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Mobile habitats for the unseen passengers: the brachyuran crabs on the loggerhead sea turtles

Published online by Cambridge University Press:  27 January 2025

Ryota Hayashi Open the ORCID record for Ryota Hayashi [Opens in a new window]  and
Naoya Ohtsuchi
Ryota Hayashi*
Affiliation:
Research & Development Center, Nippon Koei Co., Ltd., Ibaraki, Japan
Naoya Ohtsuchi
Affiliation:
Otsuchi Coastal Research Center, Atmosphere and Ocean Research Institute, The University of Tokyo, Otsuchi, Iwate, Japan
*
Corresponding author: Ryota Hayashi; Email: bubobubo32@gmail.com
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Abstract

We report on four brachyuran crabs collected from the carapaces of loggerhead sea turtles Caretta caretta nesting on Yakushima Island in Kagoshima prefecture, Japan. Three of these crab species have not been previously reported as epibionts on sea turtles. Our research suggests that physical damage to a turtle's carapace, such as cracks and holes created by other epibionts like the burrowing barnacle Tubicinella cheloniae, can create unique habitats for these opportunistic crabs.

Keywords

crabsloggerhead sea turtlesnew host records
Type
Marine Record
Information
Journal of the Marine Biological Association of the United Kingdom , Volume 105 , 2025 , e4
Copyright
Copyright © The Author(s), 2025. Published by Cambridge University Press on behalf of Marine Biological Association of the United Kingdom

Introduction

Sea turtles host diverse epibiotic communities (Robinson and Pfaller, Reference Robinson and Pfaller2022), of which the most diverse have been observed on loggerhead sea turtles, Caretta caretta (Linnaeus, 1758) (Caine, Reference Caine1986; Gramentz, Reference Gramentz1988). Epibiotic organisms can be valuable indicators of sea turtle migratory behaviour and life history (e.g., Hayashi and Tsuji, Reference Hayashi and Tsuji2008; Hayashi, Reference Hayashi2009; Fuller et al., Reference Fuller, Broderick, Enever, Thorne and Godley2010). Here, we describe new reports of brachyuran crabs as epibionts on loggerhead sea turtles and present a list of epibiotic records of crabs.

Materials and methods

We sampled 171 female loggerhead sea turtles for epibionts from 2015 to 2017 (May–July) on Yakushima Island, Kagoshima prefecture, southwestern Japan (Figure 1A). Yakushima Island contains one of the most important nesting beaches for loggerhead turtles in the North Pacific (Matsuzawa et al., Reference Matsuzawa, Kamezaki, Ishihara, Omuta, Takeshita, Goto, Arata, Honda, Kameda, Kashima, Kayo, Kawazu, Kodama, Kumazawa, Kuroyanagi, Mizobuchi, Mizuno, Oki, Watanabe, Yamamoto, Yamashita, Yamato, Hamabata, Ishizaki and Dutton2016). Samples, including crabs and other taxa, were collected from carapaces with a scraper and forceps and preserved in 99% ethanol, and the crabs were deposited in the Coastal Branch of Natural History Museum and Institute, Chiba, under accession number CMNH-ZE 2956–2960. Crab measurements (in mm) are carapace width (CW), carapace length (CL) and carapace length excluding pseudorostral spines (PCL). Turtle measurements are straight carapace length (SCL) and straight carapace width (SCW).

Figure 1. (A) Map showing the sampling site, Yakushima Island; (B) Pilumnus ikedai in the crack of the loggerhead carapace.

Result

Taxonomy

Subsection Heterotremata Guinot, 1977
Superfamily Majoidea Samouelle, 1819
Family Epialtidae MacLeay, 1838
Genus Hyastenus White, 1847
Hyastenus borradailei (Rathbun, 1907)
[Japanese name: Borradaile-tsuno-gani]
(Figure 2A, B)
Materials examined

CMNH-ZE 2956, one female (PCL 12.1 mm × CW 8.2 mm excluding branchial spines) collected from a loggerhead turtle (SCL 97.2 cm and SCW 71.1 cm) from Yakushima Island, Kagoshima, Japan, 4 June 2017, coll. R. Hayashi.

Figure 2. Brachyuran crabs collected from the loggerhead turtle Caretta caretta (Linnaeus, 1758). (A, B) Hyastenus borradailei (Rathbun, 1906), female (12.1 × 8.2 mm), CMNH-ZE 2956; (C, D) Pilumnus ikedai Takeda and Miyake, Reference Takeda and Miyake1968, female (5.7 × 7.5 mm), CMNH-ZE 2957; (E, F) Thalamita gatavakensis Nobili, Reference Nobili1906, male (2.7 × 3.5 mm), CMNH-ZE 2958; (G, H) Planes major (MacLeay, 1838), female (20.7 × 20.6 mm), CMNH-ZE 2959 and ovigerous female (20.8 × 20.6 mm), CMNH-ZE 2960.

Remarks

Hyastenus borradailei is known from the Indo-West Pacific including Seychelles, northern Australia (from Ninety Mile Beach, Western Australia to Moreton Bay, Queensland, Indonesia, Tuvalu, and Japan. This species is found in sub-tidal habitats and down to depths of 30 m (Griffin and Tranter, Reference Griffin and Tranter1986). In Japan, this species has been recorded from Misaki, Tosa Okinoshima, coast of Wakayama (Sakai, Reference Sakai1938, Reference Sakai1976); Mage-jima, Osumi Islands (Takeda, Reference Takeda1977); Kushimoto-Arita, Kii Peninsula (Miyake, Reference Miyake1983); Kakeroma-jima Island, Amami Group (Takeda, Reference Takeda1989); and Kume-jima, Okinawa (Minemizu, Reference Minemizu2000, based on a photograph). This is the first record of this species as an epibiont on sea turtles. The host turtle is the same individual Hayashi and Okanishi (Reference Hayashi and Okanishi2019) reported. The collected individual was found in a hole made by a bullowing barnacle, Tubicinella cheloniae Monroe and Limpus, 1979.

Superfamily Pilumnoidea Samouelle, 1819
Family Pilumnidae Samouelle, 1819
Genus Pilumnus Leach, 1815
Pilumnus ikedai Takeda and Miyake, Reference Takeda and Miyake1968
[Japanese name: Ikeda-kebuka-gani]
(Figure 2C, D)
Materials examined

CMNH-ZE 2957, one female (CL 5.7 mm × CW 7.5 mm) and one ovigerous female (5.9 mm × 7.9 mm) collected from a loggerhead turtle (SCL 98.6 cm and SCW 76.7 cm) from Yakushima Island, Kagoshima, Japan, 20 May 2016, coll. R. Hayashi.

Remarks

A poorly known pilumnid species, Pilumnus ikedai, was initially described based on an ovigerous female from Ototo-jima Island, Bonin [ = Ogasawara Islands] (Takeda and Miyake, Reference Takeda and Miyake1968). Marumura and Kosaka (Reference Marumura and Kosaka2003: 56) listed two males and three females from Shionomisaki, Wakayama, Kii Peninsula, in the catalogue of the Nagai Collection deposited in the Wakayama Prefectural Museum of Natural History. Our specimen fitted well with the description by Takeda and Miyake (Reference Takeda and Miyake1968), although some differences were observed. The first anterolateral spine of the carapace bears only one accessory spine (two or three in the holotype), and the left cheliped is larger in the larger, ovigerous specimen (the right one being larger in the holotype). This is the first record of this species as an epibiont on sea turtles. The material was collected from an injury approximately 1 cm deep on the turtle's carapace.

Superfamily Portunoidea Rafinesque, 1815
Family Portunidae Rafinesque, 1815
Genus Thalamita Latreille, 1829
Thalamita gatavakensis Nobili, Reference Nobili1906
[Japanese name: Gatabaku-benitsuke-gani]
(Figure 2E, F)
Materials examined

CMNH-ZE 2958, one male (CL 2.7 mm × CW 3.5 mm including lateral teeth) collected from a loggerhead turtle (SCL 78.5 cm and SCW 60.3 cm), from Yakushima Is., Kagoshima, Japan, 15 June 2017, coll. R. Hayashi.

Remarks

The specimen is a small juvenile with morphological characters that generally fit the description of Thalamita gatavakensis given by Wee and Ng (Reference Wee and Ng1995). The following characteristics are primarily diagnostic for this species: two-lobed front; five anterolateral teeth of the carapace of which the third is slightly smaller than the others and the fourth is somewhat subsidiary to the third; five spines on the dorsal surface of cheliped propodus; the presence of three granular costae on the outer chela surface; and the presence of 6–9 spines on the posterior margin of natatory leg propodus. The tubercles lined on the basal antennal ridge are obscure and transverse ridges on the carapace surface are partly faint in the present specimen. Consequently, we were unable to use the taxonomic key by Wee and Ng (Reference Wee and Ng1995).

Thalamita gatavakensis is widely distributed in the Indo-West Pacific: French Polynesia, Saipan, Japan, Australia, Philippines, Indonesia, Malaysia, Thailand, Seychelles, Madagascar, and Kenya (Nobili, Reference Nobili1906; Stephenson, Reference Stephenson1972; Wee and Ng, Reference Wee and Ng1995; Davie, Reference Davie, Wells and Houston2002; Ng and Davie, Reference Ng and Davie2002; Komatsu, Reference Komatsu2011; Poupin et al., Reference Poupin, Cleva, Bouchard, Dinhut and Dumas2018). This species has been recorded in Japan from Araihama, Miura Peninsula, Shionomisaki, Kii Peninsula, and off Ogasawara Islands (Marumura and Kosaka, Reference Marumura and Kosaka2003; Komatsu, Reference Komatsu2011). The bathymetric records include intertidal depths of 1–135.8 m (Stephenson, Reference Stephenson1972; Komatsu, Reference Komatsu2011). Shallow water specimens were found on coral sandy habitats (Crosnier, Reference Crosnier1962, intertidal) or among boulders on gravelly bottoms near rocky reefs (Takeda and Ohtsuchi, Reference Takeda and Ohtsuchi2021; at a depth of 2 m). This is the first record of this species as an epibiont on sea turtles. The material was collected from an injury approximately 1 cm deep on the turtle's carapace.

Subsection Thoracotremata Guinot, 1977
Superfamily Grapsoidea MacLeay, 1838
Family Grapsidae MacLeay, 1838
Genus Planes Bowdish, 1825
Planes major (MacLeay, 1838)
[Japanese name: Oki-nagare-gani]
(Figure 2G, H)
Materials examined

CMNH-ZE 2959, one female (CL 20.7 mm × CW 20.6 mm) collected from a loggerhead turtle (SCL 81.0 cm and SCW 64.5 cm), from Yakushima Island, Kagoshima, Japan, 25 May 2017, coll. R. Hayashi, CMNH-ZE 2960, one ovigerous female (20.8 mm × 20.6 mm) collected from a loggerhead turtle (SCL 76.8 cm and SCW 64.1 cm) from Yakushima Is., Kagoshima, Japan, 25 May 2017, coll. R. Hayashi.

Remarks

Planes Bowdich, 1825 is a rafting crab genus with three epipelagic, hyponeustonic species (Poupin et al., Reference Poupin, Davie and Cexus2005). Planes major is widely distributed in the Pacific Ocean. This species has many synonyms (see Chace, Reference Chace1951; Prado and De Melo, Reference Prado and de Melo2002) and was previously known as Planes cyaneus Dana, 1851 (Takeda, Reference Takeda1982; Miyake, Reference Miyake1983; Prado and De Melo, Reference Prado and de Melo2002; Marumura and Kosaka, Reference Marumura and Kosaka2003). In addition, Ng and Ahyong (Reference Ng and Ahyong2001) who reexamined the type specimens of Nautilograpsus major (McLeay, 1838) concluded that N. major is conspecific with P. cyaneus. This nomenclatural change was generally followed by recent taxonomic studies (Takeda and Webber, Reference Takeda and Webber2006; Wicksten, Reference Wicksten2012). Recently, Pfaller et al. (Reference Pfaller, Payton, Bjorndal, Bolten and McDaniel2019a) conducted a global molecular analysis for Planes spp. collected from sea turtles and various substrata. This genetic analysis suggested that P. major and P. minutus (originally described as Cancer minutus Linnaeus, 1758) were the same species. However, Pfaller et al. (Reference Pfaller, Payton, Bjorndal, Bolten and McDaniel2019a) did not thoroughly describe the morphological characters used to distinguish between each species. Although their conclusion has been accepted in subsequent studies (Yaghmour and Al Naqbi, Reference Yaghmour and Al Naqbi2020; Tavares and Mendonça, Reference Tavares and Mendonça2022), a direct comparison between the type specimens of C. minutus and N. major is necessary before any formal nomenclatural changes can be made.

In Japan, the rafting crabs have been documented as an epibiont primarily on floating substrates, such as rafting algae, which often strand on beaches across regions from the Ryukyu and Ogasawara Islands to the Boso Peninsula (e.g., Sakai, Reference Sakai1965, Reference Sakai1976; Miyake, Reference Miyake1983; Marumura and Kosaka, Reference Marumura and Kosaka2003; Maenosono, Reference Maenosono2018; Takeda et al., Reference Takeda, Komatsu, Shikatani, Maenosono and Naruse2019). In addition to these passive substrates, this species has also been observed on highly mobile hosts such as sea turtles, where it utilizes the supracaudal space as a microhabitat (cf. Yaghmour and Al Naqbi, Reference Yaghmour and Al Naqbi2020: Fig. 1B, as P. minutus). The morphological characteristics of the specimens examined in this study align with the descriptions and illustrations of P. major provided by Miyake (Reference Miyake1983), Prado and De Melo (Reference Prado and de Melo2002) and Poupin et al. (Reference Poupin, Davie and Cexus2005).

Discussion

A total of 23 species of brachyuran crabs have been previously reported as epibionts on sea turtles, and we add three more species to this list (Table 1). Fuller et al. (Reference Fuller, Broderick, Enever, Thorne and Godley2010) reported that non-barnacle epibionts were associated with either posterior algal mats or carapace scars. The three new host records of crabs in this report were also collected from the empty shell holes made by the burrowing barnacle T. cheloniae or cracked scars on the turtle carapace (Figure 1B). The empty shell holes of T. cheloniae also offer incidental habitats for various organisms, such as the brittlestar Ophiactis savignyi (Müller and Troschel, 1842) on turtle carapaces (Hayashi and Okanishi, Reference Hayashi and Okanishi2019). Thus, the burrowing barnacle T. cheloniae likely provides opportunistic habitats for various epipelagic organisms.

Table 1. Records of the brachyuran crabs from sea turtles

The rafting crab P. major has been frequently reported in association with sea turtles (Martinelli and Isaac, Reference Martinelli and Isaac2001; Pfaller et al., Reference Pfaller, Alfaro-Shigueto, Balazs, Ishihara, Koptisky, Mangel, Peckham, Bolten and Bjorndal2014a, Reference Pfaller, Alfaro-Shigueto, Giffoni, Ishihara, Mangel, Peckham, Bjorndal and Baeza2014b, Reference Pfaller, Payton, Bjorndal, Bolten and McDaniel2019a, Reference Pfaller, Palau, Agamboué, Barret, Ciccione, Cliff, Formia, Manfoumbi, Marco, Sounguet and Tucker2019b). Although species of Planes are commonly found on floating objects, such as plastic debris (Tutman et al., Reference Tutman, Kapiris, Kirinčić and Pallaoro2017), their presence on sea turtles remains sporadic and relatively rare. In this study, only two Planes individuals were observed on just two of the 171 turtles examined. Loggerhead turtles, the most frequent host organisms for rafting crabs, are known to dive to various depths depending on the individual, either shallow or deep waters (Sakamoto et al., Reference Sakamoto, Sato, Tanaka and Naito1993; Hatase et al., Reference Hatase, Omuta and Tsukamoto2007). It is hypothesized that turtle individuals offering habitats for rafting crabs may tend to prefer shallow waters, avoiding deeper dives where crabs might be dislodged. Although this hypothesis remains speculative, it underscores the potential for epibiotic organisms to serve as indicators of host behaviour, warranting further investigation to clarify these relationships.

Acknowledgements

We thank Yakushima Umigame-kan and many volunteers for helping attach tags to turtles at night on beaches. We thank Dr Junji Okuno (the Coastal Branch of Natural History Museum and Institute, Chiba) for his kind support in identifying Pilumnus ikedai. Field sampling was conducted with permission to catch animals in Yakushima National Park and permission from the Kagoshima Prefecture Turtle Protection Ordinance. We greatly appreciate the favourable comments by two anonymous reviewers.

Data availability

All relevant data are within the manuscript.

Author contributions

R. H. designed research. R. H. and N. O. involved in material preparation and data collection. R. H. obtained funding for field trips and conducted field research. N. O. was chiefly involved in species identification and analysed data. R. H. and N. O. wrote the first draft of the manuscript, and contributed to the refinement of the final manuscript.

Financial support

This study was supported in part by unemployment benefits (2015 to R. H.), the Cooperation Research Program of the Wildlife Research Center, Kyoto University (2015-C-11-1, 2016-K-1-15 and 2017-C-9 to R. H.), and the KAKENHI grant (JP16K21005 and JP19K04683 to R. H.) from the Japan Society for Promotion of Science.

Competing interest

The authors declare that they have no competing interests.

Ethical standards

Not applicable.

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Figure 0

Figure 1. (A) Map showing the sampling site, Yakushima Island; (B) Pilumnus ikedai in the crack of the loggerhead carapace.

Figure 1

Figure 2. Brachyuran crabs collected from the loggerhead turtle Caretta caretta (Linnaeus, 1758). (A, B) Hyastenus borradailei (Rathbun, 1906), female (12.1 × 8.2 mm), CMNH-ZE 2956; (C, D) Pilumnus ikedai Takeda and Miyake, 1968, female (5.7 × 7.5 mm), CMNH-ZE 2957; (E, F) Thalamita gatavakensis Nobili, 1906, male (2.7 × 3.5 mm), CMNH-ZE 2958; (G, H) Planes major (MacLeay, 1838), female (20.7 × 20.6 mm), CMNH-ZE 2959 and ovigerous female (20.8 × 20.6 mm), CMNH-ZE 2960.

Figure 2

Table 1. Records of the brachyuran crabs from sea turtles