Abstract
Gastropod shells play an important role in the life story of hermit crabs, influencing biological characteristics directly. The adequacy of shells for hermit crabs can be evaluated through the Shell Adequacy Index, which calculates the shell's ideal size/weight compared to the actual dimensions of the occupied shells. To avoid competition for shells, animals can display a variety of strategies including alterations in their circadian rhythms. This study aimed to evaluate if two sympatric species of hermit crabs—Pagurus brevidactylus and Pagurus criniticornis—are competing for the best fitting shells and if they present differences in their circadian rhythms. Their shells were identified and measured regarding the aperture length and width. The shell adequacy was calculated using linear models of the Shell Aperture Length and Width, and the period of activity of the animals was filmed for 24 h and later analyzed. The period between 10 am and 2 pm represented daytime, while 10 pm to 2 am represented nighttime. Pagurus brevidactylus occupied mainly Cerithium atratum and Claremontiella nodulosa shells, while P. criniticornis occupied mainly C. atratum shells. Our results showed that the two species are inhabiting shells with similar traits, which may indicate competition. The species do not present distinct activity periods; however, the shell occupation pattern suggests a competition at the functional level.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data availability
Data can be made available upon request.
References
Abrams PA (1980) Resource partitioning and interspecific competition in a tropical hermit crab community. Oecologia 46:365–379
Abrams P (1981) Shell fighting and competition between two hermit crab species in Panama. Oecologia 51:84–90
Alcaraz G, Kruesi K (2009) The role of previous shell occupancy in the wild on laboratory shell choice by the hermit crab Calcinus californiensis. Mar Freshw Behav Phy 42:55–62. https://doi.org/10.1080/10236240802663564
Alcaraz G, Toledo B, Burciaga LM (2020) The energetic costs of living in the surf and impacts of zonation of shells occupied by hermit crabs. J Exp Biol. https://doi.org/10.1242/jeb.222703
Angel JE (2000) Effects of shell fit on the biology of the hermit crab Pagurus longicarpus (Say). J Exp Mar Biol Ecol 243:169–184. https://doi.org/10.1016/S0022-0981(99)00119-7
Benedetti-Cecchi L, Trussell GC (2013) Intertidal rocky shores. In: Bertness MD, Bruno JF, Silliman BR, Stachowicz JJ (eds) Marine Community Ecology and Conservation. Sinauer Associates, pp 202–225
Bertness MD (1980) Shell preference and utilization patterns in littoral hermit crabs of the bay of Panama. J Exp Mar Biol Ecol 48:1–16. https://doi.org/10.1016/0022-0981(80)90002-7
Bertness MD (1981a) Pattern and plasticity in tropical hermit crab growth and reproduction. Am Nat 117:754–773
Bertness MD (1981b) Competitive dynamics of a tropical hermit crab assemblage. Ecology 62:751–761. https://doi.org/10.2307/1937743
Bertness MD (1981) Interference, exploitation, and sexual components of competition in a tropical hermit crab assemblage. J Exp Mar Biol Ecol 49:189–202. https://doi.org/10.1016/0022-0981(81)90070-8
Blamey KL, Branch GM (2009) Habitat diversity relative to wave action on rocky shores: implications for the selection of marine protected areas. Ann Zool Fenn 19:645–657. https://doi.org/10.1002/aqc.1014
Bollay M (1964) Distribution and utilization of gastropod shells by the hermit crabs. Veliger 6:71–76
Buckley WJ, Ebersole JP (1994) Symbiotic organisms increase the vulnerability of a hermit crab to predation. J Exp Mar Biol Ecol 182:49–64. https://doi.org/10.1016/0022-0981(94)90210-0
Carlon DB, Ebersole JP (1995) Life-history variation among 3 temperate hermit-crabs - the importance of size in reproductive strategies. Biol Bull 188:329–337
Collins PA (2005) A coexistence mechanism for two freshwater prawns in the Paraná River floodplain, Argentina. J Crustacean Biol 25:219–225. https://doi.org/10.1651/C-2528
da Silva AR, Galli GM, Stanski G, De BB, Davanso TM, Cobo VJ, Castilho AL (2018) Shell occupation as a limiting factor for Pagurus brevidactylus (Stimpson, 1859) in the Marine State Park of Laje de Santos, Brazil. Invertebr Reprod Dev 63:1–10. https://doi.org/10.1080/07924259.2018.1513087
da Silva AR, Rodrigues GFB, Lima D, Cobo VJ, Costa RC, Castilho AL (2020) The hermit crab-shell relationship through the lens of interaction networks: the use of network metrics and species role across communities. Austral Ecol 45:896–908. https://doi.org/10.1111/aec.12903
da Silva AR, Rodrigues GFB, Borthagaray AI, Costa RC, Castilho AL (2021) Morphometric traits as drivers for module structures and species specialization: a study about the hermit crab-gastropod networks from three different regions on the Brazilian coast. J Zool 316:1–10. https://doi.org/10.1111/jzo.12935
da Silva AR, Rodrigues GFB, Paluski GB, Vieira NR, Gregati RA (2022) Downscaling hermit crab-gastropod network to demographic groups unveils recurrent patterns. Ethol Ecol Evol. https://doi.org/10.1080/03949370.2021.1989052
Drzewina A (1906) Les variations periodiques du signe du photoroopisme chez les Pagures misanthropes. C R Acad Sci 145:1208–1209
Floeter SR, Nalesso RC, Rodrigues MMP, Turra A (2000) Patterns of shell utilization and selection in two sympatric hermit crabs (Anomura: Diogenidae) in sout-eastern Brazil. J Mar Biol Assoc UK 80:1053–1059. https://doi.org/10.1017/S0025315400003118
Gherardi F, Nardone F (1997) The question of coexistence in hermit crabs: population ecology of a tropical intertidal assemblage. Crustaceana 70:608–629
Gherardi F, Vannini M (1992) Hermit crabs in a mangrove swamp: clustering dynamics in Clibanarius laevimanus. Mar Beh Physiol 21:85–104
Goldstein JS, Dubofsky EA, Spanier E (2015) Into a rhythm: diel activity patterns and behaviour in Mediterranean slipper lobsters, Scillarides latus. ICES J Mar Sci 72:147–154. https://doi.org/10.1093/icesjms/fsv008
Gorman D, Barros F, Turra A (2015) What motivates hermit crabs to abandon trapped shells? Assessing the influence of shell value, olfactory attractants, and previous experience. Hydrobiologia 743:285–297. https://doi.org/10.1007/s10750-014-2047-6
Gregati RA, Fransozo V, López-Greco LS, Negreiros-Fransozo ML (2010) Reproductive cycle and ovarian development of the marine ornamental shrimp Stenopus hispidus in captivity. Aquaculture 306:185–190. https://doi.org/10.1016/j.aquaculture.2010.05.009
Holdridge EM, Cuellar-Gempeler C, terHorst CP (2016) A shift from exploitation to interference competition with increasing density affects population and community dynamics. Ecol Evol 15:5333–5341. https://doi.org/10.1002/ece3.2284
Imazu M, Asakura A (1994) Distribution, reproduction and shell utilization patterns in three species of intertidal hermit crabs on a rocky shore on the Pacific coast of Japan. J Exp Mar Biol Ecol 184:41–65. https://doi.org/10.1016/0022-0981(94)90165-1
Iossi CL, Biagi R, Mantelatto FL (2005) Egg production and shell relationship of the hermit crab Pagurus brevidactylus (Anomura: Paguridae) from southern Brazil. Anim Biol 55:111–121. https://doi.org/10.1163/1570756053993479
Kellogg CW (1976) Gastropod shells: a potentially limiting resource for hermit crabs. J Exp Mar Biol Ecol 22:101–111. https://doi.org/10.1016/0022-0981(76)90112-X
Kellogg CW (1977) Coexistence in a hermit crab species ensemble. Biol Bull 153:133–144
Lane SM, Briffa M (2020) The role of spatial accuracy and precision in hermit crab contests. Anim Behav. https://doi.org/10.1016/j.anbehav.2020.07.013
Lane SM, Cornwell TO, Briffa M (2022) The angle of attack : rapping technique predicts skill in hermit crab contests. Anim Behav 187:55–61. https://doi.org/10.1016/j.anbehav.2022.02.017
Leite FPPP, TurraGandolfi ASMM (1998) Hermit crabs (Crustacea: Decapoda: Anomura), gastropod shells and environmental structure: their relationship in southeastern Brazil. J Nat Hist 32:1599–1608. https://doi.org/10.1080/00222939800771131
Lima DJM, Cobo VJ, Aquino MAB, Fransozo A (2014) The population structure of two sympatric hermit-crab species on a subtidal rocky shore of an island in southeastern Brazil. An Acad Bras Cienc 86:1769–1782. https://doi.org/10.1590/0001-3765201420130472
Lunt J, Reustle J, Smee DL (2017) Wave energy and flow reduce the abundance and size of benthic species on oyster reefs. Mar Ecol Prog Ser 56:25–36. https://doi.org/10.3354/meps12075
Mantelatto FL, Meireles AL (2004) The importance of shell occupation and shell availability in the hermit crab Pagurus brevidactylus (Stimpson, 1859) (Paguridae) population from the Southern Atlantic. B Mar Sci 75:27–35
Mantelatto FL, Faria FCR, Iossi CL, Biagi R (2007) Population and reproductive features of the western Atlantic hermit crab Pagurus criniticornis (Anomura, Paguridae) from Anchieta Island, southeastern Brazil. Iheringia Ser Zool 97:314–320. https://doi.org/10.1590/S0073-47212007000300016
Mantelatto FL, Faria FCR, Biagi R, Meireles AL (2016) An integrative approach: using field and laboratory data to characterize shell utilization and selection pattern by the hermit crab Pagurus criniticornis (Paguridae) from Anchieta Island. Brazil. Nauplius 24:e2016011. https://doi.org/10.1590/2358-2936e2016011
Mclaughlin PA (1975) On the identity of Pagurus brevidactylus (Stimpson) (Decapoda: Paguridae), with the description of a new species of Pagurus from the western atlantic. B Mar Sci 25:359–376
Meireles AL, Mantelatto FL (2005) Shell use by the Pagurus brevidactylus (Anomura, Paguridae): a comparison between laboratory and field conditions. Acta Zool Sinica 51:813–820
Meireles AL, Biagi R, Mantelatto FL (2008) Influence of prior experience on shell selection by the white spotwrist hermit crab Pagurus criniticornis (Crustacea: Paguridae). Hydrobiologia 605:259–263. https://doi.org/10.1007/s10750-008-9305-4
Melo GAS (1999) Manual de identificação dos Crustacea Decapoda do litoral brasileiro: Anomura, Thalassinidea, Palinuridea, Astacidea. São Paulo.
Nucci PR, Melo GAS (2015) Hermit crabs from Brazil: Family Diogenidae (Crustacea: Decapoda: Paguroidea), except Paguristes. Zootaxa 3947:327–346. https://doi.org/10.11646/zootaxa.3947.3.2
Nucci P, Melo GAS (2011) Hermit crabs from Brazil family paguridae (crustacea: decapoda: paguroidea) except pagurus. Zootaxa 3104:26–41. https://doi.org/10.11646/ZOOTAXA.3104.1.2
Osorno JL, Fernández-Casillas L, Rodríguez-Juárez C (1998) Are hermit crabs looking for light and large shells?: Evidence from natural and field induced shell exchanges. J Exp Mar Biol Ecol 222:163–173. https://doi.org/10.1016/S0022-0981(97)00155-X
Osorno JL, Contreras-Garduño J, Macías-Garcia C (2005) Long-term costs of using heavy shells in terrestrial hermit crabs (Coenobita compressus) and the limits of shell preference: An experimental study. J Zool 266:377–383. https://doi.org/10.1017/S0952836905007028
Palmer JD (1971) Comparative studies of circadian locomotory rhythms in four species of terrestrial crabs. Am mid Nat 85:97–107. https://doi.org/10.2307/2423915
Ragagnin MN, Sant’AnnaGormanCastro BSDCC, Tschiptschin AP, Turra A (2016) What makes a good home for hermits? Assessing gastropod shell density and relative strength. Mar Biol Res 12:379–388. https://doi.org/10.1080/17451000.2016.1148818
Reese ES (1969) Behavioral adaptations of intertidal hermit crabs. Am Zool 9:343–355. https://doi.org/10.1093/icb/9.2.343
Rios E (2009) Compendium of Brazilian Sea Shells. Rio Grande.
Rodrigues GFB, Ballarin CS, Fransozo A, Amorim FW (2020) Structural patterns of a coastal hermit crab-gastropod shell interaction network new insights from a unique relationship. Mar Ecol Prog Ser 640:117–126
Sant’Anna BS, Dominciano LC da C, Buozi SF, Turra A, (2012) Is shell partitioning between the hermit crabs Pagurus brevidactylus and Pagurus criniticornis explained by interference and / or exploitation competition? Mar Biol Res 8:662–669. https://doi.org/10.1080/17451000.2011.653371
Santos MP, Rodrigues GFB, Negreiros-Fransozo ML, Fransozo V (2021) Resource partitioning and adequacy among ontogenetic groups in a hermit crab and gastropod shell network. Aquat Ecol 55:253–264. https://doi.org/10.1007/s10452-020-09827-0
Sato M, Jensen GC (2005) Shell selection by the hermit crab, Pagurus hartae (Mclaughlin & Jensen, 1996) (Decapoda: Anomura). Crustaceana 78:755–760. https://doi.org/10.1163/156854005774353494
da Silva AR, Santos RAP, Gryszyszyn LM, Paluski GB, & Gregati RA (2022b) Movement pattern and population structure of Clibanarius antillensis Stimpson , 1859 in south Brazil. J Mar Biol Assoc UK
Simões SM, Costa RC, Fransozo A, Castilho AL (2010) Diel variation in abundance and size of the seabob shrimp Xiphopenaeus kroyeri (Crustacea, Penaeoidea) in the Ubatuba region, southeastern Brazil. An Acad Bras Cienc 82:369–378. https://doi.org/10.1590/S0001-37652010000200013
Sokolowicz CC, Ayres-Peres L, Santos S (2007) Atividade nictimeral e tempo de digestão de Aegla longirostri (Crustacea, Decapoda, Anomura ). Iheringia Ser Zool 97:235–238. https://doi.org/10.1590/S0073-47212007000300002
Stanski G, Silva da AR, Castilho AL (2018) Characterization of epibionts associated with gastropod shells inhabited by Isocheles sawayai (Crustacea: Decapoda: Anomura) on the north coast of Santa Catarina. Rev Mex Biodivers 89:815–822. https://doi.org/10.22201/ib.20078706e.2018.3.2167
Strauss J, Dircksen H (2010) Circadian clocks in crustaceans: identified neuronal and cellular systems. Front Biosci 15:1040–1074. https://doi.org/10.2741/3661
Suárez-Rodríguez M, Kruesi K, Alcaraz G (2019) The shadow of the shell: a cue for a new home. J Mar Biol Assoc UK 99:1165–1169. https://doi.org/10.1017/S0025315419000122
Sultana Z, Babarinde IA, Asakura A (2022) Diversity and molecular phylogeny of pagurid hermit crabs (anomura: paguridae: pagurus ). Diversity 14:1–27
Trussell GC (2000) Predator-induces plasticity and morphological trade-offs in latitudinally separated populations of Littorina obtusata. Evol Ecol Res 2:803–822
Turra A (2003) Shell condition and adequacy of three sympatric intertidal hermit crab populations. J Nat Hist 37:1781–1795. https://doi.org/10.1080/00222930110116020
Turra A (2004) Intersexuality in hermit crabs: reproductive role and fate of gonopores in intersex individuals. J Mar Biol Assoc UK 84:757–759. https://doi.org/10.1017/S0025315404009877h
Turra A, Denadai MR (2004) Interference and exploitation components in interespecific competition between sympatric intertidal hermit crabs. J Exp Mar Biol Ecol 310:183–193. https://doi.org/10.1016/j.jembe.2004.04.008
Vance RR (1972) Competition and mechanism of coexistence in three sympatric of intertidal hermit crabs. Ecology 53:1062–1074. https://doi.org/10.2307/1935418
Vance RR (1972) The role of shell adequacy in behavioral interactions involving hermit crabs. Ecology 53:1075–1083. https://doi.org/10.2307/1935419
Villéger S, Mason NWH, Mouillot D (2008) New multidimensional functional diversity indices for a multifaceted framework in functional ecology. Ecology 89:2290–2301
Violle C, Navas M-L, Vile D, Kazakou E, Fortunel C, Hummel I, Garnier E (2007) Let the concept of trait be functional! Oikos 116:882–892
Vitaterna MH, Takahashi JS, Turek FW (2001) Overview of circadian rhythms. Alcohol Res Health 25:85–93
Williams JD, McDermott JJ (2004) Hermit crab biocoenoses: a worldwide review of the diversity and natural history of hermit crab associates. J Exp Mar Biol Ecol 305:1–128. https://doi.org/10.1016/j.jembe.2004.02.020
Acknowledgements
The authors are grateful to the UNICENTRO facilities, which allowed the experiments to happen. This work was supported by Pró-Reitoria de Pesquisa – USP , National Council for Scientific and Technological (A.R.S., PRP – USP, CNPq #151038/2022-8), Coordination for higher Education Staff Development (R.A.P.S., CAPES), São Paulo Research Foundation (G.F.B.R. – FAPESP #2019/01287-8). The authors are thankful for the anonymous reviewers’ suggestions.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of Interest
The authors declare there is no conflict of interest.
Ethical approval
The research was conducted according to Brazilian’s law and scientific ethics guidelines.
Additional information
Communicated by Télesphore Sime-Ngando.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
da Silva, A.R., Santos, R.A.P., Rodrigues, G.F.B. et al. Coexistence of two sympatric hermit crab species from South Brazil: the effect of the shell adequacy index and circadian movement patterns. Aquat Ecol 57, 459–469 (2023). https://doi.org/10.1007/s10452-023-10022-0
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10452-023-10022-0