Not all rotten fish stink: Microbial changes in decaying carcasses increase cytotoxicity and potential risks to animal scavengers

Abstract

Dead animal bodies occur naturally in ecosystems, are regularly washed up along ocean beaches, and are a key component of many coastal food webs where scavenging animals consume carcasses. Microbes that decompose carcasses can, however, produce toxic chemicals during putrefaction. This is frequently assumed to have negative consequences for scavengers in the wild, but has been rarely quantified. In this study, we measured how changes in the microbial assemblages of decaying fish affect the toxicity of carcasses. We did this by allowing fish carcasses to decompose in the field for up to 31 days in the dunes of a sandy beach; an ecosystem where scavenging animals are common. Carcasses were sampled daily and the tissues tested for changes in culturable microbial communities using 100 μL samples of whole carcass homogenates on marine and sheep blood agar, and changes in cytotoxicity using Vero cell assays. Cytotoxicity peaked 11 days after deployment showing 95% rounded and detached cells. Cytotoxicity was lower in the early phases of decay as microbial communities developed and after approximately two weeks when carcasses dried. The peak in toxicity correlated with peaks in the abundance of Acinetobacter, and Vibrio and Alivibrio; microbes known to produce toxins. This trajectory of toxicity suggests an ecological model where microbes may predictably determine the palatability of carrion in food webs, making both fresh and aged carcasses the least risky proposition for scavenging animals. This ‘fresh and aged carcasses are best’ model is highly amenable to testing in the context of carrion-centred food webs in multiple systems, and it has practical applications in conservation where animal carcasses are provided to threatened, and often iconic, scavenger species.