Field Surveys of Egg Mortality and Indigenous Egg Parasitoids of the Brown Marmorated Stink Bug, Halyomorpha Halys, in Ornamenta
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J Pest Sci DOI 10.1007/s10340-017-0890-8 ORIGINAL PAPER Field surveys of egg mortality and indigenous egg parasitoids of the brown marmorated stink bug, Halyomorpha halys, in ornamental nurseries in the mid-Atlantic region of the USA 1 1 1 1 Ashley L. Jones • David E. Jennings • Cerruti R. R. Hooks • Paula M. Shrewsbury Received: 31 January 2017 / Revised: 23 May 2017 / Accepted: 30 May 2017 Ó The Author(s) 2017. This article is an open access publication Abstract The brown marmorated stink bug, Halyomorpha over time and female biased sex ratio of parasitoids sug- halys (Sta˚l), is an invasive species native to regions of gests that native parasitoids may be responding to the novel China, Japan, Korea, and Taiwan. In its native and intro- host, H. halys. Consequently, the use of these native duced range, H. halys is considered a pest of tree fruits, eupelmid egg parasitoids in augmentative or conservation vegetables, legumes, and ornamental trees. The highly biological control may be a viable H. halys management polyphagous nature of this insect as well as its vast dis- strategy in ornamental nurseries. persal capabilities, require an integrated approach to management. Here we focus on the potential impact of Keywords Anastatus reduvii Á Native parasitoids Á indigenous natural enemies on H. halys in woody orna- Biological control Á Parasitism Á Predation mental nurseries in Maryland, USA. We sampled naturally field laid H. halys egg masses for mortality and parasitism rates in 2012 and 2013. Overall, egg mortality averaged Key message 54% for both years, and increased within season and between years. The largest source of mortality was from • Halyomorpha halys is abundant in ornamental plant egg parasitoids with mean parasitism rates of 30.73 and nurseries. Over 2 years, we found H. halys egg mor- 39.63% in 2012 and 2013, respectively. Mortality from tality averaging 54.1%, of which hymenopteran para- predation was much lower and averaged 4.61% by chewing sitoids (7 species total) were the primary mortality and 2.53% by sucking predators. We found seven species source (35.8%). Predation provided the lowest source of Hymenopteran egg parasitoids attacking H. halys eggs, of egg mortality (7.1%). with Anastatus reduvii being the dominant species com- • Parasitism increased within seasons and between years. prising 61.17 and 79.12% of all parasitoids in 2012 and Sex ratio of all parasitoids increased in female bias 2013, respectively. The observed increase in parasitism from 2012 to 2013. • Anastatus spp. accounted for 98.3% of parasitism (determined from enclosed parasitoids) suggesting that Communicated by T. Haye. these native eupelmids contribute to biological control Special Issue: The brown marmorated stink bug Halyomorpha halys of H. halys in nurseries. an emerging pest of global concern. Electronic supplementary material The online version of this article (doi:10.1007/s10340-017-0890-8) contains supplementary Introduction material, which is available to authorized users. & Paula M. Shrewsbury Invasive species have been well documented for their [email protected] detrimental impacts in natural and managed ecosystems and for economic consequences associated with their 1 Department of Entomology, University of Maryland, 4112 introductions (Pimentel et al. 2005; Aukema et al. 2011). Plant Sciences Building, College Park, MD 20742, USA 123 J Pest Sci The successful invasion of exotic species into new regions native natural enemies on H. halys survival in various is often attributed, partly, to their escape from natural habitats (Jones et al. 2014; Cornelius et al. 2016; Herlihy enemies in their native range where they have a shared et al. 2016; Morrison et al. 2016; Ogburn et al. 2016) evolutionary history (Keane and Crawley 2002). Conse- within the USA. Overall, impacts on H. halys egg mortality quently, re-establishing population control in the invaded tend to vary among habitat types, between predators and range can be an important tool for managing invasive parasitoids, and by parasitoid species (Jones et al. 2014; species and providing significant economic benefits (Nar- Cornelius et al. 2016; Herlihy et al. 2016; Ogburn et al. anjo et al. 2014). 2016). Some of this variation may in part be explained by The brown marmorated stink bug, Halyomorpha halys the diverse types of H. halys egg mass used in the studies. (Sta˚l), (Hemiptera: Pentatomidae), is an invasive species For example, when live sentinel (laboratory reared) was first detected in the USA in 1996 in Allentown, PA compared to naturally laid egg masses of H. halys in the (Hoebeke and Carter 2003; Hamilton 2009). Halyomorpha field, it was found that parasitism rates, parasitoid com- halys is a highly polyphagous, utilizing over 100 host plant munity composition, and parasitoid species richness were species or cultivars across its native and introduced ranges significantly less for sentinel compared with naturally laid (Bergmann et al. 2013; Rice et al. 2014; Haye et al. 2015; egg masses (Jones et al. 2014). Bergmann et al. 2016) and economically damaging pest Ornamental plants play an essential role in the biology (Leskey et al. 2012; Rice et al. 2014; Haye et al. 2015). and ecology of H. halys. As such, it is important to Host plants include fruit, row and vegetable crops, and understand the population dynamics of native natural ornamental plants in natural and managed environments enemies in ornamental plant nurseries and their potential (Leskey et al. 2012; Rice et al. 2014; Bergmann et al. for use in biological control programs. However, to our 2016). Halyomorpha halys use over 88 woody ornamental knowledge, only one previous study has been conducted to plants as feeding and/or oviposition hosts throughout the examine natural enemy activity in woody ornamental season (Bernon 2004; Bergmann et al. 2016). production nurseries (Jones et al. 2014). Nurseries often In its native range of Japan, China, and Korea (Hoebeke consist of diverse tree species offering the ability to and Carter 2003), H. halys has several natural enemies, examine patterns of natural enemy activity on different particularly scelionid egg parasitoids such as Trissolcus host plants within a common environment. The present spp. (Hymenoptera: Scelionidae). Studies performed within study was conducted to: (1) evaluate mortality factors (e.g., its native range show that egg parasitoids may be effective predation, parasitism) affecting H. halys eggs, (2) identify natural enemies of H. halys with parasitism rates as high as indigenous parasitoids associated with H. halys eggs, and 84.7% (Zhang et al. 1993; Chu et al. 1997; Qiu 2007; Hou (3) quantify the impact of egg parasitoids on H. halys egg et al. 2009), suggesting biological control has a potential mortality in ornamental nurseries. Effects of study site role in invaded ranges to keep H. halys in check. Classical location and host tree species on egg mortality and how the biological control, which entails releasing natural enemies exposure period of eggs to predation and parasitism impact from the home land of the introduced pest, often takes their mortality was also examined. multiple years of host specificity testing and other risk assessment procedures before initial releases of exotic natural enemies can begin (Kenis et al. 2017). Efforts Materials and methods toward classical biological control are well underway in the USA (Rice et al. 2014; Talamas et al. 2015, Herlihy et al. Study sites and experimental design 2016; Santacruz et al. 2017). Recently, an adventive pop- ulation of Tr. japonicus, a parasitoid of H. halys in its Three field sites in Maryland, USA, were selected for this native range, has been confirmed in several US states study. Selected nurseries were known to contain high pop- (Talamas et al. 2015; Herlihy et al. 2016; Milnes and Beers ulations of H. halys and an associated high abundance of 2016). The distribution, host use, and impact of this naturally laid H. halys egg masses, which allows for a more adventive population of Tr. japonicus are currently under realistic and statistically rigorous estimate of parasitoid study (P. Shrewsbury, unpublished). activity (Jones et al. 2014; Herlihy et al. 2016). The nursery Though classical biological control is an option, it is sites and tree species sampled were the same as those used also important to elucidate native natural enemies impacts in Jones et al. (2014) which provides a detailed description on H. halys within its invaded range, and ultimately their of sites and trees. Nursery sites included Raemelton Farm in potential use in augmentative (rearing and release of native Adamstown, MD (Frederick County) and two additional parasitoids) or conservation (habitat manipulation to favor sites at Ruppert Nurseries in Laytonsville, MD (Mont- parasitoids) biological control approaches. Several studies gomery County). Three genera of trees were chosen for have been conducted to examine the identity and impact of monitoring at each nursery site based on preliminary 123 J Pest Sci observations that H. halys used these genera as oviposition Individual eggs in each mass were monitored to determine hosts (Shrewsbury, unpublished). Trees included Acer their fate. Emerging H. halys nymphs and parasitoids were rubrum L. ‘Franksred’ (red maple), Prunus serrulata L. removed and unhatched eggs were assessed for other ‘Kwanzan’ (ornamental cherry), Ulmus americana L. causes of mortality. Parasitoids that emerged were placed ‘Princeton’ (American elm), and Ulmus parvifolia Jacq. in 70% ethanol for later identification. Egg parasitoids were ‘Patriot’ (Chinese elm). Two species of elms were used as identified according to Dieckhoff (unpublished). The there were a limited number of any one species at the dif- number of parasitoids emerging and their sex were recor- ferent sites. The number of trees surveyed for each species ded. Females were identified to species, and males were varied between nurseries due to differences in abundance of pooled by genus due to difficulty in identification and the test species at each nursery (Table 1).