Exposure to cuticular bacteria can alter host behavior in a funnel-weaving spider

Abstract

Contact with environmental microbes are arguably the most common species interaction in which any animal participates. Studies have noted diverse relationships between hosts and resident microbes, which can have strong consequences for host development, physiology, and behavior. Many of these studies focus specifically on pathogens or beneficial microbes, while the benign microbes, of which the majority of bacteria could be described, are often ignored. Here, we explore the nature of the relationships between the grass spider Agelenopsis pennsylvanica and bacteria collected from their cuticles in situ. First, using culture-based methods, we identified a portion of the cuticular bacterial communities that are naturally associated with these spiders. Then, we topically exposed spiders to a subset of these bacterial monocultures to estimate how bacterial exposure may alter 3 host behavioral traits: boldness, aggressiveness, and activity level. We conducted these behavioral assays 3 times before and 3 times after topical application, and compared the changes observed in each trait with spiders that were exposed to a sterile control treatment. We identified 9 species of bacteria from the cuticles of 36 spiders and exposed groups of 20 spiders to 1 of 4 species of cuticular bacteria. We found that exposure to Dermacoccus nishinomiyaensis and Staphylococcus saprophyticus was associated with a 10-fold decrease in the foraging aggressiveness of spiders toward prey in their web. Since bacterial exposure did not have survival consequences for hosts, these data suggest that interactions with cuticular bacteria, even non-pathogenic bacteria, could alter host behavior.

Spiders, microbes and sex: Bacterial exposure on copulatory organs alters mating behaviour in funnel‐web spiders

“…We found no effect of exposing males to bacteria on their courtship behaviour (as has been found in other host–parasite systems: Abbot & Dill, ; McLachlan, ), perhaps because this was a topical application while female exposure was an internal application. Although similar topical applications of cuticular bacteria have been found to influence spider behaviour (Keiser, Shearer, et al, ; Keiser, Wright, et al, ; Parks et al, ), more detailed experiments are needed to illuminate the mechanistic underpinnings shaping the relationship between bacterial exposure and sexual behaviour.…”

“…However, we took precautions to adhere to the ASAB/ARRIVE Guidelines for the Use of Animals in Research to minimize unnecessary stresses or harm to the spiders. A recent study showed that a similar application of cuticular bacteria to A. pennsylvanica was not detrimental to survival (Parks et al, ).…”

“…The most common ecological interaction with which any animal is confronted is undoubtedly with the diverse milieu of microbes present in their environment (Ezenwa, Gerardo, Inouye, Medina, & Xavier, ; McFall‐Ngai et al, ). Associations with environmental microbes can affect not only host physiology and behaviour (Parks et al, ), but can also shift the outcome of interactions with predators (Ramirez & Snyder, ), competitors (Grosholz, ) and potential mates (Worden, Parker, & Pappas, ). In the context of sexual behaviour, microbes encountered via contact with mates can potentially threaten future performance.…”

“…These structures are also used during courtship in (Singer et al, 2000), and for stridulation or visual signals in other spiders (Elias, Mason, & Hoy, 2004;Fernández-Montraveta & Simó, 2006), where bacteria could be acquired from the environment and transferred into the female body cavity during sperm transfer. Environmental microbes do occur on the cuticles of A. pennsylvanica and have been shown to alter host behaviour (Parks et al, 2018). However, the degree to which exposure to environmental microbes can alter male courtship effort or female receptivity remains unknown.…”

Parasites of spiders: Their impacts on host behavior and ecology

“…Some cuticular bacteria induce weight loss, mortality, and changes to host behavior when re-applied in large quantities, as has been shown in the grass spider Agelenopsis pennsylvanica (CL Koch, 1843) (Parks et al 2018) and the social spider Stegodyphus dumicola Pocock, 1898 (Keiser et al 2016b). It is unlikely that exposure to cuticular bacteria alone can induce these changes, but none of these studies identified the route by which bacteria enter the host body after a topical application.…”