podisus maculiventris (Say), to acetamiprid, cyfluthrin, dicrotophos, indoxacarb, oxamyl, and thiamethoxam, was compared in residual and oral toxicity tests. Generally, susceptibility of P. maculiventris to insecticides was significantly greater than or not significantly different from that of E. servus. Cyfluthrin and oxamyl were more toxic to the predator than to E. servus in residual and feeding tests, respectively. Dicrotophos is the only compound that exhibited both good residual and oral activity against E. servus, but even this toxicant was more toxic to the predator than to the pest in oral toxicity tests. Feeding on indoxacarb-treated food caused high mortality for both nymphs and adults of P. maculiventris. In contrast, E. servus was unaffected by feeding on food treated with this compound. Insecticide selectivity to P. maculiventris was detected only with acetamiprid for adults in residual toxicity tests and for nymphs in oral toxicity tests. Because insecticide selectivity to P. maculiventris was limited, it is extremely important to conserve P. maculiventris in cotton fields by applying these insecticides for control of brown stink bugs only when the pest reaches economic threshold.     

Effects of temperature on predation by the stinkbugs Picromerus bidens and Podisus maculiventris (Heteroptera: Pentatomidae) on noctuid caterpillars

Environmental risks associated with the use of non-indigenous organisms for augmentative biological control have received growing attention. In Europe, the native pentatomid predator Picromerus bidens (Linnaeus) has been considered a potential alternative to the North American pentatomid Podisus maculiventris (Say) for the control of lepidopteran, coleopteran and hymenopteran defoliator pests. In the current study, prey consumption and developmental duration of the predatory stages of P. bidens and P. maculiventris were investigated at three temperatures (18, 23 and 27 degrees C) in the laboratory using caterpillars of Spodoptera littoralis as prey. Development time from second to fifth instar was longer for P. bidens than for P. maculiventris, taking on average 17-44 and 14-32 days, respectively, at the different temperatures. Total nymphal consumption of fourth instar S. littoralis caterpillars indicated a greater voracity of P. bidens as compared with P. maculiventris at both the low and high temperatures tested (18 and 27 degrees C). At 23 degrees C, however, the predation rate of P. maculiventris nymphs exceeded that of P. bidens nymphs. Effect of temperature on the functional response of P. bidens to densities of fourth instar Spodoptera exigua was assessed on potted green bean plants. Female adults of P. bidens exhibited a type II functional response at 18 and 23 degrees C but a type III response at 27 degrees C. Searching efficiency was not affected by temperature but handling time decreased from 4.2 to 1.4 h as temperature increased from 18 to 23 degrees C. However, the predator spent twice as much time handling prey at 27 degrees C (2.9 h) than at 23 degrees C. This study indicates high predation rates of P. bidens at a wide range of temperatures and suggests that the species may be a valuable asset for the biological control of defoliating caterpillars, provided that obstacles to its mass production can be overcome.     

Impact of Genetically Modified Potato Expressing Plant-Derived Insect Resistance Genes on the Predatory Bug Podisus maculiventris (Heteroptera: Pentatomidae)

The effects of the transgene proteins Galanthus nivalis agglutinin (GNA) and cowpea trypsin inhibitor (CpTI) on the predatory stinkbug Podisus maculiventris were studied under laboratory conditions. When the P. maculiventris were provided with tomato moth (L. oleracea) larvae injected with either GNA or CpTI at a dose of 10 μg day^-1, growth was significantly reduced and, as a consequence, female adult weight was also significantly reduced. For GNA-fed and CpTI-fed P. maculiventris, this weight reduction was 11.3 and 16.6%, respectively. Males, however, were not significantly affected. Female bugs that had not been exposed to the transgene proteins as nymphs, however, showed no reduction in fecundity when these adults were provided with prey injected with either GNA or CpTI at this same dose. When provided with hosts that had been reared on transgenic plants expressing either GNA or CpTI, no effects on the survival of nymphs were observed and only small, largely non-significant, reductions in weights were recorded throughout preadult development. Male nymphs fed on the GNA-fed prey did, however, exhibit a significant lengthening of preadult development of 0.8 days. The subsequent adults showed significantly reduced egg production for the GNA treatment. The results indicate that P. maculiventris may suffer some indirect adverse effects from foraging for prey in crops expressing either GNA or CpTI, due to prey being of inferior quality, rather than to direct toxicity of the transgene products themselves.     

Effect of diet on male reproductive tract of Podisus nigrispinus (Dallas) (Heteroptera: Pentatomidae).

The morphology and histology of the reproductive tract of males of the predator Podisus nigrispinus (Dallas) fed on different diets were studied. P. nigrispinus was fed on diets of: larvae of Alabama argillacea (Hübner), Tenebrio molitor L., Musca domestica L., and an artificial diet. The male reproductive tract, independent of diet, showed testes with intense red coloration in a compact, circular, or slightly oval structure. The vasa deferentia were similar in color to the testes and formed long filaments, which joined with the yellow-cream colored ejaculatory duct. The morphological characteristics of the male reproductive tract were similar under all diets, except for the artificial one. The histological studies demonstrated that independent of the diet the testes of P. nigrispinus were composed of four to six follicles. The testes with six follicles generally had four developed and two atrophied follicles. The morphological and histological differences of the testes of P. nigrispinus when fed with different prey are presented and discussed.     

The control of Malpighian tubule secretion in a predacious hemipteran insect, the spined soldier bug Podisus maculiventris (Heteroptera, Pentatomidae)

Spined soldier bugs, Podisus maculiventris, are heteropteran insects that feed voraciously on other insects, particular the soft bodied larval forms of Lepidoptera and Coleoptera. The response of P. maculiventris Malpighian tubules (MTs) to serotonin and known diuretic and antidiuretic peptides has been investigated, and is compared with that of MT from the hematophagous and phytophagous heteropteran bugs Rhodnius prolixus and Acrosternum hilare, respectively. A CRF-related peptide diuretic hormone (DH) from the termite Zootermopsis nevadensis (Zoone-DH) stimulated MT secretion, which was reversed by a member of the CAP_2b family of peptides from A. hilare (Acrhi-CAP_2b-2), an antidiuretic effect. Serotonin had no effect on secretion, neither did a representative calcitonin-like DH, kinin, tachykinin-related peptide, and an antidiuretic factor from the mealworm Tenebrio molitor (Tenmo-ADFb) in both P. maculiventris or A. hilare. Serotonin is a DH in R. prolixus, and its lack of effect on MT from P. maculiventris and A. hilare suggests this is an adaptation to hematophagy. On the other hand, the antidiuretic activity of members of the CAP_2b family in all three bugs is consistent with this being a heteropteran feature rather than a specialism for hematophagy.     

Development time and predation rate of Podisus maculiventris (Hemiptera: Pentatomidae) feeding on Microtheca ochroloma (Coleoptera: Chrysomelidae)

Microtheca ochroloma St?l is a beetle native to South America and was introduced to the United States in 1945. Since then, M. ochroloma has become a serious pest in crucifer crops because of the lack of natural enemies. The objective of this study was to measure the predation rate and development time of the commercially available predator Podisus maculiventris (Say) feeding on M. ochroloma at four constant temperatures in the laboratory as a first step to evaluating the predator's capability as a biological control agent of the pest. Nymphal development of P. maculiventris increased from 23 d at 25°C to 99 d at 15°C. There was no development of first instar or egg hatch at 10°C. Number of fourth-instar M. ochroloma killed during nymphal development varied significantly from 65 at 15°C to 53 at 20°C because of length of the nymphal period. A mean total of 741 eggs of M. ochroloma were consumed during nymphal development at 25°C. Adult P. maculiventris preyed on nine and 12 times more fourth-instar M. ochroloma during 10 d at 20° and 25°C, respectively, than at 15°C. We conclude that P. maculiventris can develop successfully on a diet of eggs or fourth-instar M. ochroloma, but its predation and development rates will be significantly curtailed during the cool months from November to March when M. ochroloma is a key pest of organically grown crucifers in Florida.     

Oviposition pattern of the predator Podisus nigrispinus (Heteroptera: Pentatomidae) under different temperatures

The daily reproductive rate of Podisus nigrispinus (Dallas) (Heteroptera: Pentatomidae) fed with Alabama argillacea (Hübner) (Lepidoptera: Noctuidae) larvae was studied at constant temperatures of 20, 23, 25, 28, 30 and 33±0.2°C, relative humidity of 60±10% and photoperiod of L:D 14:10. Daily reproductive rate of P. nigripinus was affected by age of this predator. Each P. nigrispinus female laid 5.3 (20°C) to 19.9 eggs/day (28°C) which developed into 4.3–16.5 nymphs, respectively. Highest daily reproductive rate of P. nigrispinus was recorded at 28 and 30°C for 5–30-day-old females. This predator showed higher daily reproductive rate than its prey A. argillacea at 25°C. It was also able to reproduce at temperatures from 20 to 33°C with maximum daily reproductive rate between 25 and 30°C. These results are important for optimizing mass rearing of P. nigrispinus in the laboratory.     

Development of a dry artificial diet for Nezara viridula (L.) and Euschistus heros (Fabricius) (Heteroptera: Pentatomidae)

Artificial diets prepared with wheat germ, soybean protein, dextrosol, potato starch, sucrose, cellulose, soybean or sunflower oil, and vitamin solution for rearing Nezara viridula (L.) and Euschistus heros (Fabricius) were tested under controlled temperature (25 +/- 1 degrees C), RH (60 +/- 10%), and photophase (14h). Three diets were tested and compared with the natural diet privet [soybean and peanut seeds and privet Ligustrum lucidum Ait. fruit (Oleaceae)]. All three artificial diets allowed full development. The diet containing sunflower oil was the most suitable for N. viridula while E. heros developed better on a diet composed of soybean oil. Data indicated that the artificial diets were inferior to the natural diet. The artificial diets were more adequate for E. heros.     

Reproductive Strategy of Podisus rostralis (Stal) (Heteroptera: Pentatomidae) Females Under Different Feeding Intervals

The reproduction and survival of Podisus rostralis was evaluated under different feeding intervals using Tenebrio molitor larvae as food and a continuous supply of bean slices. There was a linear relationship between the pre-oviposition period and the periods without feeding. Females fed at intervals of 1-4 days laid their first egg mass 8-10 days after emergence, while those fed every 8 and 16 days did so after 13.6 and 20 days respectively. The oviposition period, number of egg masses, total number of eggs, number of eggs/egg mass, total number of nymphs and rate of egg consumption/day showed negative linear correlations with the increase in feeding interval. The longevity of P. rostralis was not affected by feeding interval (P> 0.05). The present results suggest a type of trade-off, where longevity is maintained at the expense of reproduction. This behaviour or attribute of P. rostralis can contribute to its establishment and survival in an environment of fluctuating food supply.     

A meat-based diet for rearing the predatory stinkbugsPodisus maculiventris andPodisus sagitta [Het.: Pentatomidae]

A diet based on bovine meat was evaluated as an alternative food source for rearing the predatory bugsPodisus maculiventris (Say) andPodisus sagitta (Fabricius). Thus far, 7 and 5 continuous generations of the respective species have been reared on this diet. In comparison to rearing on larvae of the greater wax moth,Galleria mellonella (L.), however, nymphal development was prolonged with 15–40% and adult weights were lower, reaching 72–82% of the control weights. Fecundity of females reared on the meat diet was reduced to about 1/3–1/2 of that of the control, but egg weight and egg fertility were comparable with those in cultures fed live prey. Results obtained for laboratory rearing on this medium were generally better forP. maculiventris than forP. sagitta.      

Ultrastructure and immunolocalization of digestive enzymes in the midgut of Podisus nigrispinus (Heteroptera: Pentatomidae)

The predatory stinkbug Podisus nigrispinus has been utilized in biological control programs. Its midgut is anatomically divided into anterior, middle and posterior regions, which play different roles in the digestive process. We describe the midgut ultrastructure and the secretion of digestive enzymes in the midgut of P. nigrispinus. Midguts were analyzed with transmission electron microscopy and the digestive enzymes amylase, cathepsin L, aminopeptidase and α-glucosidase were immunolocalized. The ultrastructural features of the digestive cells in the anterior, middle and posterior midgut regions suggest that they play a role in digestive enzyme synthesis, ion and nutrient absorption, storage and excretion. The digestive enzymes have different distribution along the midgut regions of the predator P. nigrispinus. Amylase, aminopeptidase and α-glucosidase occur in three midgut regions, whereas cathepsin L occurs in the middle and posterior midgut regions. The anterior midgut region of P. nigrispinus seems to play a role in water absorption, the middle midgut may be involved in nutrient absorption and the posterior midgut region is responsible for water transport to the midgut lumen.     

Functional response of the predators Podisus maculiventris (Say) and Podisus nigrispinus (Dallas) (Het., Pentatomidae) to the beet armyworm, Spodoptera exigua (Hübner) (Lep., Noctuidae): ef fect of temperature

Predation abilities of Podisus maculiventris and Podisus nigrispinus on caterpillars of the beet armyworm, Spodoptera exigua (Hübner), were compared at three different temperatures (18, 23 and 27°C) by performing functional response tests. In both species, predation capacity was a function of temperature and prey density: more prey were captured as temperature and number of prey offered increased. Results indicated that type II and III functional responses provided the best fit to the data obtained for P. nigrispinus at 18 and 23°C, and at 27°C, respectively. However, the data for P. maculiventris showed a better fit to type II at 18°C and to type III at higher temperatures. In both pentatomids the handling time decreased with increasing temperature. At higher temperatures, P. nigrispinus demonstrated greater predation rates than P. maculiventris . The implications of these findings for the control of caterpillar pests in glasshouses are discussed.     

Predatory behaviour of Podisus nigrispinus (Heteroptera: Pentatomidae) on different densities of Anticarsia gemmatalis (Lepidoptera: Noctuidae) larvae

The functional response of the predatory bug Podisus nigrispinus (Dallas) (Heteroptera: Pentatomidae) feeding on its prey, Anticarsia gemmatalis Hübner (Lepidoptera: Noctuidae), was studied in a greenhouse compartment. Each cage enclosed three soybean plants plus two, four, six, eight, 10, 12 or 14 prey larvae. One adult predator was released and kept inside the cages for 24h. The predation rate of adult male P. nigrispinus was highest at densities of eight or more A. gemmatalis larvae with a handling time of 5.76h and an attack rate of 0.68h^?1. Adult females had higher predation rates on plants with 10 or more A. gemmatalis larvae, with a handling time of 3.84h and an attack rate of 0.65h^?1. The maximum number of larvae consumed by males and females of this predator were 4.1 and 6.0 per day, respectively, in groups of three plants. The results suggest that P. nigrispinus may be used in biological control programmes against A. gemmatalis in soybean fields.     

Development and reproduction of Podisus distinctus (Heteroptera: Pentatomidae) fed on larva of Bombyx mori (Lepidoptera: Bombycidae).

Biological control has been reducing the use of chemical products against insect pests, especially predatory Pentatomidae. Species of this group can present high variations in their life cycle as a result of their diet. Thus, the objective of this research was to study nymph development and reproduction of Podisus distinctus (St?l, 1860) (Heteroptera: Pentatomidae) fed on Bombyx mori L., 1758 (Lepidoptera: Bombycidae) larvae (T1), compared to those fed on Tenebrio molitor L., 1758 (Coleoptera: Tenebrionidae) (T2) and Musca domestica L., 1758 (Diptera: Muscidae) larvae (T3) at a temperature of 25 +/- 0.5 degrees C, relative humidity of 70 +/- 2%, and photophase of 12 h. Predators fed on B. mori showed duration of the nymph phase (18.68 +/- 1.02) similar to those fed on T. molitor (18.32 +/- 1.49). Pre-oviposition and oviposition periods and number of egg masses, besides eggs and nymphs per female, were higher with B. mori (5.83 +/- 2.02; 15.00 +/- 7.40; 8.42 +/- 1.84; 296.69 +/- 154.75; and 228.55 +/- 141.04, respectively) while longevity of males and females of P. distinctus was 25.76 +/- 16.15 and 35.00 +/- 16.15 days with T. molitor, and 20.57 +/- 13.60 and 23.46 +/- 12.35 days with B. mori, respectively.     

Degeneration and cell regeneration in the midgut of Podisus nigrispinus (Heteroptera: Pentatomidae) during post-embryonic development

Cell death, proliferation, and differentiation in some developmental stages of insects have been studied in the midgut of ametabolous, which undergo only continuous growth, and holometabolous, which undergo complete metamorphosis. However, in hemimetabolous insects, evolutionarily intermediate between ametabolous and holometabolous, midgut reorganization during the post-embryonic development has been poorly studied. The present study evaluates the post-embryonic development of the midgut of a hemimetabolous insect, Podisus nigrispinus, to test the hypothesis that these insects have programmed cell death and proliferation followed by differentiation of regenerative cells during midgut growth from nymphs to adult. The morphometrical data showed a 6-fold increase in midgut length from the first instar nymph to the adult, which did not result from an increase in the size of the midgut cells, suggesting that the growth of the midgut occurs by an increase in cell number. Cell death was rarely found in the midgut, whereas proliferation of regenerative cells occurred quite frequently. The growth of the midgut of P. nigrispinus appears to result from the proliferation of regenerative cells present in the epithelium; unlike ametabolous and holometabolous insects, the midgut of P. nigrispinus does not undergo extensive remodeling, as shown by the low frequency of digestive cell death.     

Morphology and preliminary enzyme characterization of the salivary glands from the predatory bug Podisus nigrispinus (Heteroptera: Pentatomidae)

Podisus nigrispinus (Dallas) is a common predator in agricultural and natural systems in Neotropical America. Its feeding strategy involves extra-oral digestion and to better understand this process its salivary glands were extracted and subjected to morphological and preliminary enzyme characterization. The salivary glands of P. nigrispinus are formed by a pair of main and accessory gland complexes. The main salivary glands are further divided into an anterior and a posterior lobe. The compartmentalization of the salivary gland complex is likely to be important for the production, activation and release of the digestive enzymes used in the extra-oral digestion of prey items. Proteases and lipase, important digestive enzymes involved in zoophagy, were detected in the salivary glands of P. nigrispinus. The prevailing trypsin-like protease activity was characterized by using the serine-protease substrate N-alpha-benzoyl-L-Arg-p-nitroanilidine (L-BApNA) and the trypsin inhibitors tosyl-L-lysine chloromethyl ketone (TLCK) and benzamidine. The KM value obtained for trypsin-like activity was 1.57 mm and the different peaks of optimum pH and temperature activity suggest the presence of multiple forms of this enzyme in P. nigrispinus. Detection of amylase activity in the salivary glands of this predator suggests its ability to digest starch and obtain nutrients from plants, which may have adaptative value under prey scarcity.