Higher parasitic load was detected in the spiders in ginger
Entomopathogenic fungus and hymenopteran taxa were detected in spiders collected from both ginger and native forest (Figure 8). While these reads likely originate from parasitized prey rather than parasitized spiders, the high incidence of parasitism within arthropod taxa across both ginger and native forest, but especially in ginger, is apparent. This is yet another benefit of high throughput sequencing approaches; not only can prey communities be detected, but parasites of prey themselves may be detected, supported in other studies (Traugott & Symondson 2008).
We can identify some well-known lepidopteran parasitoids that have been accidentally or purposefully introduced, including Cotesia vestalis , Ichneumon xanthorius , Meteorus laphygmae , and the scale parasite Aphytis chrysomphali ; these parasitoids are found in both native forest and ginger-invaded sites. The major hymenopteran parasitoids were braconids, in particularMicroctonus (Rhopalophorus ) which is a well-known adventive species across the islands (Nishida 2002) and appears to parasitize beetles, notably chrysomelids (Beardsley 1961). Infiltration of native forest by nonnative parasitoids, in particular parasitoids of Lepidoptera, has been well documented (Henneman & Memmott 2001). Their prevalence in spiders from native forest, then, is not surprising. However, we do show that the overall prevalence of Hymenoptera was higher in ginger-invaded sites than native sites. A wasp, in the non-native family Pteromalidae (Beardsley 1961; Nishida 2002) was found exclusively on ginger; Pteromalidae are mostly parasitoids of Lepidoptera and Coleoptera, but can also attack larvae and pupae of Diptera and the eggs of Coccidae. Spiders from the ginger-invaded sites also showed a higher diversity of other parasitoids, includingOrasema sp., in which the one species known from Hawaii is a parasite of another invasive species in Hawaii, the little fire ant (Heraty et al. 2021).
Entomopathogenic fungal reads were detected predominantly using 28s; while not the most widely used marker for fungal DBA barcoding, 28s has been shown to be relatively effective (Xu 2016; Zhao et al.2011). For the sequences detected in the spiders in our study, their high percent identity matches and known presence on Hawaii provides more support for our finding. Entomopathogenic fungi were detected in 22 spiders in ginger sites while only found in 1 spider from native forest. This result is consistent with previous work in New Zealand which has shown that fungivores are much more abundant in sites that have been invaded by ginger (Bassett 2014). The entomopathogenic fungiGibellula, the most common spider fungal pathogen (Shresthaet al. 2019), was detected in only one spider in native forest.Beauveria was the most commonly detected fungi in spiders from ginger-invaded sites, followed by Ophiocordyceps , a known parasite of beetle larvae (Wang et al. 2021). Beauveria is genus of cosmopolitan fungal pathogens, found associated with arthropods and the surrounding habitat, including in the soil and on vegetation. It has a wide host range over 17 arthropod orders which includes spiders (Shrestha et al. 2019; Zimmermann 2007), although infections have been seldomly documented (Meyling & Eilenberg 2007). In Hawai‘i,B. bassiana is used as a component of integrated pest management strategies in coffee plantations to control the coffee berry borer (Hypothenemus hampei ) first detected in Hawai‘i in 2014 (Grecoet al. 2018; Hollingsworth et al. 2020). Multiple indigenous strains of B. bassiana are now found in Hawai‘i and detected in crops where there were no previous mycoinsecticide treatment (Castrillo et al. 2020; Hollingsworth et al. 2011).
While we cannot comment on the particular strain or on the arthropod host with which Beauveria was carried, its prevalence, along with presence of other parasites, demonstrates a higher parasitic load found in the arthropods from ginger sites. Because entomopathogenic strains such as Beauveria and Ophiocordyceps are known to infect spiders, interaction with infected prey may then increase the risk of infection of the spider itself, unlike prey infected by hymenopteran parasitoids. Additionally, parasitism can impart indirect effects by altering prey density or prey behavior. The higher detection of parasites, then, supports that ginger-invaded habitat may produce suboptimal habitat for native arthropods by introducing new biotic interactions with potentially harmful taxa.