Entomopathogens infecting brown marmorated stink bugs before, during, and after overwintering

Abstract

The microsporidian, Nosema maddoxi Becnel, Solter, Hajek, Huang, Sanscrainte & Estep, infects brown marmorated stink bug, Halyomorpha halys (Stål) (Hemiptera: Pentatomidae), populations in North America and Asia and causes decreased fitness in infected insects. This host overwinters as adults, often in aggregations in sheltered locations, and variable levels of mortality occur over the winter. We investigated pathogen prevalence in H. halys adults before, during, and after overwintering. Population level studies resulted in detection of N. maddoxi in H. halys in 6 new US states, but no difference in levels of infection by N. maddoxi in autumn versus the following spring. Halyomorpha halys that self-aggregated for overwintering in shelters deployed in the field were maintained under simulated winter conditions (4°C) for 5 months during the 2021-2022 winter and early spring, resulting in 34.6 ± 4.8% mortality. Over the 2020-2021 and 2021-2022 winters, 13.4 ± 3.5% of surviving H. halys in shelters were infected with N. maddoxi, while N. maddoxi infections were found in 33.4 ± 10.8% of moribund and dead H. halys that accumulated in shelters. A second pathogen, Colletotrichum fioriniae Marcelino & Gouli, not previously reported from H. halys, was found among 46.7 ± 7.8% of the H. halys that died while overwintering, but levels of infection decreased after overwintering. These 2 pathogens occurred as co-infections in 11.1 ± 5.9% of the fungal-infected insects that died while overwintering. Increasing levels of N. maddoxi infection caused epizootics among H. halys reared in greenhouse cages after overwintering.

Keywords: Colletotrichum fioriniae; Halyomorpha halys; Nosema maddoxi; entomopathogens; overwintering.

Fig. 1.

Distribution of sites sampled in autumn 2019, spring 2020, or both, for comparisons of Nosema maddoxi infection levels.

Fig. 2.

Deployment of an overwintering shelter for Halyomorpha halys within the top apple crate on a stack of wooden apple crates. Arrow indicates the shelter and its location.

Fig. 3.

Presence/absence of Nosema maddoxi in Halyomorpha halys collected from sites sampled in autumn 2019 and/or spring 2020.

Fig. 4.

Increase in Nosema maddoxi infection levels starting with percent infection among living overwintering adults in shelters in April 2021. Adult Halyomorpha halys were moved to greenhouse cages (day 1) and percent N. maddoxi infection post-overwintering (living and dead) increased through 2 die-offs observed 26 May (after 42 d in cages) and 3 June (50 d in cages).