Cuticular bacteria appear detrimental to social spiders in mixed but not monoculture exposure

Abstract

Much of an animal's health status, life history, and behavior are dictated by interactions with its endogenous and exogenous bacterial communities. Unfortunately, interactions between hosts and members of their resident bacterial community are often ignored in animal behavior and behavioral ecology. Here, we aim to identify the nature of host-microbe interactions in a nonmodel organism, the African social spider Stegodyphus dumicola. We collected and identified bacteria from the cuticles of spiders in situ and then exposed spiders to bacterial monocultures cultures via topical application or injection. We also topically inoculated spiders with a concomitant "cocktail" of bacteria and measured the behavior of spiders daily for 24 days after inoculation. Lastly, we collected and identified bacteria from the cuticles of prey items in the capture webs of spiders, and then fed spiders domestic crickets which had been injected with these bacteria. We also injected 1 species of prey-borne bacteria into the hemolymph of spiders. Only Bacillus thuringiensis caused increased mortality when injected into the hemolymph of spiders, whereas no bacterial monocultures caused increased mortality when applied topically, relative to control solutions. However, a bacterial cocktail of cuticular bacteria caused weight loss and mortality when applied topically, yet did not detectibly alter spider behavior. Consuming prey injected with prey-borne bacteria was associated with an elongated lifespan in spiders. Thus, indirect evidence from multiple experiments suggests that the effects of these bacteria on spider survivorship appear contingent on their mode of colonization and whether they are applied in monoculture or within a mixed cocktail. We urge that follow-up studies should test these host-microbe interactions across different social contexts to determine the role that microbes play in colony performance.

Keywords: cuticular bacteria; Stegodyphus dumicola; sickness behavior; social spider.

Figure 1.

Spiders that were injected with 2 μl of a B. thuringiensis liquid culture had increased mortality relative to spiders that were inoculated with any other monoculture or a control injection of phosphate buffered saline. Median time to death for spiders injected with B. thuringiensis was 7 days, compared to 38.5 days for M. oxydans; 14 days for Arthrobacter sp., and 17.5 days for the control spiders.

Figure 2.

Spiders that were inoculated topically with a cocktail of 3 cuticular bacterial species collected from the cuticles of spiders in situ (B. thuringiensis + M. oxydans + Pantoea sp.) had increased mortality relative to spiders that had been inoculated with LB broth alone. The median time until death for spiders inoculated with the bacterial cocktail was 73% sooner than that of control spiders.

Figure 3.

Spiders that ate crickets that had been injected with 5 μl of a cocktail containing 3 bacterial species collected from the cuticles of prey items in situ (Planomicrobium sp. + Kocuria sp. + Arthrobacter sp.) lived twice as long, on average, compared to spiders that ate control crickets injected with LB broth. Median time to death for spiders that ate bacteria-treated crickets was 11 days compared to 5 days for the control spiders.