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

Blandford, Makeely I.; Katouli, Mohammad; Gilby, Ben L.; O'Dea, Christian; Olds, Andrew D.; Schlacher, Thomas A.

doi:10.1016/j.ecss.2019.106350

Cited by 13 publications

(10 citation statements)

References 42 publications

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“…These complex interactions among microbes and scavenging fauna, along with abiotic factors (e.g., precipitation and temperature), often impact the duration and occurrence of the previously described stages (Carter, Yellowlees & Tibbett, 2008;Carter, Yellowlees & Tibbett, 2010;Comstock et al, 2015;Galloway, Jones & Parks, 1989;Payne, 1965;Rozen, Engelmoer & Smiseth, 2008;Shukla et al, 2017). For example, some microbes that begin to metabolize the carrion soft tissue after an animal's death also produce toxins in order to hinder consumption from other organisms (Blandford et al, 2019;Burkepile et al, 2006;Janzen, 1977). In response, some scavengers, such as the turkey vulture (Cathartes aura), have developed an unusually high tolerance to decomposer-produced toxins (e.g., botulinum toxin), and the highly acidic conditions present in their hindgut reduce the likelihood of microbes surviving consumption and infecting the vulture itself (Beasley, Olson & DeVault, 2015;DeVault Jr, Rhodes & Shivik, 2003;Roggenbuck et al, 2014).…”

Section: Introductionmentioning

confidence: 99%

“…Research into the interactions between animal scavengers and microbes have typically focused on scavenger avoidance of microbe-laden carrion (Blandford et al, 2019;Burkepile et al, 2006). It has long been suggested that scavengers may facilitate the spread of pathogens throughout an ecosystem (Houston & Cooper, 1975), but scavengers' involvement in disease ecology is complex and requires further study (Beasley, Olson & DeVault, 2015).…”

Section: Introductionmentioning

confidence: 99%

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Succession of bacterial communities on carrion is independent of vertebrate scavengers

Dangerfield

Frehner

Buechley

et al. 2020

PeerJ

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The decomposition of carrion is carried out by a suite of macro- and micro-organisms who interact with each other in a variety of ecological contexts. The ultimate result of carrion decomposition is the recycling of carbon and nutrients from the carrion back into the ecosystem. Exploring these ecological interactions among animals and microbes is a critical aspect of understanding the nutrient cycling of an ecosystem. Here we investigate the potential impacts that vertebrate scavenging may have on the microbial community of carrion. In this study, we placed seven juvenile domestic cow carcasses in the Grassy Mountain region of Utah, USA and collected tissue samples at periodic intervals. Using high-depth environmental sequencing of the 16S rRNA gene and camera trap data, we documented the microbial community shifts associated with decomposition and with vertebrate scavenger visitation. The remarkable scarcity of animals at our study site enabled us to examine natural carrion decomposition in the near absence of animal scavengers. Our results indicate that the microbial communities of carcasses that experienced large amounts of scavenging activity were not significantly different than those carcasses that observed very little scavenging activity. Rather, the microbial community shifts reflected changes in the stage of decomposition similar to other studies documenting the successional changes of carrion microbial communities. Our study suggests that microbial community succession on carrion follows consistent patterns that are largely unaffected by vertebrate scavenging.

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Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Succession of bacterial communities on carrion is independent of vertebrate scavengers

Dangerfield

Frehner

Buechley

et al. 2020

PeerJ

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“…It is likely that carcasses in our mesocosm setting broke down slower than carcasses in natural systems, as we observed few carcasses remaining between weekly surveys of post-spawn carcasses in regional streams (Dunkle et al 2020), which could be related to hydraulic conditions (e.g., greater velocity), different macroinvertebrate communities, and/or the presence of scavengers (e.g., raccoons or crayfish) in natural streams. Another possibility is bacteria and other microbes successfully colonized and defended carcasses in the mesocosms using secondary compounds, a phenomenon reported for marine mammal carrion (Dayton et al 2019) and coastal marine fish carcasses (Blandford et al 2019). Further research is needed to elucidate the role of carcass traits such as integument toughness, palatability, and epimicrobiomes in trophic resource processing in both controlled and natural settings.…”

Section: Discussionmentioning

confidence: 94%

Fish carcasses alter subyearling Chinook salmon dispersal behavior and density but not growth in experimental mesocosms

2021

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Similar to many fish, juvenile Pacific salmon rearing in temperate streams face a growth and survival bottleneck early in their first summer due to limitations in space and food. Fish carcasses have been shown to affect juvenile salmon growth in many systems, but carcasses likely also alter behavioral and dispersal response of hatchery-origin young-of-the-year salmon. We tested the social and emigration response of subyearling chinook salmon to carcasses of Pacific lamprey or rainbow trout using semi-open flow-through mesocosm experiments. We expected the presence of carcasses to increase salmon growth and density while decreasing intraspecific aggression and downstream emigration compared to controls without carcasses. Consistent with expectations, salmon emigrated at lower rates when carcasses were present, resulting in significantly higher holding densities. Contrary to our expectations and results from previous studies, we did not detect differences in growth rate of juvenile salmon among treatments. Our findings suggest that indirect responses of consumers to concentrated resources may have measurable effects on density mediated by movement behaviors. Differences in lamprey and trout decomposition also suggest that carcass traits mediate the behavioral responses of consumers and incorporation of carcass subsidies into food webs.

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“…Yet tigers, as well as other large size felids, do not consume the gastrointestinal contents of their prey (e.g., Delibes et al, 2011; Labisky & Boulay, 1998; Schaller, 1967; Stahler et al, 2006; Sunquist, 1981; Vucetich et al, 2012). This part of the carcasses certainly contains toxic substances, and it is not well known whether predators would ‘behaviorally avoid the consumption of maggots or different parts of a carrion to the effects of toxins’ (Blandford et al, 2019, p. 6). However, Carnivora, which consume small‐sized prey (e.g., mice) as a whole therefore come into contact with toxins (e.g., plant material from gut and stomach), which justified their assignment to a ‘low’ score, instead of a total absence of toxin in their diet.…”

Section: Resultsmentioning

confidence: 99%

Reconstruction of evolutionary changes in fat and toxin consumption reveals associations with gene losses in mammals: A case study for the lipase inhibitor PNLIPRP1 and the xenobiotic receptor NR1I3

Wagner

Ruf

Lehmann

et al. 2022

J of Evolutionary Biology

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The inactivation of ancestral protein-coding genes (gene loss) can be associated with phenotypic modifications. Within placental mammals, repeated losses of PNLIPRP1 (gene inhibiting fat digestion) occurred preferentially in strictly herbivorous species, whereas repeated NR1I3 losses (gene involved in detoxification) occurred preferentially in strictly carnivorous species. It was hypothesized that lower fat contents of herbivorous diets and lower toxin contents of carnivorous diets cause relaxed selection pressure on these genes, resulting in the accumulation of mutations and ultimately to convergent gene losses. However, because herbivorous and carnivorous diets differ vastly in their composition, a fine-grained analysis is required for hypothesis testing.We generated a trait matrix recording diet and semi-quantitative estimates of fat and toxin consumption for 52 placental species. By including data from 31 fossil taxa, we reconstructed the ancestral diets in major lineages (grundplan reconstruction). We found support that PNLIPRP1 loss is primarily associated with low levels of fat intake

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

Cited by 13 publications

References 42 publications

Succession of bacterial communities on carrion is independent of vertebrate scavengers

Succession of bacterial communities on carrion is independent of vertebrate scavengers

Fish carcasses alter subyearling Chinook salmon dispersal behavior and density but not growth in experimental mesocosms

Reconstruction of evolutionary changes in fat and toxin consumption reveals associations with gene losses in mammals: A case study for the lipase inhibitor PNLIPRP1 and the xenobiotic receptor NR1I3

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