Attack efficacy by Podisus nigrispinus and Brontocoris tabidus on Thyrinteina arnobia with different pre-release strategies

doi:10.21203/rs.3.rs-1497570/v1

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Attack efficacy by Podisus nigrispinus and Brontocoris tabidus on Thyrinteina arnobia with different pre-release strategies

https://doi.org/10.21203/rs.3.rs-1497570/v1

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Predatory stink bugs are important biological control agents in agricultural and forest crops. The use of these natural enemies by companies, growers and research centers has been an important tactic to control caterpillar pest outbreaks. Podisus nigrispinus (Dallas) and Brontocoris tabidus (Signoret) (Heteroptera: Pentatomidae) were kept for 24, 36, or 48 hours without food, and the time taken by theses predators for the first attack and to kill a sixth-instar Thyrinteina arnobia (Stoll) (Lepidoptera: Geometridae) larvae, as well as the number of attacks during four-hour period were evaluated. The starving periods that the predators were subjected to affect the time for the first attack and also the number of attacks. Podisus nigrispinus and B. tabidus attacked faster when kept for 36 and 48 hours without food, respectively. The time taken for the first attack was similar for all periods for both predators, but B. tabidus was faster than P. nigrispinus during all periods. Brontocoris tabibus’ constant feeding on the plant may explain its attack efficiency and capacity for controlling of the T. arnobia caterpillar, because water obtained during phytophagy is important for the process of extra-oral digestion of Asopinae predators.

Forestry

Control

Death time

extra-oral digestion

pre-release strategy

Insects may reduce wood quality, delay development and cause the death of eucalyptus plants (Santos et al. 2008). Thyrinteina arnobia (Stoll) (Lepidoptera: Geometridae) is considered the main species of Lepidoptera defoliator for this plant (Zanuncio et al. 2006), due to its high voracity, especially during the last two instars (Zanuncio et al. 1993). Plantings attacked by this caterpillar may present less development and tree death, justifying the need for its control (Zanuncio et al. 1994).

Chemical products (Zanuncio et al. 1995), and natural enemies such as parasitoid wasps (Pereira et al. 2008a, b) and Pentatomidae predators (Holtz et al. 2007; Pires et al. 2015) are used to control T. arnobia outbreaks. These methods must be efficient, as this caterpillar has a high reproductive potential, short period of embryonic development and high fertility (Zanuncio et al. 1993), which, associated with defense strategies, makes its control and location in eucalyptus plantations difficult (Soares et al. 2009).

Podisus nigrispinus and Brontocoris tabidus (Heteroptera: Pentatomidae) are important predators for defoliating caterpillars in the agricultural and forestry sector (Lemos et al. 2003; Zanuncio et al. 1994). These bugs and other predatory arthropods perform phytophagy (Coll 1998), a special form of omnivory, sometimes also called zoophytophagy (Lalonde et al. 1999), with plant material supplementing their diet.

Zoophytophagy allows predatory bugs to obtain water, favoring their metabolism and predation behavior (Gillespie and McGregor 2000). Feeding on plant sap is greater during periods of prey scarcity (Holtz et al. 2009), showing that these insects can use plants as a food resource when prey availability is low (Agrawal et al. 1999).

The use of prey and plants has been evaluated to determine their effect on the biology of Heteropteran predators as it can improve nutrition, fecundity, functional response and facilitate extraoral digestion of prey. This is mainly due to the adapted mouthparts and digestive enzyme complex that allow these predators to exercise phytophagy (Sinia et al. 2004; Oliveira et al. 2006).

The extra-oral digestion primarily consists of the phases of injection of salivary content containing toxins and/or digestive enzymes, initial digestion of food and ingestion of liquefied material. This process involves the ingestion of pre-existing substances such as liquids (hemolymph) and the degradation of solids and reduction of the viscosity of insoluble liquids (Cohen 1995). Extraoral digestion allows predators to reduce prey handling time and for smaller individuals to consume relatively larger prey (Kaspari 1990).

The objectives of this study were to verify the effects of 24, 36, and 48 hour-intervals without feeding on the time taken for the first attack of P. nigrispinus and B. tabidus, killing the sixth instar caterpillar of T. arnobia, on the number of attack attempts, and on the ability to control these caterpillars with just one attack. In addition, the size of the mouthparts (mandibular stylets and maxillary setae), important in prey controlling and in the enzymatic activity of amylase, lipase and protease in the salivary content of these predators, were also evaluated.

P. nigrispinus and B. tabidus adults obtained from rearing maintained in eucalyptus plants in the field, up to 15 days after emergence, were used. These predators were fed with pupae of Tenebrio molitor (Linnaeus) (Coleoptera: Tenebrionidae) on a plant of Eucalyptus cloeziana.

Podisus nigrispinus and B. tabidus were individualized in Petri dishes (15 x 1.5 mm) at a temperature of 25 ± 2 oC, 70 ± 10% RH and a 14-hour photoperiod and submitted to 24, 36, and 48 hour-periods without feeding. Then, one sixth instar T. arnobia caterpillar (166.4 ± 0.8 mg) was placed per dish, totaling 30 dishes per predator species and time of day.

The time taken for the first attack, caterpillar death (absence of movements and reflexes), and the number of attempts (prey controlling) were evaluated with 30 repetitions per period without food, during four hours of observation. The results were submitted to analysis of variance with p < 0.05 and the means compared by the Tukey test at 5% probability.

The mouthparts of the predators P. nigrispinus and B. tabidus were evaluated to verify the size of the structures that hold the prey (arrows). The rostrum of three females of each predator was removed and dissected. These structures were metallized and submitted to electron microscope scanning to obtain images and visualize details of the morphology.

Individuals that killed the caterpillar with a single lunge were used to evaluate the time taken to kill the prey and the attack efficiency. The attack efficiency data were submitted to non-parametric analysis by the Wilcoxon test with α < 0.05 to verify the efficiency to control of T. arnobia caterpillars by predators.

Enzymatic activity of Podisus nigrispinus and Brontocoris tabidus: Acquisition of predators and extraction of salivary glands

Twenty pairs of P. nigrispinus and B. tabidus salivary glands were used to evaluate the enzymatic activity of the salivary content of these insects. The salivary glands were removed and transferred to two 2 mL microtubes in the proportion of 20 pairs of glands to 500 µL of 10 − 3 M HCl in an ice bath. These glands were macerated to obtain the crude enzyme extract.

Enzymatic activities in salivary gland extracts of Podisus nigrispinus and Brontocoris tabidus

The amylase, lipase and protease activities of the crude extract from the salivary glands of P. nigrispinus and B. tabidus were evaluated with three replications. Amylase activity was determined with the BIOCLIN enzyme kit (Caraway 1959). This technique consists of incubating 5 µL of glandular extract with 250 µL of starch at 0.4 g/L and 100 mM monophosphate/disodium phosphate buffer, pH 7.0 for seven minutes and thirty seconds at 37 ^oC, followed by reading of the absorbance at 660 nm. Amylase activity, expressed in Amylase Units, represents the total hydrolysis of 100 mg of starch for 30 minutes at 37 ^oC.

Lipase activity was determined with the BIOCLIN enzyme kit (Cherry & Crandall, 1932). The extracts (50 µL) were incubated in 200 µL of 100 mM Tris buffer (hydroxymethylaminomethane), 20 µL of 100 mM DTNB (dithionitrobenzoic acid) and 10 µL of protease inhibitor phenylmethyl sulfonyl fluoride (PMSF) at 37°C for thirty minutes. After two minutes, 20 µl of 200 mM dithiopropanol tributyrate was added to the mixture. After incubation for 30 minutes at 37°C, 400 µL of acetone were added to stop the reaction and the material was centrifuged for five minutes at 3500 rpm in a microcentrifuge. The absorbance of the supernatant was determined at 410 nm. Activity was expressed in IU (International Units), representing the conversion of 1.0 µmol of substrate per minute or formation of 1.0 µmol of product per minute.

Protease activity was evaluated (Erlanger et al., 1961) and the extract was incubated with 5 mM Nα-Benzoyl-L-Arginylp-Nitroanilide (L-BApNA) in 0.05M Tris-HCl buffer, pH 8.0 at 37.5 ^oC. The initial reaction rates were determined by the formation of p-nitroanilide, by measuring the absorbance at 410 nm as a function of time (2:30 minutes), using the molar extinction coefficient 8800 M-1 cm-1 of the product.

Brontocoris tabidus showed a greater ability to control T. arnobia caterpillars than P. nigrispinus (Z = 4.11; α = 0.0002), arround killing 72% of the caterpillars in the first attack, while P. nigrispinus only killed 30%.

The time taken by the predator P. nigrispinus for the first attack on the T. arnobia caterpillar differed between the 24, 36, and 48-hour intervals without food. Podisus nigrispinus was faster at 36 and 48 hours than at 24 hours without food. The period without food affected the time taken for first attack of B. tabidus, these predators without food for 48 hours were faster than those without food for 24 and 36 hours. The time taken for the first attack was similar at 24, 36, and 48 hours without food for the two species (Table 1).

Podisus nigrispinus and B. tabidus killed the T. arnobia caterpillar at a similar time after different food-free intervals. On the other hand, B. tabidus was faster than P. nigrispinus with 24, 36, and 48 hours without food (Table 1).

The number of attempts, over four hours, showed the effect of time without food (pre-release) on the number of attacks by the predator P. nigrispinus, with a higher number of attacks for those submitted to 36 and 48-hour periods without food. The number of attacks by B. tabidus, without food for 24, 36, or 48 hours, was similar. Attacks by this predator, after 24 hours without food, were fewer than for P. nigrispinus. After 36 hours, the number of attacks was similar between species, but at 48 hours, P. nigrispinus carried out fewer attacks than B. tabidus (Table 1).

Table 1

Time taken for the first attack, death and the number of attempts to attack the sixth instar caterpillar of *Thyrinteina arnobia* (Lepidoptera: Geometridae) by the predators *Podisus nigrispinus* and *Brontocoris tabidus* (Hemiptera: Pentatomidae) after 24, 36 or 48 hours without food
	Predators	24 hours	36 hours	48 hours
1st attack (min)	P. nigrispinus	31.8 ± 4.7 A a	10.2 ± 2.4 B a	7.6 ± 0.9 B a
1st attack (min)	B. tabidus	22.4 ± 4.9 A a	18.8 ± 5.9 A a	7.4 ± 1.8 B a
Caterpillar death (min)	P. nigrispinus	75.8 ± 12.9 A a	63.9 ± 9.8 A a	75.3 ± 10.0 A a
Caterpillar death (min)	B. tabidus	13.4 ± 1.1 A b	11.9 ± 1.2 A b	15.1 ± 1.2 A b
Attack attempts	P. nigrispinus	4.3 ± 0.4 A a	2.7 ± 0.9 B a	2.2 ± 0.3 B b
Attack attempts	B. tabidus	1.9 ± 0.3 A b	1.6 ± 0.1 A a	2.8 ± 0.5 A a

Means followed by the same capital case letters in the line or lower-case in the column do not differ by the Tukey test at 5% of probability. (Mean ± Standard Error).

Brontocoris tabidus showed greater ability to control T. arnobia caterpillars than P. nigrispinus, killing 72% of them in the first attack, while P. nigrispinus killed only 30%.

Digestive enzymes from the salivary content of P. nigrispinus and B. tabidus showed differences in amylase activity, with the predator B. tabidus presenting a higher amount of this enzyme. Lipase and protease activity were similar between these predators (Table 2).

Table 2

Enzymatic activity of salivary content of predators *Podisus nigrispinus* and *Brontocoris tabidus* (Hemiptera: Pentatomidae)
Enzyme (unit)	Podisus nigrispinus	Brontocoris tabidus
Amylase (U/dL)	20.1 ± 8.2 B	187.9 ± 9.8 A
Lipase (UI)	0.9 ± 0.2 A	1.6 ± 0.1 A
Protease (nM)	0.0025 ± 0.0000 A	0.0026 ± 0.0001 A
Means followed by the same letter in the line do not differ by the F test with p < 0.05. (Mean ± Standard Deviation).

The morphological analysis of the mouthparts responsible for prey fixation showed that B. tabidus has mandibular stylets and maxillary setae larger than those of P. nigrispinus (Fig. 1; Table 3).

Table 3

Size of mouthparts of *Podisus nigrispinus* and *Brontocoris tabidus* (Hemiptera: Pentatomidae)
	Podisus nigrispinus	Brontocoris tabidus
Mandibular stylets (mm)	4.35 ± 0.02 B	5.33 ± 0.03 A
Maxillary setae (µm)	49.6 ± 0.3 B	60.0 ± 0.5 A
Means followed by the same letter in the line do not differ by the F test with p < 0.05. (Mean ± Standard Deviation).

The period that P. nigrispinus and B. tabidus remained without food affected the time for the first attack on T. arnobia caterpillars, which shows that hunger stimulates the searching ability (Frazer and Gill 1981; Bell 1990) and the speed of for food (Torres et al. 2002) of predatory insects.

The time taken for T. arnobia caterpillar death may be related to the higher amylase activity of the predator B. tabidus. The occurrence of this enzyme in the salivary glands has also been reported for other bed bugs (Cohen 1996) and, in predatory arthropods such as centipedes (Lewis 1982), spiders (Mommsen 1978; Nentwin and Wissel 1986) and some aquatic species such as Lethocerus uhleri (Montandon) and Belostoma struggleium (Stal) (Heteroptera: Belostomatidae), which also showed amylase in their salivary content (Swart et al. 2006). The greater amylase activity in the salivary glands of B. tabidus and the fact that this insect often uses plant material as a food supplement and water source, which facilitates the extraoral digestion process (Gillespie and McGregor 2000; Sinia et al. 2004), may explain the greater ability for predation and control of the defoliating caterpillar T. arnobia by this predator.

The less successful attack by P. nigrispinus is due to this predator having smaller attachment structures (stylets and arrows) than those of B. tabidus, given that the caterpillar's defense can also make the attack difficult (Zanuncio et al. 2008b). On the other hand, the larger attachment structures of B. tabidus provide a firmer grip on the prey and prevent the T. arnobia caterpillar from evading this predator's attack. The lower number of attacks occurrence by P. nigrispinus when maintained for 48 hours without food may be due to this predator having a greater ability to remain longer periods without food (Pires et al. 2011), when compared with B. tabidus maintained for long periods without food too (Pires et al. 2011). Larger predators without food partially lose their ability to control caterpillars, which was observed by the higher number of attacks when compared with P. nigrispinus.

The larger B. tabidus mouthparts, together with the greater amylase activity, makes this predator more successful than P. nigrispinus in attacking and controlling T. arnobia caterpillars.

A total removal of food is not recommended, as the ingestion of plant material, in addition to minimizing the effects of the absence of prey, is also a water source, which helps in the process of extra-oral digestion. Therefore, it is recommended that, as part of the pre-release strategy for P. nigrispinus and B. tabidus, plant material and water are provided to improve the efficiency of attack by these predators.

Acknowledgments

We are greatfull to “Conselho Nacional de Desenvolvimento Científico e Tecnológico” (CNPq).

Funding

This work was supported just by Conselho Nacional de Desenvolvimento Científico e Tecnológico” (CNPq).

The authors declare that no funds, grants, or other support were received during the preparation of this manuscript.

Competing Interests

The authors have no relevant financial or non-financial interests to disclose.

Author Contributions

Evaldo Martins Pires and Roberta Martins Nogueira designed, directed the study, and developed the experiments, analyzed the data and to the writing of the manuscript. José Eduardo Serrão contributed to the implementation of the research and to the analysis of the results, mainly about internal morphology. José Cola Zanuncio contributed to the development of this study and to data analyzis.

Data Availability

The datasets generated during and/or analysed during the current study are available from the corresponding author on reasonable request.

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Attack efficacy by Podisus nigrispinus and Brontocoris tabidus on Thyrinteina arnobia with different pre-release strategies

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