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Feeding responses of Euthyrhinchus floridanus (Hemiptera: Pentatomidae) to brown marmorated stinkbug (Hemiptera: Pentatomidae) adults and nymphs.

Euthyrhynchus floridanus (L.) (Hemiptera: Pentatomidae), is a native predator that is common throughout the yr in many agro-ecosystems. It preys on a diversity of crop pests, including immature beetles, lepidopterous pests, and true bugs including plant-damaging pentatomoids (Mead 1976; Logan et al. 1987; Medal et al. 2018). The distribution range includes the central and southeastern USA, Mexico, Central, and South America into southern Brazil (Abies 1975; Mead & Richman 2013). Adults and nymphs tend to be aggregated and have a low level of cannibalism (Medal personal observation). Both nymphs and adults capture prey of different sizes, and feed individually or in aggregations. Since the discovery of the brown marmorated stink bug in Pennsylvania in 1996 (Hoebeke & Carter 2003), attempts have been made to use parasitoids and predators (Dieckhoff & Hoelmer 2014; Lara et al. 2016) as a sustainable management option of this new invasive polyphagous Asian immigrant (Hamilton et al. 2008; Haye et al. 2015; Leskey & Nielsen 2018) that has been reported in 44 states, including a limited reproductive localized infestation in Lake County, Florida (Northeastern IPM Center 2017; Penca & Hodges 2018). In this laboratory study, we determined the feeding response of E. floridanus to brown marmorated stinkbug Halyomorpha halys (Stal) (Hemiptera: Pentatomidae) nymphs and adults in controlled environmental conditions.

Euthyrhynchus floridanus used in this study was obtained from a laboratory colony established from nymphs and adults collected in a kudzu (Pueraria montana Lour (err.) variety lobata (Willd.); Fabaceae) patch in Gainesville, Alachua County, Florida, USA (29.639686[degrees]N, 82.399092[degrees]W) during the summer-fall of 2014. The second to fifth in-stars and adult brown marmorated stinkbug used in the experiments were obtained from a colony obtained from the USDA-ARS laboratory colony located in Newark, New Jersey, USA, and held in the laboratory in clear plastic containers (23 cm width x 32 cm length x 10 cm height) with moistened paper, and bean pods and carrots. Growing conditions were set at 25 [+ or -] 3 [degrees]C, 16:8 h (L:D) photoperiod, and 50 to 60% RH.

Euthyrhynchus floridanus nymphs, and male and female adults were starved for 24 h before the experiment. Predators were placed individually in Petri dishes (14.6 cm x 2.5 cm) with a bean pod, Phaseolus vulgaris L. (Fabaceae), and moistened paper as food and moisture sources. Crumpled Kimwipes[R] (Kimberly-Clark, Roswell, Georgia, USA) were inserted in each dish to provide refugia for predators. One brown marmorated stinkbug nymphal instar or an adult was provided to 1 E. floridanus third nymphal instar, or a male or female adult predator. Control consisted of the same experimental set-up with only prey. The predator-prey studies incorporated a completely randomized design with 20 replications for predator prey interaction. After 24 h, the number of dead prey was recorded. Percent prey mortality data for each predator stage was analyzed using Fisher's Exact Test for Count Data (Fisher 1970). Mean prey mortality resulting from predation on developmental stage was analyzed as a 2-way factorial and compared using Tukey's multiple comparison test of means (Montgomery 2013). Means were considered statistically different at P < 0.05). Brown marmorated stinkbug mortality data were not adjusted because of low (< 5%) mortality in controls. These studies were conducted during 2015 and 2016. Predation rate of E. floridanus to brown marmorated stinkbug has not been reported previously in the literature.

These studies indicated that the feeding responses of E. floridanus male, female, and third nymphal instar to brown marmorated stinkbug generally were affected by the prey developmental stage (Tables 1 & 2). The percent mortality of brown marmorated stinkbug adults or nymphs due to E. floridanus male, female, or intermediate nymph differed significantly ([chi square] = 25; df = 7; P = 0.036584738). Females had a preference to feed on brown marmorated stinkbug second to fourth nymphal instar, whereas males did not show any difference in the feeding response to the brown marmorated stinkbug nymphal instar (Table 1). The E. floridanus female was more effective than males, showing higher prey mortality of brown marmorated stinkbug male or female (df = 3; P = 0.021). The feeding responses (30-40%) by E. floridanus third nymphal instar to brown marmorated stinkbug second to fourth nymphal instars were significantly different (df = 3; P< 0.05) than those obtained on the fifth nymphal instar (Table 2). Mortality of brown marmorated stinkbug nymphs ranged from 30 to 100% for E. floridanus females, and from 50 to 70% for E. floridanus males. Euthyrhynchus floridanus males were not able to feed on brown marmorated stinkbug females, probably due to the larger size of the female prey than the male predator. This was contrary to the female predators, which fed an average of 80% on female prey (Table 1). A possible explanation for the lower feeding response, in addition to the difference in size, may be related to the defense mechanism of larger prey sizes when attacked by a predator. Results indicated that E. floridanus, as an effective predator of the brown marmorated stinkbug, may complement other control strategies to reduce its population in infested regions.

The authors thank J. Howard Frank (University of Florida) and Phillip Lake (Florida Department of Agriculture and Consumer Services) for reviewing the manuscript. We also thank the staff of FDACS-Division of Plant Industry's Biological Control Rearing Facility for providing the Lepidoptera caterpillars used to feed the predator colony. This research was partially funded by the USDA-APHIS-PPQ, FDACS-DPI, and Universidad Autonoma Chapingo, Mexico. Summary

The Florida predatory stink bug, Euthyrhynchus floridanus L. (Hemiptera: Pentatomidae), is a generalist predator native to North America that feeds on a broad range of lepidopterous and heteropterous key pests in a great diversity of crops and non-crop situations. Feeding tests conducted in the laboratory to determine the most susceptible stage of the brown marmorated stink bug, Halyomorpha halys (Stal) (Hemiptera: Pentatomidae), to third nymphal instar, and male and female E. floridanus, indicated that this predator has great potential for biological control of H. halys nymphs and adult stages.

Key Words: Heteroptera; biological control; predator; agriculture pest

Sumario

La chinche hedionda depredadora de Florida, Euthyrhynchus floridanus L. (Hemiptera: Pentatomidae), es una generalista nativa de Norte America que se alimenta de un amplio rango de plagas importantes lepidopteros y heteropteros en una gran diversidad de cultivos y areas naturales. Pruebas de alimentacion en laboratorio para determinar el estado mas susceptible de la chinche hedionda marron marmoleada, Halyomorpha halys (Stal) (Hemiptera: Pentatomidae) al tercer estadio ninfal, y macho y hembra E. floridanus indicaron que este depredador tiene un gran potencial para control biologico de ninfas y adultos de H. halys.

Palabras Claves: Heteroptera; control biologico; depredador; plaga agricola

References Cited

Abies JR. 1975. Notes on the biology of the predaceous pentatomid Euthyrhynchus floridanus (L.). Journal of the Georgia Entomological Society 10: 353-356.

Dieckhoff C, Hoelmer KA. 2014. Classic biological control: status of host-range tests with Asian egg parasitoids. Northeastern IPM Center. https://www.northeastipm.org/neipm/assets/File/BMSB%20Resources/BMSB-IWG-Dec-2014/15-Classical-Biological-Control-Status-of-Host-Range-Tests-with-Asian-Egg-Parasitoids-Dieckhoff.pdf (last accessed 18 May 2019).

Fisher RA. 1970. Statistical Methods for Research Workers. Oliver & Boyd, London, United Kingdom.

Hamilton GC, Shearer PW, Nielsen AL. 2008. Brown marmorated stink bug--a non-native insect in New Jersey. Fact Sheet FS002. Rutgers NJAES Cooperative Extension. Rutgers University, New Brunswick, New Jersey, USA.

Haye T, Gariepy T, Hoelmer K, Rossi JP, Streito JC, Tassus X, Desneuz N. 2015. Range expansion of the invasive brown marmorated stinkbug, Halyomorpha halys: an increasing threat to field, fruit, and vegetable crops worldwide. Journal of Pest Science 88: 665-673.

Hoebeke ER, Carter ME. 2003. Halyomorpha halys Stal (Hemiptera: Pentatomidae): a polyphagous plant pest from Asia newly detected in North America. Proceedings of the Entomological Society of Washington 105: 225-237.

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Leskey TC, Nielsen AL. 2018. Impact of the invasive brown marmorated stink bug in North America and Europe: history, biology, ecology, and management. Annual Review Entomology 63: 433-452.

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Mead FW, Richman DB. 2013. Florida predatory stinkbug, Euthyrhynchus floridanus (Linnaeus) (Insecta: Hemiptera: Pentatomidae). UF/IFAS, FDACS, DPI Publication EENY-157. University of Florida, Gainesville, Florida, USA. https://entomology.ifas.ufl.edu/creatures/beneficial/e_flori-danus.htm (last accessed 18 May 2019).

Medal J, Srivastava M, Sharma S, Wolaver D, Santa Cruz A, Rohrig E, Howe A. 2018. Laboratory feeding responses of Euthyrhynchus floridanus and Podisus maculiventris (Hemiptera: Pentatomidae) to the kudzu bug, Megacopta cribraria (Hemiptera: Plataspidae). Florida Entomologist 101: 382-388.

Montgomery DC. 2013. Design and Analysis of Experiments. John Wiley & Sons, Inc., Hoboken, New Jersey, USA.

Northeastern IPM Center. 2017. www.northeastipm.org. Cornell University, Ithaca, New York, USA.

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Rubi Arellano (1), Julio Medal (2,*), Gregorio Arellano (3), and Juan Perez (1)

(1) Universidad Autonoma Chapingo, Carretera Mexico-Texcoco, Km. 38.5, Texcoco de Mora 56230, Estado de Mexico, Mexico; E-mail: dayanerubi@outlook.com (R. A.); jcforestall991@gmail.com (J. P.)

(2) Florida Department of Agriculture and Consumer Services, Division of Plant Industry, Gainesville, Florida 32608, USA (former address); E-mail: medal@ufl.edu (J. M.)

(3) Colegio de Posgraduados, Carretera Mexico-Texcoco, Km. 36.5, Montecillo, Texcoco 56230, Estado de Mexico, Mexico; E-mail: arellano@colpos.mx (G. A.)

(*) Corresponding author; E-mail: medal@ufl.edu
Table 1. Mortality (% [+ or -] SD) of brown marmorated stinkbug,
Halyomorpha halys caused by Euthyrhynchus floridanus male and female.

Predator gender  Prey growth stage    Prey mortality % ([+ or -] SD)

Female           Nymph second instar   80 [+ or -] 10 b
Female           Nymph third instar    80 [+ or -]8 b
Female           Nymph fourth instar  100 [+ or -] 0 a
Female           Nymph fifth instar    30 [+ or -] 10 d
Male             Nymph second instar   60 [+ or -]8 c
Male             Nymph third instar    60 [+ or -]6 c
Male             Nymph fourth instar   50 [+ or -] 10 c
Male             Nymph fifth instar    70 [+ or -] 10 bc
Male             Female prey          Oe
Female           Female prey           80[+ or -]6 b
Male             Male prey             70[+ or -]4 c
Female           Male prey             90[+ or -]10 ab

Means % followed by the same letter in the column for each treatment
did not differ significantly (P [greater than or equal to] 0.05); 20
replications.

Table 2. Mortality (% [+ or -] SD) of brown marmorated stinkbug,
Halyomorpha halys nymphs caused by Euthyrhynchus floridanus third
instar.

                                             Prey mortality
Treatment                                    % ([+ or -] SD)

Predator nymph vs. prey nymph second instar  40[+ or -]10 ab
Predator nymph vs. prey nymph third instar   30[+ or -]5 b
Predator nymph vs. prey nymph fourth instar  40[+ or -]8 ab
Predator nymph vs. prey nymph fifth instar   20[+ or -]4 c

Means % followed by the same letter in the column for each treatment
did not differ significantly (P [greater than or equal to] 0.05); 20
replications.


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Author:Arellano, Rubi; Medal, Julio; Arellano, Gregorio; Perez, Juan
Publication:Florida Entomologist
Geographic Code:100NA
Date:Sep 1, 2019
Words:1829
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