Natural Enemies of the Brown Marmorated Stink Bug:

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Natural Enemies of the Brown Marmorated Stink Bug: What are the Prospects for Biological Control? Kim Hoelmer Kathy Tatman USDA ARS Beneficial Insects Introduction Research Unit Newark, DE Photo: J. Wildonger USDA ARS

Pathogens No records from BMSB Metarhizium used with some impact on Sunn pests Ophiocordiceps spp. reported * all stages of BMSB potentially vulnerable

Predators not yet well studied Photo: K. Bernhard Photo: K. Bernhard of eggs: ants, earwings, lacewings Photo: R. Fertig of nymphs & adults: assassin bugs, predatory stink bugs, spiders, birds (starlings, chickens, geese)

Parasitoids of pentatomids Many species of stink bug egg parasitoids: Scelionids (1 o ), Chalcidoids (2 o ) No parasitoids of nymphs are known M. Merchant/TAMU Tachinid flies (1 o ) and braconids (rarely) attack adults

Parasitoids of adult stink bugs: Tachinidae (Diptera) Generally considered to be not very host specific - however - M. Merchant/TAMU Recent taxonomic studies show considerable cryptic speciation in some tachinids Many hosts records likely based on erroneous ID of tachinids May be more specific than previously thought

Egg parasitoids: Many are generalists - various chalcidoids (Eupelmidae, Encyrtidae) Anastatus sp. Anastatus spp. attack eggs of many insect orders; habitat specialists rather than host specialists Anastatus sp.

Specialist egg parasitoids: Telenomus, Trissolcus, Gryon, Psix (Scelionidae) Trissolcus spp. are typically specific to pentatomids Photo: UC IPM/JK Clark

Mid Atlantic States Parasitism Survey to evaluate the need for a classical biocontrol project for Initiated in 2005 and continued through 2010 (summer months) 1 o conducted in Newark, DE & Allentown, PA Sentinel and wild-collected egg masses (N = 300-600 per year) placed in the field for 2-3 days Parasitoids reared from egg masses and identified Tachinid parasitism (egg deposition) measured in Newark samples

10 Percent Parasitism 8 6 4 2 0 Egg Mass Parasitism - Newark 2005 2006 2007 2008 2009 Individual Eggs Egg Masses Individual eggs in sentinel masses were parasitized at a relatively low overall rate of 3-4% or less. The proportion of egg masses discovered (with any eggs attacked) was higher, but relatively few individual eggs per mass were attacked (low parasitism efficiency). The rate of discovery of egg masses has not been increasing with time (2010 data not shown here).

Species composition of indigenous egg parastioids Newark 2008 2007 Trissolcus spp. male Anastatus PA & NJ 2008 2007 A.reduvii A. pearsalli Parasitoids reared from sentinel egg masses & field-collected BMSB egg masses in PA, NJ & DE include: 3 species of Anastatus: reduvii, near pearsalli and mirabilis. 3 native species of Trissolcus (brochymenae, edessa, euschisti) occur in lower numbers (1% or less). Ooencyrtus sp. & Telenomus podisi (very rare).

Parasitoids of adult BMSB by Tachindae (Diptera) incidence of eggs on adult stink bugs ca. 1.7% no tachinid emergence from stink bugs with eggs indigenous North American tachinids may not be physiologically adapted to develop in H. halys

10 Percent of BMSB with Tachinid Eggs 9 8 7 6 5 4 3 2 1 0 2005 2006 2007 2008 2009 2010

Is parasitism greater in some habitats than others?

Parasitoids of BMSB previously reported from Asia Scelionidae * Trissolcus itoi, T. mitsukurii, T. plautiae (Japan) * Trissolcus halyomorphae (China) * Trissolcus sp. & Gryon japonicum (Korea) Chalcidoidea * occasional generalist chalcidoids (found in low numbers) Tachinidae * Bogosia sp. reported to attack adult BMSB (Japan)

Locations explored for natural enemies of BMSB in Asia (2005 to date)

Tachinid attacking BMSB in Korea: Pentatomophaga latifascia tachinid egg on dorsum Biology is not well known; most specimens collected fail to develop to emergence adult fly adult emerging from cocoon Larva emerging from BMSB body

Parasitoid cultures at ARS BIIR in Newark maintained for host range and efficacy evaluations: - 12+ populations representing at least 4 species of Trissolcus Japan: T. mitsukurii (Tskuba 2007) T. plautiae (Tskuba 2007) T. flavipes (Tskuba 2007) China: T. halyomorphae (Beijing 2007, Beijing 2008, Nanjing 2009) S. Korea: T. plautiae (Seoul 2009, 2010)

Species Characterization Morphology Molecular characterization Cross-mating studies

M. Saito J & Y Dabry J. Wessels Plautia crossota Nezara antennata Dolycoris baccarum Piezodorus hybneri The Japanese Trissolcus spp. from BMSB are known to attack other Asian pentatomid pests, including the species shown above, indicating they are not absolutely host specific. The full extent of their host range in Asia is unknown.

HOST RANGE TESTING Attack & Development No Choice Choice

HOST RANGE TESTING Physiological Selectivity Complete development Successful emergence Sex ratio of progeny Fitness of progeny (size, fecundity) Behavioral Selectivity Egg recognition Length of time probing Oviposition time Patch residence time Ecological Selectivity Residence time Searching behavior

Euschistus servus W. Tedders PEST SPECIES Piezodorus guildinii Stiretrus anchorago UF/IFAS Acrosternum hilare BENEFICIAL SPECIES Brochymena spp. Flickr/cotinus W. Sterling Podisus maculiventris M. Merchant/TAMU

Phylogentics of Pentatomidae Aphylinae Asopinae Cyrtocorinae Discocephalinae Edessinae Pentatominae Phyllocephalinae Podopinae Serbaninae Stirotarsinae Aeliini Aeptini Aeschrocorini Agaeini Agonoscelidini Amyntorini Antestiniini Aulacetrini Axiagastini Bathycoeliini Cappaeini Carpocorini Catacanthini Caystrini Chlorocorini Coquereliini Degonetini Diemeniini Diplostirini Diploxyini Eurysaspidini Eysarcorini Halyini Hoplistoderini Lestonocornini Mecideini Memmiini Menidini Myrocheini Mealeriini Nezarini Opsitomini Pentatomini Phricodini Piezodorini Procleticini Rhynchocorini Rolstoniellini Sciocornini Sephalini Strachiini Triplatyxini Edessa Euschistus Menecles Oebalus Proxys Mormidea Brochymena Nezara Chlorochroa Nezara Chlorochroa Piezodorus Bagrada Murgantia Halyomorpha Stiretrus Perillus Podisus Euthyrhynchus Nezara Chlorochroa

Photo Credits and Acknowledgments: Jeff Aldrich, USDA ARS Jeff Wildonger & Adam Mitchell, USDA-ARS Anne Nielsen & George Hamilton, Rutgers University Karen Bernhard, PA Agric. Extension Hongyin Chen & Sino-American Lab staff Seunghwan Lee & his students, SNU, Korea Masatoshi Toyama, NARO, Japan