Scent of death: Evolution from sea to land of an extreme collective attraction to conspecific death

Abstract

All living organisms must eventually die, though in some cases their death can bring life-giving opportunities. Few studies, however, have experimentally tested how animals capitalize on conspecific death and why this specialization would evolve. Here, we conducted experiments on the phylogenetically most closely-related marine and terrestrial hermit crabs to investigate the evolution of responses to death during the sea-to-land transition. In the sea, death of both conspecifics and heterospecifics generates unremodeled shells needed by marine hermit crabs. In contrast, on land, terrestrial hermit crabs are specialized to live in architecturally remodeled shells, and the sole opportunity to acquire these essential resources is conspecific death. We experimentally tested these different species' responsiveness to the scent of conspecific versus heterospecific death, predicting that conspecific death would have special attractive value for the terrestrial species. We found the terrestrial species was overwhelmingly attracted to conspecific death, rapidly approaching and forming social groupings around conspecific death sites that dwarfed those around heterospecific death sites. This differential responsiveness to conspecific versus heterospecific death was absent in marine species. Our results thus reveal that on land a reliance on resources associated exclusively with conspecifics has favored the evolution of an extreme collective attraction to conspecific death.

Keywords: collective behavior; death; evolutionary innovation; sea to land; shells; sociality.

Figure 1

Study species and experimental design. (a) Natural grouping of highly social terrestrial hermit crabs (Coenobita compressus), one of the study species. This land‐based species is special, in that it lives in architecturally remodeled shells, which can only be acquired after conspecifics are evicted or die. The scent of conspecific death may therefore generate extreme collective attraction. Photo by Mark Laidre. (b) Experimental design, with a capped bottle containing different chemical cues (including the scent of death) being placed on the substrate and then opened. The same setup was used both on land (with terrestrial hermit crabs, Coenobita compressus) and in the sea (with marine hermit crabs, Calcinus obscurus and Clibanarius albidigitus). The number of hermit crabs within a circular area (30 cm radius of the bottle) was counted both before the bottle was introduced (at t = 0 min) and after individuals had an opportunity to be attracted (at t = 5 min)

Figure 2

Attraction to the scent of death on land versus in the sea. Number (mean ± SEM) of (a) terrestrial hermit crabs (in the experiments on land) and (b) marine hermit crabs (in the experiments in the sea) before and after chemical cues were released. Y‐axis is scaled the same for terrestrial and marine. ***p < 0.0001 and NS = nonsignificant

Figure 3

Attraction on land to conspecific versus closely‐related heterospecific death. Number (mean ± SEM) of terrestrial hermit crabs before and after chemical cues were released indicating either the death of a closely‐related heterospecific marine hermit crab or the death of a conspecific terrestrial hermit crab. *p < 0.005