The effect of vineyard groundcover on the abundance of naturally occurring entomopathogenic fungi isolated using a quantitative Galleria bait method

Abstract

Although sold commercially as myco-insecticides, naturally occurring soil borne entomopathogenic fungi (EPF) pose a unique opportunity for regulating soil-dwelling insect herbivore populations via conservation biological control. Plant identity has a significant effect on soil borne fungi, which may includee EPF. We asked whether the choice of covercrops could affect the diversity and infectivity of EPF in a vineyard. We studied the effect of different mixtures of groundcover vegetation on the infectivity and community composition of the naturally occurring EPF community in a semi-arid vineyard in British Columbia, Canada. Soil was collected from a groundcover field trial and used in a quantitative laboratory bioassay with the model insect, Galleria mellonella. Death by mycosis was greater when Galleria was exposed to soil collected from groundcovers containing native versus exotic grasses. EPF communities isolated from Galleria cadavers also differed among groundcovers. This study presents the first evidence that manipulating vegetative identity can alter the composition and infectivity of soil-dwelling EPF. Future work should investigate the potential for groundcovers and cover crops to increase conservation biological control of soil-dwelling insect pests via changes to EPF communities in specific crop-pest scenarios.

Introduction

Along with an increasing awareness of the negative side effects of heavy insecticide use (Goulson, 2013), there has been a growing interest in managing agricultural landscapes to increase natural mortality of insect herbivores via conservation biological control (Daane et al., 2018; Winter et al., 2018). Naturally occurring biological pest control is estimated to be worth the equivalent of $4.5 billion worldwide (Losey and Vaughn, 2006). The viability of conservation biological control of insect pests, wherein habitat is managed to encourage beneficial insect species that prey upon or parasitize pests, is relatively well known and generally relies on the maintenance of diverse plant communities within cropping systems (Landis et al., 2000). Because plant communities can also affect soil fungal communities, including entomopathogenic fungi (Vukicevich et al., 2019), the manipulation of soil habitat to encourage indigenous entomopathogenic fungi (EPF) may offer another form of below ground conservation biological control. The idea of conservation biological control of soil dwelling insect pests via various management practices has been proposed (Meyling and Eilenberg, 2007; Pell et al., 2010) but until now, not tested experimentally in a perennial cropping system.

EPF are ubiquitous in most soils and include both host-specific pathogens such as those

in the Entomophthorales as well as more generalist pathogens in the Hypocreales (e.g. Beauveria spp., Metarhizium spp.) (Lacey et al., 2015). Although there has been considerable attention on the

factors controlling their distribution in soils (Quesada-Moraga et al., 2007), less is known about the role of vegetation identity on EPF occurrence and diversity. Recent evidence points to a divergence of this latter group from grass endophytes (Moonjely et al., 2016), suggesting that these fungi still posses some ability to live in close relation with plant hosts. Indeed, hypocrealean EPF have been shown to inhabit rhizospheres, roots, and shoots of many plant species (Hu and St. Leger, 2002; Sasan and Bidochka, 2012; Barelli et al., 2016). There is recent evidence of N transfer from infected insects to colonized plant hosts via hyphae of EPF (Behie et al., 2012), perhaps in return for C resources from the plant host (Behie et al., 2017). Beauveria spp. have also been seen to colonize roots to a greater extent in response to simulated herbivory, suggesting recruitment of these endophytes when plants are under attack by herbivores (McKinnon et al., 2018). Because of this close association with plants and their ability to infect a wide variety of insect pests, manipulation of agricultural plant communities may play an important role in regulating insect pests, decreasing the need for chemical treatment.

Groundcovers are common in many perennial agricultural systems where crop rows cover only a portion of the land area and drive rows are maintained to facilitate cultural practices and harvesting. Maintenance of vegetation in the drive row provides many well-known benefits such as erosion control, nutrient cycling, and above ground conservation biological control (Winter et al., 2018). The identity of groundcover vegetation may also be important in influencing soil microbial communities (Vukicevich et al., 2016), including naturally-occurring EPF communities (Randhawa et al., 2018) and subsequent conservation biological control of insect pests. For example, Randhawa et al. (2018) saw that EPF abundance was positively correlated with plant biomass and soil moisture. In a recent study, we observed changes in the abundance of a common EPF, Beauveria bassiana, depending on groundcover vegetation across different vineyards and seasons (Vukicevich et al., 2019). Notably, B. bassiana increased with the proportion of native plant cover at these sites. Whether these changes in EPF abundance equates to any functional differences in terms of insect mortality has yet to be seen.

The purpose of the present study was to measure the effect of groundcover vegetation on the community composition as well as the overall prevalence of naturally occurring EPF in vineyard soil. Based on previous findings in the study area (Vukicevich et al., 2019), we expected to find greater prevalence of B. bassiana in groundcovers comprised of native plant species, potentially leading to greater insect mortality. However, because there is also evidence pointing to the importance of plant biomass and soil moisture in driving EPF infectivity (Ranhawa et al., 2018), groundcovers that produce more overall plant growth, e.g. with supplemental irrigation or inclusion of legumes, may promote greater occurrence of these fungi.