Abstract
Rhizocephalan barnacles are highly specialized parasitic crustaceans that profoundly alter the morphology, physiology, and reproduction of their decapod hosts. In hermit crabs (Paguridae), parasitism by peltogastrid rhizocephalans has been reported to induce feminization of male secondary sexual traits, such as the development of female-specific pleopods and the reduction of cheliped size; however, quantitative and comparative analyses across host–parasite combinations remain limited. In this study, we examined morphological feminization in four hermit crab species (Pagurus lanuginosus, Pa. filholi, Pa. nigrivittatus, and Pa. japonicus) parasitized by three peltogastrid rhizocephalans (Peltogaster sp., Pe. postica, and Pe. aff. ovalis). The frequency of individuals possessing a second pleopod, a female-specific structure for egg brooding, was significantly higher in parasitized males of Pa. lanuginosus and Pa. nigrivittatus, whereas no significant difference was detected in Pa. filholi. Allometric analyses revealed pronounced reductions in cheliped length in parasitized males of Pa. lanuginosus and Pa. japonicus, with regression slopes approaching those of unparasitized females. Effect size analyses further demonstrated that cheliped lengths of parasitized Pa. lanuginosus and Pa. japonicus were similar to those of unparasitized females, whereas those in parasitized Pa. filholi and Pa. nigrivittatus were not, indicating the magnitude of feminization differed markedly among host–parasite combinations. These results indicate that peltogastrid-induced morphological feminization in hermit crabs is species-specific and depends on both host and parasite identity. Our findings highlight the importance of integrating molecular identification of parasites with quantitative morphological analyses to elucidate the diversity of host manipulation strategies in rhizocephalan barnacles.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data availability
All data collected in this study have been included in this manuscript.
References
Alvarez F, Calderon J (1996) Distribution of Loxothylacus texanus (Cirripedia: Rhizocephala) parasitizing crabs of the genus Callinectes in the Southwestern Gulf of Mexico. Gulf Caribb Res 9:205–210. https://doi.org/10.18785/grr.0903.08
Feng C, Zhang J, Bao J, Luan D, Jiang N, Chen Q (2023) Transcriptome analysis of germ cell changes in male Chinese mitten crabs (Eriocheir sinensis) induced by rhizocephalan parasite, Polyascus gregaria. Front Mar Sci 10:144448. https://doi.org/10.3389/fmars.2023.1144448
Folmer O, Black M, Hoeh W, Lutz R, Vrijenhoek R (1994) DNA primers for amplification of mitochondrial cytochrome C oxidase subunit I from diverse metazoan invertebrates. Mol Mar Biol Biotechnol 3:294–299. https://doi.org/10.1371/journal.pone.0013102
Galil BS, Lützen J (1995) Biological observations on Heterosaccus dollfusi Boschma (Cirripedia: Rhizocephala), a parasite of Charybdis longicollis Leene (Decapoda: Brachyura), a lessepsian migrant to the Mediterranean. J Crust Biol 15:659–670. https://doi.org/10.2307/1548815
Hartnoll RG (1962) Parasitic castration of Macropodia longirostris (Fabricius) by a sacculinid. Crustaceana 295–300. https://doi.org/10.1163/156854062X00265
Hedges LV (1981) Distribution theory for Glass’s estimator of effect size and related estimators. J Educ Stat 6:107–128. https://doi.org/10.3102/10769986006002107
Høeg JT (1995a) The biology and life cycle of the Cirripedia rhizocephala. J Mar Biol Assoc UK 75:517–550. https://doi.org/10.1017/S0025315400038996
Høeg JT (1995b) Sex and the single cirripede: a phylogenetic perspective. In: Schram FR, Høeg JT (eds) New frontiers in barnacle evolution. Crustacean Issues, vol 10. A. A. Balkema, Rotterdam, pp 195–208
Høeg JT, Lützen J (1995) Life cycle and reproduction in the Cirripedia Rhizocephala. Oceanogr Mar Biol Annu Rev 33:427–485
Høeg JT, Rees DJ, Jensen PC, Glenner H (2019) Unravelling the evolution of the Rhizocephala: a case study for molecular-based phylogeny in the parasitic Crustacea. In: Smit NJ, Bruce NKL, Hadfield KA, editors. Parasitic Crustacea: State of knowledge and future trends. Zool Monogr. Vol. 3. Feldhar H, Schmidt-Rhaesa A, series editors. Cham: Springer:387–419. https://doi.org/10.1007/978-3-030-17385-2_9
Hines AH, Alvarez F, Reed SA (1997) Introduced and native populations of a marine parasitic castrator: variation in prevalence of the rhizocephalan Loxothylacus panopaei in xanthid crabs. Bull Mar Sci 61:197–214
Innocenti G, Vannini M, Galil BS (1998) Notes on the behaviour of the portunid crab Charybdis longicollis Leene parasitized by the rhizocephalan Heterosaccus dollfusi Boschma. J Nat Hist 32:1577–1585. https://doi.org/10.1080/00222939800771111
Jung J, Yoshida R, Kim W (2019) Diversity of parasitic peltogastrid barnacles (Crustacea: cirripedia: Rhizocephala) on hermit crabs in Korea. Zool Stud 58:33. https://doi.org/10.6620/ZS.2019.58-33
Jung J, Yoshida R, Lee D, Park JK (2021) Morphological and molecular analyses of parasitic barnacles (Crustacea: Cirripedia: Rhizocephala) in Korea: preliminary data for the taxonomy and host ranges of Korean species. PeerJ 9:e12281. https://doi.org/10.7717/peerj.12281
Kajimoto A, Høeg JT, Kato K, Yusa Y (2022) Variations in life cycle and seasonal sex ratio in the rhizocephalan Peltogasterella gracilis (Boschma, 1927) (Cirripedia: Rhizocephala: Peltogasterellidae). J Crustac Biol 42:ruac057. https://doi.org/10.1093/jcbiol/ruac057
Kajimoto A, Iwasaki A, Ohira T, Toyota K (2025a) Morphological feminization in hermit crabs (family Paguridae) induced by rhizocephalan barnacles. Zool Lett 11:6. https://doi.org/10.1186/s40851-025-00252-5
Kajimoto A, Toyota K, Yusa Y (2025b) Effects of morphological changes induced by the rhizocephalan parasite Polyascus polygenea on predation risk of the Asian shore crab Hemigrapsus sanguineus. Zool Stud 64:59. https://doi.org/10.6620/ZS.2025.64-59
Kirby KN, Gerlanc D (2013) Boot ES: An R package for bootstrap confidence intervals on effect sizes. Behav Res Methods 45:905–927. https://doi.org/10.3758/s13428-013-0330-5
Kristensen T, Nielsen AI, Jørgensen AI, Mouritsen KN, Glenner H, Christensen JT, Lützen J, Høeg JT (2012) The selective advantage of host feminization: a case study of the green crab Carcinus maenas and the parasitic barnacle Sacculina carcini. Mar Biol 159:2015–2023. https://doi.org/10.1007/s00227-012-1988-4
Kuris AM (1974) Trophic interactions: similarity of parasitic castrators to parasitoids. Q Rev Biol 49:129–148. https://doi.org/10.1086/408018
Lafferty KD, Kuris AM (1994) Potential uses for biological control of alien marine species. In: Proceedings of the Conference and Workshop on Nonindigenous Estuarine and Marine Organisms. NOAA, Washington, DC:97–102
Lafferty KD, Kuris AM (2009) Parasitic castration: the evolution and ecology of body snatchers. Trends Parasitol 25:564–572. https://doi.org/10.1016/j.pt.2009.09.003
Lützen J, Itani G, Jespersen Å, Hong JS, Rees D, Glenner H (2016) On a new species of parasitic barnacle (Crustacea: Rhizocephala), Sacculina shiinoi sp. nov., parasitizing Japanese mud shrimps Upogebia spp. (Decapoda: Thalassinidea: Upogebiidae), including a description of a novel morphological structure in the Rhizocephala. Zool Sci 33:204–212. https://doi.org/10.2108/zs150112
Lützen J, Jensen KH, Glenner H (2018) Life history of Sacculina carcini Thompson, 1836 (Cirripedia: rhizocephala: Sacculinidae) and the intermoult cycle of its host, the shore crab Carcinus maenas (Linnaeus, 1758)(Decapoda: Brachyura: Carcinidae). J Crustac Biol 38:413–419. https://doi.org/10.1093/jcbiol/ruy044
McDermott JJ, Williams JD, Boyko CB (2010) The unwanted guests of hermits: a global review of the diversity and natural history of hermit crab parasites. J Exp Mar Biol Ecol 394:2–44. https://doi.org/10.1016/j.jembe.2010.06.022
McLaughlin PA (2002) A review of the hermit crab (Decapoda: anomura: Paguridea) fauna of Southern Thailand, with particular emphasis on the Andaman Sea, and descriptions of three new species. PMBC Spec Publ 23:385–460
Mouritsen KN, Geyti SN, Lützen J, Høeg JT, Glenner H (2018) Population dynamics and development of the rhizocephalan Sacculina carcini, parasitic on the shore crab Carcinus maenas. Dis Aquat Org 131:199–211. https://doi.org/10.3354/dao03290
Nagler C, Hörnig MK, Haug JT, Noever C, Høeg JT, Glenner H (2017) The bigger, the better? Volume measurements of parasites and hosts: parasitic barnacles (Cirripedia, Rhizocephala) and their decapod hosts. PLoS ONE 12:e0179958. https://doi.org/10.1371/journal.pone.0179958
Nielsen SO (1970) The effects of the rhizocephalan parasites Peltogaster paguri Rathke and Gemmosaccus sulcatus (Lilljeborg) on five species of Paguridan hosts (Crustacea Decapoda). Sarsia 42:17–32. https://doi.org/10.1080/00364827.1970.10411160
Oanh LET, Kieu ATN, Hoang TQ, Vu VT, Ha Sang Quang Tran, Oanh Thi Truong, Henrik Glenner, Binh Thuy Dang (2025) Morphological and molecular characterization of Heterosaccus papillosus Boschma, 1933 (Rhizocephala: Sacculinidae) and its effects on the swimming crab Charybdis anisodon De Haan, 1850 (Decapoda: Portunidae) in Nha Trang Bay, Vietnam. Zootaxa 5673:213–226. https://doi.org/10.11646/zootaxa.5673.2.3
Oguro C (1955) On the sacculinization of the hermit-crab, Eupagurus ochotensis (Brandt). Annot Zool Jpn 28:100–105
Percie du Sert N, Hurst V, Ahluwalia A, Alam S, Avey MT, Baker M, Browne WJ, Clark A, Cuthill IC, Dirnagl U, Emerson M (2020) The ARRIVE guidelines 2.0: updated guidelines for reporting animal research. J Cereb Blood Flow Metab 40:1769–1777. https://doi.org/10.1177/0271678X20943823
Podsiadlowski L, Bartolomaeus T (2005) Organization of the mitochondrial genome of mantis shrimp Pseudosquilla ciliata (Crustacea: Stomatopoda). Mar Biotechnol 7:618–624. https://doi.org/10.1007/s10126-005-0017-8
Rahayu DL (2022) Hermit crabs of Singapore (Crustacea: decapoda: anomura: diogenidae, Paguridae), with description of two new species. Raffles Bull Zool 1:70. https://doi.org/10.26107/RBZ-2022-0017
R Core Team (2022) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. URL: https://www.R-project.org/ Accessed 17 December 2025
Rees D, Glenner H (2014) Control region sequences indicate that multiple externae represent multiple infections by Sacculina carcini (Cirripedia: Rhizocephala). Ecol Evol 4:3290–3297. https://doi.org/10.1002/ece3.1177
Reinhard EG (1950) An analysis of the effects of a sacculinid parasite on the external morphology of Callinectes sapidus Rathbun. Biol Bull 98:255–288. https://doi.org/10.2307/1538676
Ritchie LE, Høeg JT (1981) The life history of Lernaeodiscus porcellanae (Cirripedia: Rhizocephala) and co-evolution with its porcellanid host. J Crustac Biol 1:334–347. https://doi.org/10.2307/1547966
Schmidt M, Martin I, Melzer RR (2024) Just a matter of size? Evaluating allometry and intersexual heterometry in Pagurus bernhardus using ratios and indices (Decapoda, Anomura). Integr Zool 19:807–823. https://doi.org/10.1111/1749-4877.12794
Shiino SM (1931) Studies on the modification of sexual characters in Eupagurus samuelis caused by a rhizocephalan parasite Peltogaster sp. Mem Coll Sci Kyoto Imp Univ Ser B 7:63–101. http://hdl.handle.net/2433/257760
Takahashi T, Iwashige A, Matsuura S (1997) Behavioral manipulation of the shore crab, Hemigrapsus sanguineus by the rhizocephalan barnacle, Sacculina polygenea. Crustacean Res 26:153–161. https://doi.org/10.18353/crustacea.26.0_153
Toyota K, Ito T, Morishima K, Hanazaki R, Ohira T (2023) Sacculina-Induced morphological feminization in the Grapsid crab Pachygrapsus crassipes. Zool Sci 40:367–374. https://doi.org/10.2108/zs230022
Tsuchida K, Lützen J, Nishida M (2006) Sympatric three-species infection by Sacculina parasites (Cirripedia: Rhizocephala: Sacculinidae) of an intertidal grapsoid crab. J Crust Biol 26:474–479. https://doi.org/10.1651/S-2682.1
Xie J, Ying C, Tang Z, Yang Y, Liu K (2025) Eyestalk transcriptome analysis reveals sexually dimorphic host-parasite interactions: divergent molecular strategies of Polyascus sp. for reproductive and growth regulation in Eriocheir sinensis. PeerJ 13:e20089. https://doi.org/10.7717/peerj.20089
Yanagimachi R (1960) The life cycle of Peltogasterella gracilis (Rhizocephala, Cirripedia). Bull Mar Biol Stn Asamushi 10:109–110. https://doi.org/10.1163/156854061X00158
Yanagimachi R (1961) Studies on the sexual organization of the Rhizocephala. III. The mode of sex-determination in Peltogasterella. Biol Bull 120:272–283. https://doi.org/10.2307/1539383
Yoshida R, Hirose M, Hirose E (2014) Hermit crab host prevalence by species of Peltogastridae (Cirripedia: Rhizocephala): hosts vary with locations on the Pacific coast in mainland Japan. J Crustac Biol 34:467–480. https://doi.org/10.1163/1937240X-00002246
Acknowledgements
We offer our deepest thanks to Dr. Ryota Yoshida (Ochanomizu University) for his valuable comments on this manuscript. We express our gratitude to Mr. Soma Nakatogawa (Kanagawa University), Soma Kyotani (Tokyo University of Marine Science and Technology), Naoto Takiyama (Tokyo University of Marine Science and Technology), Haruki Shinoda (Kyoto University), and Keito Tsunoda (Hiroshima University / Kanazawa University) for field sampling. We thank all the members of the Laboratory of Physiological Ecology, Hiroshima University, for their kind help.
Funding
This work was supported by a grant from Research Institute of Marine Invertebrates (KO2024-04) and a Grant-in-Aid for Scientific Research (25K18553) to AK, and by the TAKARA Harmonist Fund 202, the Mikimoto Fund for Marine Ecology, Grants-in-Aid for Scientific Research (24K09616 and 25H02425), and NIBB Collaborative research projects for Trans-Scale Biology (25NIBB103) to KT.
Author information
Authors and Affiliations
Contributions
AK, TO, and KT designed the research. AK and AT conducted the sampling and measured the morphological parameters. AK and AT conducted the sequencing. AK analyzed all data and wrote the first draft, and all authors approved the final version of the manuscript.
Corresponding authors
Ethics declarations
Conflict of interest
The authors declare that they have no competing interests.
Ethical Standards
All experimental procedures and sampling protocols complied with the guidelines of the Institutional Animal Care and Use Committee of Kanagawa University. All animal experiments were conducted in accordance with the ARRIVE guidelines (Percie du Sert et al. 2020).
Additional information
Responsible Editor: F. Bulleri.
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
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
Kajimoto, A., Tanaka, A., Ohira, T. et al. Parasite-induced feminization across host–parasite combinations in pagurid hermit crabs infected by peltogastrid rhizocephalans (Crustacea: Cirripedia: Rhizocephala). Mar Biol 173, 105 (2026). https://doi.org/10.1007/s00227-026-04860-3
Received:
Accepted:
Published:
Version of record:
DOI: https://doi.org/10.1007/s00227-026-04860-3
