The brown marmorated stink bug, Halyomorpha halys (Stål) (Hemiptera: Pentatomidae), is a highly polyphagous horticultural pest of northeastern Asia (Lee et al. Reference Lee, Short, Shimat, Bergh and Leskey2013). The discoveries of adults in North America and Europe suggest its potential to become a global pest (Lee Reference Lee2015). Some natural enemies, namely the parasitoid wasps Trissolcus mitsukurii (Ashmead) (Hymenoptera: Scelionidae) (Arakawa and Namura Reference Arakawa and Namura2002), Trissolcus plautiae (Watanabe) (Hymenoptera: Scelionidae) (Arakawa and Namura Reference Arakawa and Namura2002), Gryon japonicum (Ashmead) (Hymenoptera: Scelionidae) (Noda Reference Noda1990), and Trissolcus japonicus (Ashmead) (Hymenoptera: Scelionidae) (Avila and Charles Reference Avila and Charles2018), have been reported as egg parasitoids of H. halys in Japan. Moreover, tachinid bristle flies, Bogosia sp., are reported to parasitise the adults of H. halys in Japan (Kawada and Kitamura Reference Kawada and Kitamura1992). In this context, from 2015 onwards, the author found that the larvae of the parasitic tachinid fly, Pentatomophaga latifascia (Villeneuve), emerged from the adults of H. halys collected at a hibernation site in Akita Prefecture, northern Japan. The adult specimens were identified by Sin Komagata of the Biosystematics Laboratory, Faculty of Social and Cultural Studies, Kyushu University, Fukuoka, Japan.
Pentatomophaga latifascia was originally distributed in Asia, Japan, China, Korea, Russia, India, and Malaysia (Chen et al. Reference Chen, Li, Mi, Zhang, Shi and Zhang2020). Recently, Chen et al. (Reference Chen, Li, Mi, Zhang, Shi and Zhang2020) reported on the parasitic and morphological characteristics of P. latifascia and its potential as a biological control agent of H. halys. The eggs are laid on the surface of H. halys, and the hatched larvae penetrate the host body and feed on the haemolymph and nonvital tissues, eventually transitioning to the vital organs (Chen et al. Reference Chen, Li, Mi, Zhang, Shi and Zhang2020). The last larval instar emerges from the host to develop into a pupa, killing the host in the process (Chen et al. Reference Chen, Li, Mi, Zhang, Shi and Zhang2020). However, little is known about the biology of the tachinid fly. In the present study, P. latifascia’s potential to suppress H. halys overwintering populations was investigated.
Halyomorpha halys is univoltine in northern Japan, with most newly emerging adults appearing in September (Funayama Reference Funayama2008, Reference Funayama2013). Adults arrive at hibernation structures, such as houses and sheds, from late September through November and pass the winter (Funayama Reference Funayama2013). In the present study, the overwintering adults were collected from 2017 to 2019 from a building (39° 18′ N, 140° 38′ E) located in Yokote, Akita Prefecture, northern Japan, by using eight plastic container traps (63 × 33 × 31 cm; constructed by the author), each filled with 20 bundles of rice straw (60 cm long × 5 cm diameter). The traps were arranged on the veranda of the building from early September to mid-November each year and then removed, and live adults were collected. The total numbers of female and male adults were, respectively, 697 and 567 in 2017, 2490 and 1630 in 2018, and 1398 and 973 in 2019. The adults collected each year were put in transparent polypropylene bags (25 × 25 cm, with 1-mm-diameter holes all over), at about 50 adults per bag, and the bags were tied off at the top. Each of about six bags were wrapped in newspaper and placed individually in transparent polypropylene containers (27 × 20 × 10 cm) with a water-soaked cotton ball. The lid was then closed. The containers were placed in a shed at the Akita Fruit Tree Experiment Station (39.14° N, 140.32° E) located in Yokote, Akita Prefecture, before the start of rearing. The ambient temperature in the shed stayed below about 10 °C from December to February.
Experiment 1
Sixty-five females and 55 males of the adult H. halys carrying the eggs of P. latifascia on their body surfaces were sampled from among the adults collected in 2019. The adult H. halys were put individually into glass Petri dishes (2 cm high × 9 cm diameter) with a damp absorbent cotton ball and a fresh peanut. The dishes were then placed in an incubator (20 °C, 16:8 light:dark photoperiod). The cotton ball was soaked with water every five days, and the peanut was replaced with a fresh one to prevent rotting. The dishes were examined daily for viable H. halys adults and the presence of P. latifascia larvae or pupae until all H. halys died.
Experiment 2
On 1 March, from 2018 to 2020 (i.e., in the year after each collection of adult H. halys), 300 adult H. halys of each sex were sampled at random from among the adults collected the previous year. The adults were placed in groups of 50 in the transparent polypropylene containers (as described above), lined with filter paper (27 × 20 cm) on the bottom. The container had a transparent polyethylene lid with a 10 × 10-cm opening patched with a 224-μm-mesh nylon filter. Food and a water-soaked cotton ball were put into each container. The containers were placed in the incubator (as described above). The food was renewed and the cotton balls were soaked with water at five-day intervals. The containers were opened at two-day intervals, and the numbers of dead H. halys adults and of P. latifascia larvae and pupae were counted.
Unparasitised adult H. halys live a comparatively long time under suitable food conditions. For example, Funayama (Reference Funayama2004) reported that female and male adults reared on raw peanuts and soybeans under field conditions after overwintering survived a mean of 76.9 and 84.0 days, respectively. In contrast, in the present study, most of the overwintering adult female and male H. halys parasitised by P. latifascia lived for only a few days after emergence of the parasitoid larvae, and the total mean survival period (days until emergence of P. latifascia + days surviving after P. latifascia emergence; Table 1) was less than 30 days at 20 °C (experiment 1). Based on this, most of the overwintering adult female and male H. halys parasitised by P. latifascia can live only for a few days after the emergence of the parasitoid larvae. Moreover, none of the female adult H. halys from which P. latifascia emerged laid eggs. The parasitism of adult H. halys by Bogosia sp. seems similar: Bogosia sp. started to emerge 10–12 days after the start of H. halys rearing at 25 °C, and female and male H. halys adults survived for 5.3 and 2.3 days, respectively, after emergence of the parasitic flies (Kawada and Kitamura Reference Kawada and Kitamura1992). The newly hatched larvae of tachid flies penetrate into the host body and feed on the reproductive organs (Beard Reference Beard1940). Bogosia sp. hibernate in the host’s body as early instar larvae; they start to develop at the end of hibernation and grow to the final instar by feeding on the fat bodies of adult H. halys (Kawada and Kitamura Reference Kawada and Kitamura1992). Larval Bogosia sp. emerges from the reproductive organs, including the genital chamber, of adult H. halys at the end of hibernation (Kawada and Kitamura Reference Kawada and Kitamura1992). The emergence of P. latifascia may be similar to that of Bogosia sp., suggesting that adult H. halys parasitised by P. latifascia may be unable to reproduce, and die within a short period.
Numbers and survival periods of adult male and female Halyomorpha halys parasitised by Pentatomophaga latifascia at 20 °C
* Excluding the one female adult that survived 185 days.
Figure 1 shows the relationship between the percentage of H. halys survival and the emergence period of larvae of P. latifascia on adult H. halys reared at 20 °C after overwintering (experiment 2). Emergence of larvae P. latifascia was observed between 18 and 36 days after the start of rearing. The numbers of P. latifascia larvae emerging from 300 H. halys adult females and 300 adult males were, respectively, 36 and 32 in 2018, 35 and 31 in 2019, and 30 and 34 in 2020. No significant differences were found between H. halys females (5.6 ± 1.6) and males (5.4 ± 2.3; P = 0.374) in the mean numbers of larvae of P. latifascia emerging from 50 adults. No significant differences were found between the three years in the mean numbers of larvae of P. latifascia emerging from 50 adult H. halys of each sex (female: 6.0 ± 0.8 in 2018, 5.8 ± 2.1 in 2019, 5.0 ± 1.4 in 2020; F = 0.603, df = 2, 17, P = 0.560; male: 5.3 ± 2.4 in 2018, 5.2 ± 2.2 in 2019, 5.7 ± 2.1 in 2020; F = 0.064, df = 2, 17, P = 0.938) by Scheffé’s method (Excel Statistics 2012). These results suggest that P. latifascia was widespread at the collection site and that the population density of or numbers of eggs laid by P. latifascia changes with the population density of overwintering adult H. halys.
Relationship between survival rates of post-overwintering adult Halyomorpha halys and emergence times of their parasitising Pentatomophaga latifascia larvae at 20 °C from 2018 to 2020. Six replications of 50 adults of H. halys of each sex (i.e., 300 adults in total of each sex) were reared on raw peanuts and dry soybean seeds. Lines with open circles, survival rates of adult H. halys; bars, numbers of larvae of P. latifascia.
Most of the sampled unparasitised overwintering adult H. halys were still alive 30 days after the start of rearing, when they typically start to reproduce (Funayama Reference Funayama2012). In contrast, the survival rates of adult H. halys of each sex reared at 20 °C after overwintering decreased by about 10% during the period of larval emergence (Fig. 1). In this context, regression analysis (JMP 8; SAS Institute, Cary, North Carolina, United States of America) was used to determine the relationship between the cumulative numbers of larvae or pupae of P. latifascia emerging from adult H. halys of each sex each year and the cumulative numbers of dead adults of H. halys during the period of P. latifascia emergence. In all years, a significant positive correlation occurred between the cumulative numbers of larvae of P. latifascia emerging from adult H. halys (and counted as either larvae or as pupae outside the adult H. halys body) and the cumulative numbers of dead adults of H. hays in females (period: 18–32 days after the start of rearing in 2018: F = 25.00, df = 1, 7, P = 0.025, r = 0.898; 20–28 days after in 2019: F = 24.01, df = 1, 4, P = 0.016, r = 0.943; 26–36 days after in 2020: F = 13.14, df = 1, 5, P = 0.022, r = 0.876) and in males (period: 18–32 days after the start of rearing in 2018: F = 387.35, df = 1, 7, P < 0.001, r = 0.993; 20–28 days after in 2019: F = 29.72, df = 1, 4, P = 0.012, r = 0.953; 26–36 days after in 2020: F = 26.83, df = 1, 5, P = 0.007, r = 0.933). In experiment 1, only one larvae or pupae of P. latifascia emerged from one adult H. halys. Therefore, the 10% decrease in the survival percentage of adult H. halys may be related to the rate of parasitism of the field population by P. latifascia, which was about 10% each year. The rates of parasitism of overwintering female and male adult H. halys by Bogosia sp. are estimated to be similar, at 10.8% and 11.8%, respectively (Kawada and Kitamura Reference Kawada and Kitamura1992). The 10% rate of parasitism by P. latifascia is higher than that found by Chen et al. (Reference Chen, Li, Mi, Zhang, Shi and Zhang2020) in China, where the average parasitism rate was 2.42%. These observations indicate that P. latifascia contributed to a decrease in the population density of post-overwintering adult H. halys in the collection area, at least in early spring, suggesting that P. latifascia be considered a potentially suitable agent for the biological control of H. halys adults. Detailed investigations of the life history of P. latifascia will be needed for the practical application of tachinids to control H. halys.
