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First Report of Trissolcus japonicus Parasitizing Halyomorpha halys inNorth American AgricultureAuthors: Joe M. Kaser, Clement Akotsen-Mensah, Elijah J. Talamas, and Anne L. NielsenSource: Florida Entomologist, 101(4) : 680-683Published By: Florida Entomological SocietyURL: https://doi.org/10.1653/024.101.0406

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1Rutgers, The State University of New Jersey, Department of Entomology, Bridgeton, New Jersey 08302, USA; E-mail: joe.kaser@rutgers.edu (J. M. K.), ca555@scarletmail.rutgers.edu (C. A. M.), nielsen@njaes.rutgers.edu (A. L. N.)2Florida State Collection of Arthropods, Division of Plant Industry, Florida Department of Agriculture and Consumer Services, 1911 SW 34th St Gainesville, Florida 32608, USA; E-mail: Elijah.Talamas@freshfromflorida.com (E. J. T.)*Corresponding author; E-mail: nielsen@njaes.rutgers.edu

680 2018 — Florida Entomologist — Volume 101, No. 4

First report of Trissolcus japonicus parasitizing Halyomorpha halys in North American agricultureJoe M. Kaser1, Clement Akotsen-Mensah1, Elijah J. Talamas2, and Anne L. Nielsen1,*

The invasive ro n marmorated stin ug, Halyomorpha halys (Stål) (Hemiptera: Pentatomidae) is a polyphagous agricultural pest that feeds on over 1 0 plant species, including many cultivated fruits, vegeta les, ro crops, ornamentals, and ild host plants ( es ey

ielsen 2018). ative to Asia, the earliest record of H. halys in North America is from 1996 in Allento n, Pennsylvania, in the eastern USA ( oe e e Carter 2003). It has since spread throughout much of

orth America, causing idespread economic harm ( ice et al. 2014; es ey ielsen 2018). In 2014, an Asian egg parasitoid, Trissolcus ja-

ponicus (Ashmead) ( ymenoptera: Scelionidae), as found successful-ly parasiti ing la oratory reared, eld deployed (sentinel) H. halys egg masses in eltsville, aryland, USA (Talamas et al. 201 ; erlihy et al. 2016). Several other eld populations have since een reported in the mid-Atlantic and Paci c orth estern regions of the US (10 states and Washington, DC, oelmer personal communication), hich li ely rep-resent multiple independent introductions of the parasitoid ( ilnes et al. 2016; ara et al. 2016; edstrom et al. 201 ). It is unclear through what pathways T. japonicus entered orth America, ut genetic data indicate that the parasitoid did not escape from uarantine facilities

here it is eing studied as a potential classical iological control agent of H. halys (Bon et al. 2017).

The recent introductions of T. japonicus in orth America may in-crease biological control of H. halys. o ever, to our no ledge, T. japonicus has yet to e documented parasiti ing H. halys within North American cultivated crops. All pu lished recoveries of adventive T. ja-ponicus in orth America have occurred in non-agricultural, largely

oody ha itat despite surveys in crops (Talamas et al. 201 ; Cornelius et al. 2016a, ; erlihy et al. 2016; g urn et al. 2016; edstrom et al. 201 ; orrison et al. 2018) that has led to concern that introduced strains of T. japonicus may have limited iological control potential in

orth America. During the invasion process, genetic o lenec s can a ect life history characteristics, such as ecological host range (i.e., the number of host species that a parasitoid is able to complete develop-ment on in the eld), and may limit the a ility of introduced iological control agents to a ac pests across the same readth of ha itat as in their native range ( u auer 2002).

We conducted surveys in 2 commercial apple and 3 peach or-chards in southern e Jersey, USA (apple: onroeville, Gloucester County 39.68 , .18 W and ich ood, Gloucester Coun-ty 39. 3 , .1 48 W ; peach: ich ood, Gloucester County 39. 3 , .1 48 W , Glass oro, Gloucester County 39. 08 ,

.1331 W , and Salem, Salem County 39. 66 , .4248 W ) that had previous pest issues with H. halys. n each farm, contiguous

loc s ere selected ranging from 2.0 to 9. ha of peach or apple, and assigned to 1 of 2 management regimes: Integrated Pest anage-ment - Crop Perimeter estructuring (IP -CP ) or gro er standard. There ere 3 IP -CP loc s and 1 gro er standard loc replicated on 4 orchards for peach and 2 orchards for apple. loc s ithin the IP -CP (Crop Perimeter estructuring; descri ed in detail in laau et al. 201 ) management protocol applied insecticides only to the or-chard order plus the rst full ro for H. halys management. In peach, this began at 100 DD14 and continued ee ly until harvest. In apple,

order- ased management as initiated hen a cumulative threshold of 10 adult H. halys ere found in any aggregation pheromone- aited H. halys trap (Short et al. 2016) and then continued until harvest. All IP -CP loc s per farm had a companion gro er standard loc of a minimum of 2.0 ha, managed according to recommendations from

utgers University Fruit anagement Guidelines ( JAES 201 ). In each loc , sentinel H. halys egg masses < 24 h old were sourced from the e Jersey Department of Agriculture, Trenton, e Jersey, USA, and

deployed on orchard trees at 3 time points in apples (11 Jul, 2 Jul, and 8 Aug 201 ) and 4 time points in peach (20 Jun, 11 Jul, 2 Jul, and 8 Aug 201 ). Sentinel egg masses ere glued using Elmer s ulti-purpose Glue-A (Elmer s Products, Inc., igh Point, orth Carolina, USA) onto paper cardstoc and deployed y a aching an egg mass card to the underside of a leaf using a paper clip. Egg masses were deployed on 2

order trees and 2 interior trees (a out 6 trees 18.3 m) in a transect, and placed et een 2 and 3 m from the ground. Trees on the order were adjacent to a pheromone baited H. halys trap. There ere 192 sentinel H. halys egg masses ( ,4 8 individual eggs) deployed in peach, and 48 in apple (1,321 individual eggs) (Ta le 1). Egg masses ere le in orchards for about 48 h, then returned to the laboratory where each egg mass as placed separately in closed plastic containers, placed in an incu ator (2 C, 60 0 , 16:8h ( :D) photoperiod), monitored until emergence of H. halys or parasitoids, and the species identi ed

ased on adult morphological characteristics. If parasitoids emerged from an egg mass, or a guarding female as found in association ith the retrieved egg mass, a er aiting 1 mo, the remaining unhatched eggs were dissected and inspected for dead parasitoids (larvae or pha-rate adults) or H. halys nymphs.

The e ect of management strategy on the num er of parasiti ed egg masses as analy ed using a 2-sided Fisher s e act test (FET) (So al and ohlf 199 ), pooling order and interior trees. The analysis as conducted on a 2 2 contingency ta le of management regime (IP -CP vs. gro er standard) and parasitism status (parasiti ed vs. un-parasiti ed egg mass). The GPS locations of sentinel egg masses ere

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Scienti c otes 681

recorded in the eld, and the distances of successfully parasiti ed egg masses to eld edge and the nearest oody order ere estimated in Google Earth Pro.

o successful parasitism as found on eggs placed in apple or-chards. In peach, 4 (2.2 ) of 18 retrieved egg masses ere success-fully parasiti ed ( egg masses ere not recovered from the eld). All successful parasitism in peach occurred under IP -CP management; ho ever, the e ect of management regime as not statistically sig-ni cant (P 0. , FET). In total, 4 T. japonicus adults emerged from 3 egg masses, ith an average proportion parasitism of each successfully parasiti ed egg mass of 0.91 ( 0.083 SE ), and no emerging H. halys.

ne of the egg masses parasiti ed y T. japonicus was deployed on 20 Jun, and 2 ere deployed on 8 Aug 201 . Egg masses parasiti ed y T.

japonicus had a distance to the nearest wooded border ranging from 19. m to 68.3 m (mean 40.0 m, SE 1 .3) (Fig. 1). T o adults of the native parasitoid Trissolcus edessae Fouts (Hymenoptera: Platygas-tridae) emerged from a single egg mass, along with 1 H. halys nymph and 1 eggs ithout emergence. Dissection of the 1 unhatched eggs uncovered 8 dead parasitoid larvae, 1 dead pharate parasitoid adult, and 6 with no clear insect development. The egg mass was deployed on 11 Jul at an interior location, 2 .8 m (6 trees) from the nearest or-chard edge that interfaced a soy ean eld, and 11 m from the near-est ooded order. ne native adult female parasitoid, Telenomus astrictus Johnson (Scelionidae), was captured guarding an egg mass, deployed on 8 Aug and collected on 10 Aug, at a order location in an IP -CP peach orchard, 19.9 m from the nearest ooded order.

Table 1. Sentinel egg masses deployed and num er of e otic (Trissolcus japonicus) and native (Trissolcus edessae) parasitoids emerging as adults.

Crop Treatment No. of egg masses No. of eggs Trissolcus japonicus adults ative adults

Peach Gro er Standard 48 1,383 0 0Peach IP -CP 144 4,0 4(3) 2(1)Apple Gro er Standard 24 662 0 0Apple IP -CP 24 6 9 0 0

um ers of sentinel egg masses deployed and total num er of parasitoid adults successfully emerging are listed (num er of egg masses parasiti ed). All egg masses parasiti ed y Trissolcus japonicus ere deployed on either 20 Jun or 8 Aug 201 .

Fig. 1. White and lac circles indicate the locations of 2 sentinel egg masses that ere parasiti ed y Trissolcus japonicus within a heterogeneous landscape at 1 of the eld sites in e Jersey. lac lines indicate the nearest tree line, and the inset map of e Jersey indicates ith a star here this farm as located.

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682 2018 — Florida Entomologist — Volume 101, No. 4

Twenty-two H. halys nymphs successfully emerged from the guarded egg mass, and 6 eggs did not hatch. Dissection of the 6 unhatched eggs uncovered 4 dead parasitoid larvae, 1 dead partially developed H. halys nymph, and 1 with no clear insect development. Whereas H. halys nymphs and adults are highly mo ile ( ee et al. 2014; ee es-ey 201 ), it is not clear ho far T. japonicus moves during its lifetime.

In fre uently distur ed agricultural ha itat, T. japonicus may be able only to disperse from source ha itats li e a ooded eld order.

To our no ledge, these are the rst o servations of successful parasitism of H. halys by T. japonicus on a cultivated crop in the US that occurred in 2 di erent orchards. In China, the percentage of each H. halys egg mass a ac ed y T. japonicus ranges et een 20 and 80 of eggs, ith a season-long average parasitism of each egg mass of 0 among eld collected egg masses on fruit and forest trees ( ang et al. 2009; ara et al. 2016). In northern China, T. japonicus was the dominant egg parasitoid a ac ing H. halys sentinel egg masses de-ployed in cultivated peach, mul erry (Morus alba .; oraceae), and jujube (Ziziphus jujuba ill.; hamnaceae) trees ( hang et al. 201 ).

o ever, novel environments for parasitoid-host interactions, as ith T. japonicus and H. halys in the US, open up an array of uestions. For a given host species, its ris of parasitism may vary in di erent ecological conte ts (Cronin eeve 200 ).

Despite the high success of T. japonicus in its native range ithin agricultural crops ( hang et al. 201 ), the paucity of parasitism in US commercial agriculture had raised concerns. ur results suggest 2 im-portant ndings. First, T. japonicus can successfully forage and parasit-i e in US crops. Peach is a preferred host plant of H. halys (Ace es-Doria et al. 2016) and produces n-tridecane volatiles to hich female T. japonicus also respond ( hong et al. 201 ), perhaps enhancing foraging

ehavior. Second, despite di erences in management styles et een Asia and the US, our results suggest that T. japonicus may be com-pati le ith the IP -CP tactic in peaches, as all parasitism occurred

ithin these reduced input loc s. The IP -CP tactic targets a out 2 of the orchard ith insecticide and integrates mating disruption for lepidopteran pests, signi cantly reducing insecticide applications throughout the gro ing season ( laau et al. 201 ). Further research on the impact of insecticides on foraging ehavior and survivorship of T. japonicus is needed to balance managing injury caused by H. halys in tree fruit with enhanced biological control.

We than Ann uc er, eghin ollins, and arina Pere for their assistance in the la oratory and eld. This project as supported in part y USDA IFA 201 - 0006-24282, USDA IFA 2016- 1181-2 409, and the e Jersey Agricultural E periment Station ulti-State Proj-ect J0822 . We than the Florida Department of Agriculture and Consumer Services, Division of Plant Industry for their support on this contri ution.

Summary

Halyomorpha halys (Stål) (Hemiptera: Pentatomidae), the brown marmorated stin ug, an invasive agricultural pest in America and Europe, is reaching a glo al distri ution. In the US, the rst detection of H. halys as in the mid 1990s, and it has ecome a serious pest in multiple crop systems. In 2014, an e otic egg parasitoid, Trissolcus japonicus (Ashmead) ( ymenoptera: Scelionidae), as documented parasiti ing sentinel H. halys egg masses in a wooded habitat in Belts-ville, aryland, USA. The parasitoid has since een reported in several other locations in the eastern and estern US, and its population ap-pears to e e panding in geographic range. o ever, there have een no reports of T. japonicus parasiti ing H. halys egg masses within cul-tivated crops in the US. Whereas a ac of H. halys in non-agricultural

habitat may provide important biological control services in the land-scape, if T. japonicus is not able to successfully forage for H. halys eggs within crops, its impact as a biological control agent may be limited.

ere e report on successful parasitism of egg masses deployed in 2 peach orchards in e Jersey, USA. Egg masses ere deployed as part of an e periment investigating the e cacy of an integrated pest man-agement (IP ) strategy utili ing order insecticide sprays in apple and peach. While overall egg parasitism as lo , the majority of success-fully developing parasitoids (9 .4 of total adult parasitoids emerging, and from of successfully parasiti ed sentinel egg masses) ere T. japonicus.

ey Words: Invasive species; iological control; parasitism; rst oc-currence; Scelionidae

Sumario

Halyomorpha halys (Stål) (Hemiptera: Pentatomidae), el chinche marmorino caf , una plaga agr cola invasora en Am rica y Europa, est alcan ando una distri uci n mundial. En los Estados Unidos, la primera detecci n de H. halys fue a mediados de la d cada del 1990, y se ha convertido en una plaga seria en sistemas de cultivos m ltiples. En el 2014, se document un parasitoide e tico de los huevos, Trissolcus ja-ponicus (Ashmead) ( ymenoptera: Scelionidae), parasitando las masas centinelas de H. halys en un h itat de os ue en eltsville, aryland, EE. UU. El parasitoide ha sido reportado en varios otros lugares en el es-te y el oeste de los EE. UU. y su po laci n parece estar e pandiendo su rango geogr co. Sin em argo, no ha ha ido informes de T. japonicus parasitando masas de huevos de H. halys dentro de cultivos en los EE. UU. ientras ue el ata ue de H. halys en h itats no agr colas puede proporcionar un servicio importante de control iol gico en el campo, si T. japonicus no es capa de alimentarse con ito de los huevos de H. halys dentro de los cultivos, su impacto como agente de control iol -gico puede ser limitado. A u informamos so re el parasitismo e itoso de masas de huevos puestos en dos huertos de melocotones en Nueva Jersey, EE. UU. as masas de huevos se implementaron como parte de un e perimento ue investiga la e cacia de una estrategia integra-da de manejo de plagas utili ando aerosoles insecticidas de frontera en man ana y melocot n. ientras ue el total del parasitismo de los huevos fue bajo, la mayoría de los parasitoides desarrollandose con e ito (el 9 .4 del total de parasitoides adultos ue emergieron y del

de las masas de huevos centinela parasitados con ito) fueron T. japonicus.

Pala ras Clave: especies invasoras; control iol gico; parasitismo; primera aparici n; Scelionidae

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