American Society of Naturalists

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“Life-history modeling reveals the ecological and evolutionary significance of autotomy”

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Masaki Hoso and Ichiro K. Shimatani (Dec 2020)

Mark-recapture study reveals how much fitness advantage is conferred by snail autotomy against snake predation

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A land snail (<i>Satsuma caliginosa caliginosa</i>) showing a regenerated foot.<br />(Credit: Masaki Hoso)
A land snail (Satsuma caliginosa caliginosa) showing a regenerated foot.
(Credit: Masaki Hoso)

When attacked, lizards drop their tails and grasshoppers release their legs. Autotomy, the self-shedding of body parts, is widespread in animals, and its survival benefit seems apparent. But it remains unknown what proportion of deaths is prevented by autotomy in nature. The authors tackled this classic and fundamental question by modeling the invisible process of prey’s life history. They applied their novel approach to a unique predator-prey system in Iriomote Island, Japan, where a land snail autotomizes and regenerates its foot in response to snake bites. Using field and laboratory data, they estimated three properties of the snail prey that have rarely or never been quantified in the wild: (1) how frequently they encountered snake predators; (2) what proportion of their mortality was attributable to snake predation; and (3) how much advantage was conferred by autotomy. Their approach is applicable to a range of predator-prey systems where unsuccessful predation attempts cause identical changes in appearance of prey animals.


Recapture of a land snail (<i>Satsuma caliginosa caliginosa</i>) showing a regenerated foot.<br />(Credit: Masaki Hoso)<br/>
Recapture of a land snail (Satsuma caliginosa caliginosa) showing a regenerated foot.
(Credit: Masaki Hoso)

Abstract

Autotomy, the self-amputation of body parts, serves as an anti-predator defense in many taxonomic groups of animals. However, its adaptive value has seldom been quantified. Here, we propose a novel modeling approach for measuring the fitness advantage conferred by the capability for autotomy in the wild. Using a predator-prey system where a land snail autotomizes and regenerates its foot specifically in response to snake bites, we conducted a laboratory behavioral experiment and a 3-year multi-event capture–mark–recapture (CMR) study. Combining these empirical data, we developed a hierarchical model and estimated the basic life history parameters of the snail. Using samples from the posterior distribution, we constructed the snail’s life table as well as that of a snail variant incapable of foot autotomy. As a result of our analyses, we estimated the monthly encounter rate with snake predators at 3.3% (95% CI: 1.6–4.9%), the contribution of snake predation to total mortality until maturity at 43.3% (15.0–95.3%), and the fitness advantage conferred by foot autotomy at 6.5% (2.7–11.5%). This study demonstrated the utility of the multi-method hierarchical modeling approach for the quantitative understanding of the ecological and evolutionary processes of anti-predator defenses in the wild. 

自切の生態学的および進化学的意義を生活史モデリングによって解き明かす

自切、すなわち身体の一部を自発的に切り離す行動は、さまざまな分類群の動物において被食防御の効果をもつことが知られている。しかし、実際にどの程度、適応度が自切によって向上しているのかは、定量的に評価されたことがほとんどない。そこで我々は、自切する能力を備えることによって向上する適応度を野外で測定する手法を開発し、現実のシステムに対して適用した。用いた動物は、ヘビからの被食に際して特異的に腹足を自切するカタツムリである。我々は、捕食行動実験の結果と3年間におよぶ標識再捕獲データを階層モデルによって統合し、カタツムリの生活史に関わるパラメーターを推定した。また、パラメーターの事後分布を用いたシミュレーションにより生命表を構築した。解析の結果、カタツムリにとってのヘビとの月間遭遇率は 3.3% (95%信用区間: 1.6–4.9%)、成熟に至るまでの死因に占めるヘビからの捕食圧は 43.3% (15.0–95.3%)、そして自切能力によって向上している適応度は 6.5% (2.7–11.5%) と推定された。この研究は、野外における被食防御の生態的および進化的過程を定量的に理解するにあたり、複数のデータを統合する階層モデルの有用性を示すものでもある。