Effects of captivity and rewilding on amphibian skin microbiomes

Kueneman, Jordan G.; Bletz, Molly C.; Becker, Matthew H.; Gratwicke, Brian; Orlando, Garcés,; Hertz, Andreas; Holden, Whitney M.; Ibáñez, Roberto; Loudon, Andrew H.; McKenzie, Valerie J.; Parfrey, Laura Wegener; Sheafor, Brandon; Rollins‐Smith, Louise A.; Richards‐Zawacki, Corinne L.; Voyles, Jamie; Woodhams, Douglas C.

doi:10.1016/j.biocon.2022.109576

Cited by 29 publications

(28 citation statements)

References 52 publications

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“…This generally matches what other studies have found that compared the skin microbiome of captive and wild individuals [16,23]. A multi-species meta-analysis recently found no consistent impact of captivity on the skin microbiome of adult amphibians, but that dataset did include some boreal toad samples which did indicate a large impact of captivity on microbial richness and phylogenetic diversity [25]. The lower alpha diversity in captive toad skin is intuitive, since their environment has signi cantly less source inoculum than wild individuals are likely exposed to.…”

Section: Effects Of Captivity On Different Body Sites and Development...supporting

confidence: 88%

“…In one study that examined multiple species, the effect of captivity was clear in all of them, and they maintained species-speci c skin microbial communities generations into their captivity [18], underscoring that captivity does not erase intrinsic, biotic factors that in uence skin microbial communities. A recent meta-analysis involving 18 amphibian species failed to nd a consistent impact of captivity on multiple microbial diversity and function metrics [25]. Data from our system, boreal toads (Anaxyrus boreas boreas), show that there are large differences in the skin microbiome between captive and wild postmetamorphic animals [16].…”

Section: Introductionmentioning

confidence: 77%

“…Translocations in deer mice (both captive to wild and wild to captive) produced gut microbial communities that resembled their cohabitants without a signature of the environment in which they were reared [41]. In the only other study to look at amphibian reintroductions, adult Atelopus varius transitioned from captivity to outdoor mesocosms acquired skin microbiomes that more closely resembled those of wild individuals than those from captivity [25]. On the other end of the spectrum, in giant pandas released into the wild, authors concluded that 2-3 months may not be long enough to establish a fully wild-type gut microbial community in captive born individuals [42].…”

Section: Implications For Conservation and Amphibian Translocationsmentioning

confidence: 99%

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Captivity, reintroductions, and the rewilding of the amphibian microbiome

Korpita

Muths²,

Watry³

et al. 2022

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Many studies have noted differences in microbes associated with animals reared in captivity compared to their wild counterparts, but few studies have examined how microbes change when animals are reintroduced to the wild after being reared in captivity. As captive assurance populations and reintroduction programs increase, a better understanding of how microbial symbionts respond during animal translocations is critical. We examined changes in microbes associated with boreal toads (Anaxyrus boreas boreas), a threatened amphibian, after reintroduction to the wild following captive rearing. Previous studies demonstrate that developmental life stage is an important factor in amphibian microbiomes. We collected 16S marker-gene sequencing datasets to investigate: i) comparisons of the skin, mouth, and fecal bacteria of boreal toads across four developmental life stages in captivity and the wild, ii) tadpole skin bacteria before and after reintroduction to the wild, and iii) adult skin bacteria during reintroduction to the wild. We demonstrated that differences occur across skin, fecal, and mouth microbial communities in captive versus wild boreal toads, and that the degree of difference depends on developmental stage. Skin bacterial communities from captive tadpoles were more similar to their wild counterparts than captive post-metamorphic individuals were to their wild counterparts. When captive-reared tadpoles were introduced to a wild site, their skin bacteria changed rapidly to mirror wild tadpoles. Similarly, the microbiome of reintroduced adult boreal toads also shifted to mirror that of wild toads. Our results indicate that the microbial signature of captivity in amphibians does not persist after release into natural habitat.

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Section: Effects Of Captivity On Different Body Sites and Development...supporting

confidence: 88%

Section: Introductionmentioning

confidence: 77%

Section: Implications For Conservation and Amphibian Translocationsmentioning

confidence: 99%

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Captivity, reintroductions, and the rewilding of the amphibian microbiome

Korpita

Muths²,

Watry³

et al. 2022

Preprint

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“…As found in studies of other amphibians ( Kueneman et al, 2022 ), captivity affected the cane toad skin bacteria. Only small sample sizes of captive parental toads were available at the time of sampling, limiting our statistical power and the extent to which we can interpret results from parental toads’ communities.…”

Section: Discussionsupporting

confidence: 64%

“…A focus on heritable differences in microbiome assembly removes priority effects from the varied histories of wild-caught individuals. We expected to find both an ancestral population-level signal (reflecting host traits) and a unique signature in captive toads regardless of their geographic origin, due to conditions in captivity ( Kueneman et al, 2022 ).…”

Section: Introductionmentioning

confidence: 99%

Geographic variation in bacterial assemblages on cane toad skin is influenced more by local environments than by evolved changes in host traits

et al. 2023

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Bacterial assemblages on amphibian skin may play an important role in protecting hosts against infection. In hosts that occur over a range of environments, geographic variation in composition of bacterial assemblages might be due to direct effects of local factors and/or to evolved characteristics of the host. Invasive cane toads (Rhinella marina) are an ideal candidate to evaluate environmental and genetic mechanisms, because toads have evolved major shifts in physiology, morphology, and behavior during their brief history in Australia. We used samples from free-ranging toads to quantify site-level differences in bacterial assemblages and a common-garden experiment to see if those differences disappeared when toads were raised under standardised conditions at one site. The large differences in bacterial communities on toads from different regions were not seen in offspring raised in a common environment. Relaxing bacterial clustering to operational taxonomic units in place of amplicon sequence variants likewise revealed high similarity among bacterial assemblages on toads in the common-garden study, and with free-ranging toads captured nearby. Thus, the marked geographic divergence in bacterial assemblages on wild-caught cane toads across their Australian invasion appears to result primarily from local environmental effects rather than evolved shifts in the host.

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