Next Article in Journal
The Interacting Head Motif Structure Does Not Explain the X-Ray Diffraction Patterns in Relaxed Vertebrate (Bony Fish) Skeletal Muscle and Insect (Lethocerus) Flight Muscle
Previous Article in Journal
Rational Design of an Orthogonal Pair of Bimolecular RNase P Ribozymes through Heterologous Assembly of Their Modular Domains
 
 
Order Article Reprints
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:
Background:
Communication

Parasitism of the Invasive Brown Marmorated Stink Bug, Halyomorpha halys (Hemiptera: Pentatomidae), by the Native Parasitoid, Trichopoda pennipes (Diptera: Tachinidae)

1
Department of Entomology and Plant Pathology, 217 Plant Science Building, University of Arkansas, Fayetteville, AR 72701, USA
2
Department of Biology, Long Island University, 1 University Plaza, Brooklyn, NY 11201, USA
3
Fruit Research and Extension Center, Entomology, Pennsylvania State University, 290 University Drive, Biglerville, PA 17307, USA
*
Authors to whom correspondence should be addressed.
Biology 2019, 8(3), 66; https://doi.org/10.3390/biology8030066
Received: 31 July 2019 / Revised: 30 August 2019 / Accepted: 5 September 2019 / Published: 14 September 2019
(This article belongs to the Section Ecology)

Abstract

:
The invasive brown marmorated stink bug, Halyomorpha halys (Hemiptera: Pentatomidae), has been an important agricultural pest in the Mid-Atlantic United States since its introduction in 1996. Biological control by native species may play an important role in suppressing H. halys populations and reduce reliance on chemical control. We collected H. halys adults in agricultural areas of five Pennsylvania counties over two years to examine the extent and characteristics of adult stink bug parasitism by Trichopoda pennipes (Diptera: Tachinidae), a native parasitoid of hemipterans. The overall parasitism rate (in terms of T. pennipes egg deposition) was 2.38 percent. Rates differed among counties and seasons, but not between years. Instances of supernumerary oviposition were evident, and eggs were more commonly found on the ventral side of the thorax, although no differences in egg deposition were found between males and female hosts. T. pennipes has begun to target H. halys adults in Pennsylvania and has the potential to play a role in regulating this pest. Adult parasitism of H. halys by T. pennipes should continue to be monitored, and landscape management and ecological pest management practices that conserve T. pennipes populations should be supported in agricultural areas where H. halys is found.

1. Introduction

The invasive brown marmorated stink bug, Halyopmorpha halys Stål (Hemiptera: Pentatomidae), was first found in Allentown, PA in the United States in 1996 [1] and has since spread to many states throughout the country, as well as to Canada, Europe and South America [2,3]. H. halys, which is native to Eastern Asia, has become an economically important pest of many crops in the U.S., especially tree fruit in the Mid-Atlantic states [3,4]. For example, in Eastern U.S. apples and peaches, H. halys was shown to damage up to 25% of fruit per tree [5], and losses in apple production exceeded $37 million in 2010 alone [3]. As a result, the frequency and intensity of insecticide applications to control H. halys in orchards has also increased substantially [6]. There are relatively few insecticides that provide reliable control of H. halys adults, which fly into the orchards from adjacent managed and unmanaged habitats in the late summer and fall close to harvest for apples and peaches. This further restricts insecticide control options to those with short pre-harvest label restrictions. The majority of insecticides have limited residual activity against the adults, whereas eggs and nymphs are easier to control [7]. As an agricultural pest, H. halys is a promising candidate for biological regulation by predators and parasitoids, since it spends the majority of the fruit-growing season in unmanaged, wooded habitats rather than in agricultural crops where pesticides can limit biological control [8].
In commercial agriculture settings, as well as other ecosystems, the decoupling of invasive pests from their native biocontrol agents is often thought to be the most probable mechanism by which invasive species become extremely successful pest species [9]. Classical biological control programs seek to correct this imbalance by importing co-evolved natural enemies from the countries of origin, but this technique has been called into question for impacts on non-target arthropods and further disruption of natural ecosystems [10,11,12,13]. It has been argued that invasion biologists and ecologists should consider responses of native biological control agents (parasitoids and predators) to invasive host species [14]. Native species of predators and parasitoids may play an important role in regulating populations of not only native host species, but also other related invasive and exotic host species. Such shifts in the preference of native natural enemies may influence the population dynamics and long-term establishment of exotic species [14]. Classical biological control may have the advantage of much more rapid control of the co-evolved exotic prey than native predators or parasitoids, which may take many years to adapt to new prey, but native biological control agents have the advantage of already being adapted to local environmental conditions and ecosystems.
While classical biological control of exotic pests in agriculture has met with some notable successes in the past, there have also been some failures where the introduced species negatively impacted non-target species [12]. It is these failures that have led to more stringent regulatory constraints in releasing exotic biological control agents [15]. Many exotic biological control introductions have been made with little knowledge or consideration of the biological control factors already present in the introduced ecosystem. Due to a tendency to focus on exotic biological control agents of exotic prey, there is often less information on the importance of native natural enemies in controlling populations of exotic species. However, in the area of tree fruit integrated pest management (IPM) in the U.S., there are several key examples in which the primary biological control agents of exotic pests – such as codling moth [Cydia pomonella (L.)], Oriental fruit moth [Grapholita molesta (Busck)], spotted wing drosophila [Drosophila suzukii (Matsumura)], and European red mite (Panonychus ulmi Koch)—are native predators or parasitoids that adapted to these exotic hosts over time [16,17,18].
This study was part of a large, multi-state group effort to survey for and characterize the impact of indigenous arthropod natural enemies that were attacking H. halys [19]. In the Mid-Atlantic region, there are several parasitoids of stink bugs that could potentially contribute to H. halys control. Here, we focus on field parasitism by Trichopoda pennipes Fab. (Diptera: Tachinidae) that was previously noted to parasitize this introduced pest in caged studies [20]. This common and widely distributed fly is found throughout North America and is reported to have three geographically isolated host strains that are important in the biological control of several species of Coreidae, Pentatomidae and Largidae [21]. While most parasitoids target the egg stage of stink bugs, T. pennipes targets the adults (and late-stage nymphs), a life stage that is more difficult to control chemically. In this study, we document and provided baseline data on adult H. halys parasitism rates (in terms of egg deposition on the host) in the field by T. pennipes in several counties of Pennsylvania. In addition, both the sex of the host and the location of the tachinid eggs on the host were recorded, since the location of where the eggs are laid is important to the successful penetration of the host cuticle by tachinids [22], and there has been speculation that the ventral thoracic pheromone glands of the male stink bugs are likely the main host finding mechanism [20].

2. Materials and Methods

2.1. Field Collection

A total of 43 samples ranging from 21 to 868 H. halys adults were collected from orchards, vegetables, field crops and overwintering sites in buildings during the 2012 and 2013 growing seasons as part of an effort to establish laboratory colonies for pesticide bioassay work. Samples were taken from 11 locations spread across five Pennsylvanian counties: Adams, Allegheny (2013 only), Berks (2012 only), Franklin and Lancaster. Field-collected adults were maintained in screened cages where they were allowed to mate and lay eggs to start new colonies for bioassays.

2.2. Oviposition Patterns

Spent adults were placed in plastic petri dishes and then examined for the presence of tachinid eggs and any resulting tachinid flies that emerged from these cadavers were collected and identified. For each parasitized individual, the sex of the host and the location of the tachinid eggs on the host were recorded. Records related to location of egg deposition indicated whether eggs were found on the dorsal or ventral surface, and whether eggs were on the thorax or the abdomen (in only rare instances was an egg found on the head of the host). Because multiple eggs on a single host may occur—despite only a single parasitoid ultimately surviving [23]—the number of eggs on each host was also recorded.
T. pennipes eggs on H. halys hosts were identified according to the original description and drawings [24], photographs and descriptions [20], and from adults reared from parasitized hosts. Parasitized H. halys and reared T. pennipes adults are preserved and stored at the Penn State Frost Entomological Museum, University Park, PA or the Penn State Fruit Research and Extension Center, Biglerville, PA, U.S.

2.3. Data Analysis

Chi-square contingency tests were conducted to examine independence of parasitism frequency between years, among counties, and among seasons. Collection dates within years spanned three seasons—spring (Mar 20–Jun 20), summer (Jun 21–Sept 21), and fall (Sept 22–Dec 20)—and were grouped accordingly for seasonal analysis. The Holm’s sequential Bonferroni method was used for post hoc comparisons in parasitism rates among counties and seasons. One-sample t-tests were conducted to examine if parasitism rates (i.e., percent of tachinid eggs deposited on H. halys) were significantly different from the expected value of 50 percent for: (1) males and females; (2) dorsal and ventral surface; and (3) thorax and abdomen. Since t-tests were based on percentage values, samples with small numbers of total eggs found (i.e., ≤5) were excluded from the analysis. Lastly, a descriptive analysis of frequency of supernumerary oviposition was conducted.

3. Results

During the two-year study, a total of 7857 H. halys adults were collected (2012: n = 4737; 2013: n = 3120) from 43 samples, of which 187 H. halys were parasitized (2.38%). Thirty of the 43 samples contained at least one parasitized individual. The percentage of parasitized individuals did not differ between the two years of the study [Figure 1; χ2 (1, N = 7587) = 1.37, p = 0.24]. Numerous H. halys adults were collected from multiple samples in Adams (n = 3332 individuals), Lancaster (n = 2178), and Franklin (n = 1636) counties, whereas fewer individuals were collected from a single sample taken in each of Allegheny (n = 121) and Berks (n = 590) counties. Parasitism rates differed among counties and ranged from 1.2 to 3.3 percent [Figure 1; (χ2 (4, N = 7587) = 14.07, p = 0.007]. H. halys adults were collected over three seasons: spring (n = 981), summer (n = 1477) and fall (n = 5399). Parasitism rates were higher in spring than in summer and fall [Figure 1; χ2 (2, N = 7587) = 19.33, p < 0.0001].
A total of 259 eggs were found on the 187 parasitized H. halys adults. There was no difference in the percentage of eggs found on males versus females (Figure 2; t(15) = 0.15, p = 0.88). However, a greater percentage of eggs was found on the ventrum relative to dorsum (Figure 2; t(17) = 3.01, p = 0.008), and on the thorax relative to the abdomen (Figure 2; t(17) = 3.42, p = 0.003).
Supernumerary oviposition (>1 egg/host) was observed on 22.4 percent of parasitized H. halys adults, whereas 77.8 percent had only one parasitoid egg (Figure 3). An average of 1.38 eggs was found on parasitized H. halys adults with up to nine eggs found on a single individual (Figure 3).

4. Discussion

Native predators and parasitoids have the potential to play an important role in the regulation of invasive species populations [14]. This study provides evidence that the native tachinid fly and known parasitoid of hemipterans, T. pennipes, is targeting up to 3.3% of adult brown marmorated stink bugs (H. halys) in Pennsylvanian agricultural landscapes. Other studies have recently provided evidence of other indigenous species exploiting H. halys [19] including egg parasitoids [25,26], egg predators [27], and nymph/adult predators [28,29,30]. Our findings, in combination with these other studies, reveal that native predators and parasitoids have begun to use the invasive H. halys as a food source or host, and could help regulate populations of this economically important pest.
Although current adult parasitism rates are quite low, it is possible that the contribution of T. pennipes to the biological control of H. halys could increase over time. T. pennipes is multivoltine and a single adult female can lay hundreds of eggs. In addition, T. pennipes is already known to parasitize a range of other hemipteran pests [31]. Parasitism by T. pennipes can influence both lifetime fecundity and population growth of pests such as the southern green stink bug [Nezara viridula (L.)], although the effectiveness of T. pennipes can be limited due to the fact that the adult host is not immediately killed [32,33]. T. pennipes can also show host preference, and actually consists of a complex of biotypes or cryptic species across North America that specialize on regionally abundant pests, such as squash bugs [Anasa tristis (DeGeer)] [34] and bordered plant bugs [Largus californicus (Van Duzee)] in California [35]. It is thus worth monitoring if the exploitation of H. halys by T. pennipes increases in the Mid-Atlantic region of the U.S., and determining if this may represent the emergence of a new regional biotype that specializes on H. halys.
T. pennipes populations should be conserved as part of the larger community of indigenous natural enemies in Mid-Atlantic agricultural landscapes to encourage biological control and potentially reduce reliance on insecticide use against H. halys. Native species of stink bugs in this area, which can cause catfacing (peaches), dimpling, scarring, discoloration and internal corking on tree fruits, are considered relatively minor pests, as their populations are held in check by a complex of parasitoids and generalist predators. Since H. halys exhibits similar characteristics and often moves into cropping areas from a surrounding unmanaged habitat, the best option for long-term population suppression may come from biological control in areas outside of the crop. However, in the absence of robust natural regulation, broad-spectrum insecticides, such as pyrethroids, are often needed for H. halys control. These products can impact the natural enemy community as a whole and can be quite disruptive to current IPM programs in tree fruit [6,36,37,38]. Similarly, pesticide drift to field margins or forest edges could negatively affect pollinators and natural enemies using these extra-orchard habitats.
Our study found different parasitism rates among locations and this may have to do with T. pennipes abundance in the surrounding landscape. Certain plants, especially members of Asteraceae and Apiaceae, are known to support populations of beneficial flies such as syrphids and tachinids in agricultural areas [39]. For example, in Pennsylvania, T. pennipes emerges in late spring and has been observed using nectar sources from host plants such as wild carrot (Dacaus carota L.) and goldenrod (Solidago spp. L.) [39]. In general, agricultural landscapes with higher levels of plant diversity and/or habitat structure can provide shelter, favorable microclimatic conditions, and alternative food sources for natural enemies [40,41,42,43]. Therefore, providing nectar-rich resources in agricultural landscapes, whether through deliberate floral plantings or setting aside unmanaged areas in field margins, could potentially result in greater numbers of parasitoids and increased biological control (i.e., “parasitoid nectar provision hypothesis”) [43], and can be an important part of integrated pest and pollinator management (IPPM) programs in tree fruit orchards [44], where H. halys is an important pest and causes severe fruit infestation.
In this study, we found significantly higher parasitism in H. halys adults during the spring season. Higher incidence of parasitism detected in the spring may have been an artifact of time, as eggs may have been deposited on spring-collected H. halys either during the previous year (prior to overwintering) or during the spring collection period. We also found significant patterns related to the location of egg deposition on H. halys adults. Studies suggest that T. pennipes locates stinkbug hosts by following the thoracic aggregation pheromones secreted by males [22,45] and field collections of southern green stinkbugs (Nezara viridula) found a greater number of parasitized males than females [46]. While our results did reveal a distinct preference for egg deposition on the ventral side of the thorax of H. halys adults, we did not find a preference for males. It is possible that T. pennipes used the male pheromones to locate H. halys aggregations and then laid eggs indiscriminately among males and females. Although not included in this analysis of adult parasitism, last instar nymphs of field-collected H. halys were also found with T. pennipes eggs, which supports previous findings that members of the Phasiine endoparasitoid group of Tachinidae are attracted to nymphal defensive allomones despite attacking mostly the adult stages [20,47].

5. Conclusions

Here, we provide evidence that T. pennipes has begun to target H. halys adults in agricultural landscapes of Pennsylvania, although at low rates. Parasitism rates varied across seasons and location. Although other studies suggest that T. pennipes more frequently targets male hosts, we found no difference in egg deposition on male and female hosts; however, T. pennipes oviposited more frequently on the ventral side of the thorax relative to other body regions of the host. T. pennipes is an effective and regionally specialized parasitoid of other hemipteran pests throughout the U.S. and thus has potential to contribute to the biological control of H. halys. In combination with targeted floral provisions and judicious use of insecticides, biological control by T. pennipes and other native parasitoids and predators, may play an increasingly prominent role in suppressing H. halys populations as part of IPM programs in the Mid-Atlantic region of the U.S.

Author Contributions

Conceptualization, D.J.B. and N.K.J.; methodology, D.J.B. and N.K.J.; software, T.W.L.; validation, T.W.L., D.J.B. and N.K.J.; formal analysis, T.W.L.; investigation, D.J.B. and N.K.J.; resources, D.J.B.; data curation, T.W.L.; writing—original draft preparation, T.W.L., N.K.J. and D.J.B.; writing—review and editing, N.K.J., T.W.L., and D.J.B.; visualization, T.W.L.; supervision, D.J.B.; project administration, D.J.B.; funding acquisition, D.J.B.

Funding

This research was supported in part by the USDA NIFA SCRI 2011-01413-30937, the State Horticultural Association of Pennsylvania (SHAP), and the Pennsylvania State University Hatch Project No. Pen04619.

Acknowledgments

Authors are thankful to K. Wholaver for project assistance during the study period.

Conflicts of Interest

The authors declare no conflict of interest.

References

  1. Hoebeke, E.R.; Carter, M.E. Halyomorpha halys (Stahl) (Heteroptera: Pentatomidae): A polyphagous plant pest from Asia newly detected in North America. Proc. Entomol. Soc. Wash. 2003, 105, 225–237. [Google Scholar]
  2. Haye, T.; Gariepy, T.; Hoelmer, K.; Rossi, J.-P.; Streito, J.-C.; Tassus, X.; Desneux, N. Range expansion of the invasive brown marmorated stinkbug, Halyomorpha halys: An increasing threat to field, fruit and vegetable crops worldwide. J. Pest Sci. 2015, 88, 665–673. [Google Scholar] [CrossRef]
  3. Leskey, T.C.; Nielsen, A.L. Impact of the invasive brown marmorated stink bug in North American and Europe: History, biology, ecology, and management. Annu. Rev. Entomol. 2018, 63, 599–618. [Google Scholar] [CrossRef] [PubMed]
  4. Kuhar, T.P.; Kamminga, K.L.; Whalen, J.; Dively, G.P.; Brust, G.; Hooks, C.R.R.; Hamilton, G.; Herbert, D.A. The Pest Potential of Brown Marmorated Stink Bug on Vegetable Crops. Plant Heal. Prog. 2012, 13, 41. [Google Scholar] [CrossRef]
  5. Nielsen, A.L.; Hamilton, G.C. Seasonal occurrence and impact of Halyomorpha halys (Hemiptera: Pentatomidae) in tree fruit. J. Econ. Entomol. 2009, 102, 1133–1140. [Google Scholar] [CrossRef] [PubMed]
  6. Leskey, T.C.; Short, B.D.; Butler, B.R.; Wright, S.E. Impact of the invasive brown marmorated stink bug, Halymorpha halys (Stal), in mid-Atlantic tree fruit orchards in the United States: Case studies of commercial management. Psyche A J. Entomol. 2012, 535062, 2012. [Google Scholar] [CrossRef]
  7. Rice, K.B.; Berg, C.J.; Bergmann, E.J.; Biddinger, D.J.; Dieckhoff, C.; Dively, G.; Fraser, H.; Gariepy, T.; Hamilton, G.; Hayes, T.; et al. Biology, ecology, and management of brown marmorated stink bug (Hemiptera: Pentatomidae). J. Integr. Pest Manag. 2014, 5, A1–A13. [Google Scholar] [CrossRef]
  8. Bakken, A.J.; Schoof, S.C.; Bickerton, M.; Kamminga, K.L.; Jenrette, J.C.; Malone, S.; Abney, M.A.; Herbert, D.A.; Reisig, D.; Kuhar, T.P.; et al. Occurrence of Brown Marmorated Stink Bug (Hemiptera: Pentatomidae) on Wild Hosts in Nonmanaged Woodlands and Soybean Fields in North Carolina and Virginia. Environ. Entomol. 2015, 44, 1011–1021. [Google Scholar] [CrossRef][Green Version]
  9. Colautti, R.I.; Ricciardi, A.; Grigorovich, I.A.; MacIsaac, H.J. Is invasion success explained by the enemy release hypothesis? Ecol. Lett. 2004, 7, 721–733. [Google Scholar] [CrossRef]
  10. Lockwood, J.A. The ethics of biological control: Understanding the moral implications of our most powerful ecological technology. Agric. Hum. Values 1996, 13, 2–19. [Google Scholar] [CrossRef]
  11. Lockwood, J.A. The ethics of “classical” biological control and the value of place. In Balancing Nature: Assessing the Impact of Importing Non-Native Biological Control Agents (An International Perspective); Lockwood, J.A., Howarth, F.G., Purcell, M.F., Eds.; Thomas Say Publications in Entomology, Entomological Society of America: Lanham, MD, USA, 2001; pp. 100–119. [Google Scholar]
  12. Lockwood, J.A.; Purcell, M.F.; Howarth, F.G. The value of place and the place of values. In Balancing Nature: Assessing the Impact of Importing Non-Native Biological Control Agents (An International Perspective); Lockwood, J.A., Howarth, F.G., Purcell, M.F., Eds.; Thomas Say Publications in Entomology, Entomological Society of America: Lanham, MD, USA, 2001; pp. 1–2. [Google Scholar]
  13. Howarth, F.G. Environmental issues concerning the importation of nonindigenous biological control agents. In Balancing Nature: Assessing the Impact of Importing Non-Native Biological Control Agents (An International Perspective); Lockwood, J.A., Howarth, F.G., Purcell, M.F., Eds.; Thomas Say Publications in Entomology, Entomological Society of America: Lanham, MD, USA, 2001; pp. 70–99. [Google Scholar]
  14. Carlson, N.O.; Sarnelle, O.; Strayer, D.L. Native predators and exotic prey—An acquired taste? Front. Ecol. Environ. 2009, 7, 525–532. [Google Scholar] [CrossRef]
  15. Messing, R.H.; Purcell, M.F. Regulatory constraints to the practice of biological control in Hawaii. In Balancing Nature: Assessing the Impact of Importing Non-Native Biological Control Agents (An International Perspective); Lockwood, J.A., Howarth, F.G., Purcell, M.F., Eds.; Thomas Say Publications in Entomology, Entomological Society of America: Lanham, MD, USA, 2001; pp. 3–14. [Google Scholar]
  16. Allen, H.W. Parasites of the Oriental Fruit Moth in the Eastern United States; Agricultural Research Service, US Department of Agriculture: Washington, DC, USA, 1962; p. 1265.
  17. Stacconi, M.V.R.; Grassi, A.; Dalton, D.T.; Miller, B.; Ouantar, M.; Loni, A.; Ioriatti, C.; Walton, V.M.; Anfora, G. First field records of Pachycrepoideus vindemiae as a parasitoid of Drosphila suzukii in European and Oregon small fruit production areas. Entomologia 2013, 1, 11–16. [Google Scholar]
  18. Biddinger, D.; Butler, B.; Joshi, N.K. Biological control of mites in Pennsylvania and Maryland apple orchards. Pa. Fruit News 2014, 91, 41–51. [Google Scholar]
  19. Abram, P.K.; Hoelmer, K.A.; Acebes-Doria, A.; Andrews, H.; Beers, E.H.; Bergh, J.C.; Bessin, R.; Biddinger, D.; Botch, P.; Buffington, M.L.; et al. Indigenous arthropod natural enemies of the invasive brown marmorated stink bug in North America and Europe. J. Pest Sci. 2017, 90, 1009–1020. [Google Scholar] [CrossRef]
  20. Aldrich, J.R.; Khrimian, A.; Zhang, A.; Shearer, P.W. Bug pheromones (Hemiptera: Heteroptera) and tachinid fly host-finding. Denisia 2006, 19, 1015–1031. [Google Scholar]
  21. Pickett, C.H.; Schoenig, S.E.; Hoffman, M.P. Establishment of the squash bug parasitoid Trichopoda pennipes Fabr. (Diptera: Tachinidae), in northern California. Pan-Pac. Entomol. 1996, 72, 220–226. [Google Scholar]
  22. Shahjahan, M.; Beardsley, J.W. Egg viability and larval penetration in Trichopoda pennipes pilipes Fabricius (Diptera: Tachinidae). Proc. Hawaii. Entomol. Soc. 1975, 21, 133–136. [Google Scholar]
  23. Todd, J.W.; Lewis, W.J. Incidence and oviposition patterns of Trichopoda pennipes (F), a parasite of the southern green stink bug, Nezara viridula (L.). J. Ga. Entomol. Soc. 1976, 11, 50–54. [Google Scholar]
  24. Worthley, H.N. The biology of Trichopoda pennipes Fab. (Diptera, Tachinidae), a parasite of the common squash bug. Psyche A J. Entomol. 1924, 31, 7–16. [Google Scholar] [CrossRef]
  25. Herlihy, M.V.; Talamas, E.J.; Weber, D.C. Attack and Success of Native and Exotic Parasitoids on Eggs of Halyomorpha halys in Three Maryland Habitats. PLoS ONE 2016, 11, e0150275. [Google Scholar] [CrossRef]
  26. Moraglio, S.T.; Tortorici, F.; Pansa, M.G.; Castelli, G.; Pontini, M.; Scovero, S.; Visentin, S.; Tavella, L. A 3-year survey on parasitism of Halyomorpha halys by egg parasitoids in northern Italy. J. Pest Sci. 2019. [Google Scholar] [CrossRef]
  27. Morrison, W.R., III; Mathews, C.R.; Leskey, T.C. Frequency, efficiency, and physical characteristics of predation by generalist predators of brown marmorated stink bug (Hemiptera: Pentatomidae) eggs. Biol Control 2016, 97, 120–130. [Google Scholar] [CrossRef][Green Version]
  28. Biddinger, D.J.; Joshi, N.K. First report of native Astata unicolor (Hymenoptera: Crabronide) predation on the nymphs and adults of the invasive brown marmorated stink bug, Halyomorpha halys (Hemiptera: Pentatomidae). Fla. Entomol. 2017, 100, 809–812. [Google Scholar] [CrossRef]
  29. Biddinger, D.; Surcica, A.; Joshi, N.K. A native predator utilizing the invasive brown marmorated stink bug, Halyomorpha halys (Hemiptera: Pentatomidae) as a food source. Biocontrol Sci. Technol. 2017, 27, 903–907. [Google Scholar] [CrossRef]
  30. Morrison, W.R., III; Bryant, A.N.; Poling, B.; Quinn, N.F.; Leskey, T.C. Predation of Halyomorpha halys (Hemiptera: Pentatomidae) from web-building spiders associated with anthropogenic dwellings. J. Insect Behav. 2017, 30, 70–85. [Google Scholar] [CrossRef]
  31. Arnaud, J. Host-Parasite Catalog of North American Tachnidae (Diptera); United States Department of Agriculture, Science and Education Administration: Washington, DC, USA, 1978.
  32. Harris, V.E.; Todd, J.W. longevity and reproduction of the southern green stink bug, nezara viridula, as affected by parasitization by trichopoda pennipes. Entomol. Exp. Et Appl. 1982, 31, 409–412. [Google Scholar] [CrossRef]
  33. De Salles, L.A.B. Effect of Trichopoda pennipes parasitization on Nezara viridula. Pesq. Agropec. Bras. 1992, 27, 981–986. [Google Scholar]
  34. Decker, K.B.; Yeargan, K.V. Seasonal phenology and natural enemies of the squash bug (Hemiptera: Coreidae) in Kentucky. Environ. Entomol. 2014, 37, 670–678. [Google Scholar] [CrossRef]
  35. Booth, C.L. Biology of Largus californicus (Hemiptera: Largidae). Southwest. Nat. 1990, 35, 15. [Google Scholar] [CrossRef]
  36. Biddinger, D.J.; Leslie, T.W.; Joshi, N.K. Reduced-risk pest management programs for eastern U.S. peach orchards: Effects on arthropod predators, parasitoids, and select pests. J. Econ. Entomol. 2014, 107, 1084–1091. [Google Scholar] [CrossRef]
  37. Beard, R.L. The biology of Anasa tristis DeGeer with particular reference to the tachinid parasite, Trichopoda pennipes Fabr. Bull. Conn. Agric. Exp. Stn. 1940, 440, 595–680. [Google Scholar]
  38. Blaauw, B.R.; Polk, D.; Nielsen, A.L. IPM-CPR for peaches: Incorporating behaviorally-based methods to manage Halyomporpha halys and key pests in peach. Pest Manag. Sci. 2015, 71, 1513–1522. [Google Scholar] [CrossRef] [PubMed]
  39. Tooker, J.F.; Hauser, M.; Hanks, L.M. Floral Host Plants of Syrphidae and Tachinidae (Diptera) of Central Illinois. Ann. Entomol. Soc. Am. 2006, 99, 96–112. [Google Scholar] [CrossRef]
  40. Wratten, S.D.; Landis, D.A.; Gurr, G.M. Habitat Management to Conserve Natural Enemies of Arthropod Pests in Agriculture. Annu. Rev. Entomol. 2000, 45, 175–201. [Google Scholar]
  41. Langellotto, G.A.; Denno, R.F. Responses of invertebrate natural enemies to complex-structured habitats: A meta-analytical synthesis. Oecologia 2004, 139, 1–10. [Google Scholar] [CrossRef] [PubMed]
  42. Bianchi, F.; Booij, C.; Tscharntke, T. Sustainable pest regulation in agricultural landscapes: A review on landscape composition, biodiversity and natural pest control. Proc. R. Soc. B Boil. Sci. 2006, 273, 1715–1727. [Google Scholar] [CrossRef] [PubMed]
  43. Heimpel, G.E.; Jervis, M.A. Does floral nectar improve biological control by parasitoids. In Plant-Provided Food for Carnivorous Insects; Wackers, F.L., van Rijn, P.C.J., Bruin, J., Eds.; Cambridge University Press: Cambridge, MA, USA, 2005; pp. 267–304. [Google Scholar]
  44. Biddinger, D.; Rajotte, E.G.; Joshi, N.K. Integrating pollinator health into tree fruit IPM—A case study of Pennsylvania apple production. In The Pollination of Cultivated Plants: A Compendium for Practitioners, 2nd ed.; FAO: Rome, Italy, 2018; Volume 1, pp. 69–83. [Google Scholar]
  45. Harris, V.E.; Todd, J.W. Male mediated aggregation of male, female and 5th instar southern green stink bugs and concomitant attraction of a tachinid parasite, Trichopoda pennipes. Entomol. Exp. Appl. 1980, 27, 117–126. [Google Scholar] [CrossRef]
  46. Mitchell, W.C.; Mau, R.F.L. Response of the female southern green stink bug and its parasite, Trichopoda pennipes, to male stink bug pheromones. J. Econ. Entomol. 1971, 64, 856–859. [Google Scholar] [CrossRef]
  47. Aldrich, J.R. Chemistry and biological activity of pentatomid sex pheromones. In Biologically Active Natural Products: Potential Use in Agriculture; Cutler, H.G., Ed.; American Chemical Society: Washington, DC, USA, 1988; pp. 417–431. [Google Scholar]
Figure 1. A comparison of H. halys adult parasitism rates between years, among counties, and among seasons in Pennsylvania (2012–2013).
Figure 1. A comparison of H. halys adult parasitism rates between years, among counties, and among seasons in Pennsylvania (2012–2013).
Biology 08 00066 g001
Figure 2. Mean percentage (+/− SEM) of T. pennipes eggs deposited on H. halys adults: (1) males versus females; (2) dorsum versus ventrum; and (3) thorax versus abdomen. a,b Different letters indicate significant differences in means.
Figure 2. Mean percentage (+/− SEM) of T. pennipes eggs deposited on H. halys adults: (1) males versus females; (2) dorsum versus ventrum; and (3) thorax versus abdomen. a,b Different letters indicate significant differences in means.
Biology 08 00066 g002
Figure 3. Frequency distribution of number of T. pennipes eggs found on parasitized H. halys adults.
Figure 3. Frequency distribution of number of T. pennipes eggs found on parasitized H. halys adults.
Biology 08 00066 g003

Share and Cite

MDPI and ACS Style

Joshi, N.K.; Leslie, T.W.; Biddinger, D.J. Parasitism of the Invasive Brown Marmorated Stink Bug, Halyomorpha halys (Hemiptera: Pentatomidae), by the Native Parasitoid, Trichopoda pennipes (Diptera: Tachinidae). Biology 2019, 8, 66. https://doi.org/10.3390/biology8030066

AMA Style

Joshi NK, Leslie TW, Biddinger DJ. Parasitism of the Invasive Brown Marmorated Stink Bug, Halyomorpha halys (Hemiptera: Pentatomidae), by the Native Parasitoid, Trichopoda pennipes (Diptera: Tachinidae). Biology. 2019; 8(3):66. https://doi.org/10.3390/biology8030066

Chicago/Turabian Style

Joshi, Neelendra K., Timothy W. Leslie, and David J. Biddinger. 2019. "Parasitism of the Invasive Brown Marmorated Stink Bug, Halyomorpha halys (Hemiptera: Pentatomidae), by the Native Parasitoid, Trichopoda pennipes (Diptera: Tachinidae)" Biology 8, no. 3: 66. https://doi.org/10.3390/biology8030066

Note that from the first issue of 2016, MDPI journals use article numbers instead of page numbers. See further details here.

Article Metrics

Back to TopTop