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Steibl and Laforsch BMC Ecol (2020) 20:1 https://doi.org/10.1186/s12898-019-0268-2 BMC Ecology RESEARCH ARTICLE Open Access Shell resource partitioning as a mechanism of coexistence in two co-occurring terrestrial hermit crab species Sebastian Steibl and Christian Laforsch* Abstract Background: Coexistence is enabled by ecological diferentiation of the co-occurring species. One possible mecha- nism thereby is resource partitioning, where each species utilizes a distinct subset of the most limited resource. This resource partitioning is difcult to investigate using empirical research in nature, as only few species are primarily limited by solely one resource, rather than a combination of multiple factors. One exception are the shell-dwelling hermit crabs, which are known to be limited under natural conditions and in suitable habitats primarily by the avail- ability of gastropod shells. In the present study, we used two co-occurring terrestrial hermit crab species, Coenobita rugosus and C. perlatus, to investigate how resource partitioning is realized in nature and whether it could be a driver of coexistence. Results: Field sampling of eleven separated hermit crab populations showed that the two co-occurring hermit crab species inhabit the same beach habitat but utilize a distinct subset of the shell resource. Preference experiments and principal component analysis of the shell morphometric data thereby revealed that the observed utilization patterns arise out of diferent intrinsic preferences towards two distinct shell shapes. While C. rugosus displayed a preference towards a short and globose shell morphology, C. perlatus showed preferences towards an elongated shell morphol- ogy with narrow aperture. Conclusion: The two terrestrial hermit crab species occur in the same habitat but have evolved diferent preferences towards distinct subsets of the limiting shell resource. Resource partitioning might therefore be the main driver of their ecological diferentiation, which ultimately allowed these co-occurring species to coexist in their environment. As the preferred shell morphology of C. rugosus maximizes reproductive output at the expense of protection, while the preferred shell morphology of C. perlatus maximizes protection against predation at the expense of reproductive output, shell resource partitioning might refect diferent strategies to respond to the same set of selective pressures occurring in beach habitats. This work ofers empirical support for the competitive exclusion principle-hypothesis and demonstrates that hermit crabs are an ideal model organism to investigate resource partitioning in natural populations. Keywords: Coenobita perlatus, Coenobita rugosus, Coexistence, Competitive exclusion principle, Shell utilization, Resource partitioning Background Troughout all ecosystems, species can be found that are closely related to each other, occupy the same trophic level within the food web and share the same habitat, thus fulflling similar ecological roles for the ecosystem [1]. *Correspondence: [email protected] When two or more species overlap to a certain degree in Department Animal Ecology I, University of Bayreuth and BayCEER, their biology and share a common and essential resource Universitaetsstr. 30, 95440 Bayreuth, Germany © The Author(s) 2020. This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creat iveco mmons .org/licen ses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/ publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Steibl and Laforsch BMC Ecol (2020) 20:1 Page 2 of 9 that is limited in supply, these species experience compe- competition, as the utilization of an empty shell makes it tition [2, 3]. Tis interspecifc competition can occur in unavailable for other individuals [11, 13, 14, 21–23]. Tis two forms, either via direct interference competition (i.e. competition can force hermit crabs to utilize shells out- fghting over resources) or via indirect exploitative com- side their optimal ft range, resulting in a reduced ftness petition (i.e. consumption of resources by one species [10, 20, 24]. A number of studies, however, were able to makes it unavailable for second species). In ecological demonstrate, that, contrary to the proposed shell com- research, evidence for competition between two species petition, at least some co-occurring hermit crab species can be provided by comparing which resources are used partition the shell resource [10, 25–27]. In these stud- and which are intrinsically preferred [4]. ies, the utilized gastropod shells and their morphomet- When investigating resource utilization between co- ric parameters (e.g. size, weight) of co-occurring hermit occurring species, studies have shown that some animals crab species in the feld were investigated and compared. that presumably compete over the same resource, actu- It was thereby shown that co-occurring hermit crabs uti- ally partition the resource [5, 6]. According to the com- lize indeed shells of diferent gastropod species or with petitive exclusion principle, this resource partitioning, diferent shell parameters [8, 25], although other studies as a form of ecological diferentiation between species, suggested that the observed diferences in shell utiliza- can thereby be the mechanism that allows co-occurring tion arise not out of diferent preferences [11, 21]. Tere- species to coexist in the same environment [7]. Tis fore, it is discussed whether shell resource partitioning coexistence can only be realized when each species uses is indeed the mechanism of coexistence in co-occurring a discrete subset of the limiting resource, which difers hermit crab species [10, 23]. qualitatively from those of the co-occurring species [8, One major limitation of many research approaches that 9]. Tis premise for resource partitioning is described in investigate shell resource partitioning in hermit crabs is the concept of limiting similarity, which states that there that the proposed preferences are based on the species needs to be a limit to how similar two species can be to identities of the gastropod shells [e.g. 20, 26]. Te utili- each other in order to stably coexist, rather than compete zation of diferent shell species depends on the gastro- [5]. pod communities in the particular habitat and gastropod Such theoretical hypotheses are difcult to test using species vary between diferent regions [19, 24, 28, 29]. empirical research, as most animals in nature are not lim- Proposing that co-occurring hermit crab species parti- ited by only a single resource, but rather by a multitude tion the shell resource by preferring diferent shell spe- of abiotic and biotic factors [10]. Tere exist, however, cies is an uninformative and not universally applicable some co-occurring species, where enough evidence has approach, because the available set of utilizable gastro- been collected to suggest that they are indeed primarily pod species varies between regions and does not refect limited by only one resource. Shell-dwelling hermit crabs the actual preference of a hermit crab species, i.e. the are limited under natural conditions and in suitable habi- same hermit crab species can prefer two completely dif- tats only by the availability of the shell resource, while ferent shell species in two diferent populations but food and habitat are not considered as a limiting fac- in both cases select for the same morphological shell tor [10–13]. Terefore, they appear to be suitable model parameters. organisms to investigate competition theory in empirical A better approach is the comparison of preferences for research. diferent shell parameters. Determining the shell par- Hermit crabs (Superfamily: Paguroidea) are charac- titioning mechanism based on single shell parameters, terized by an uncalcifed and reduced abdomen, which however, is restricted, as the various shell variables are they protect by utilizing mainly gastropod shells [14, 15]. all highly intercorrelated, making it impossible to char- As a well-ftting shell optimizes growth and maximizes acterize a single parameter on which preferences could clutch size [16], ofers protection against predators and be based upon [30]. Using morphometric data, it was mechanical disruption [17, 18], and decreases the risk of demonstrated that co-occurring hermit crab species have desiccation in the intertidal and terrestrial species [19], distinct preferences towards e.g. large shells or narrow hermit crabs are under constant pressure to fnd a well- apertures [25]. ftting shell. Te availability of empty and well-ftting To deepen our understanding of resource partition- shells thereby depends on the gastropod population and ing as a possible driver of coexistence using empirical their mortality and hence is the limiting resource of her- research on hermit crabs, it would be essential to incor- mit crab populations [10, 14, 20]. porate (I) a large-scale sampling efort to pool data of Co-occurring species of hermit crabs experience multiple distinct hermit crab and gastropod populations, direct interference competition by fghting over shells (II) a comparison between shell utilization patterns in in a highly

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