Shell occupation by the land hermit crab Coenobita violascens (Anomura, Coenobitidae) from Phuket Island, Thailand

Abstract

Shell occupation by the land hermit crab Coenobita violascens Heller, 1862 was investigated from January 2011 to March 2012 on Phuket Island in the Andaman Coast of Thailand. The samples of C. violascens were collected monthly using multiple quadrat sampling. Twenty shell species from 11 families were found occupying by C. violascens, which were mainly marine gastropods (90%). The three most common occupied shell species were Chicoreus brunneus (Link, 1807) (21.3% of hermits), followed by Filifusus filamentosus (Röding, 1798) (14.9%) and Laevistrombus canarium (Linnaeus, 1758) (14.9%). Biconical shells and those with ovate apertures were the most commonly occupied shell types. Furthermore, individual C. violascens probably occupy the shells of at least three different gastropod species during their lifetime. Interestingly, C. violascens shows a tendency of occupying specific categories of shells in relation to shell species, shape and aperture shape. Other aspects of shell occupation by C. violascens compared to congeneric species are also discussed.

Key words:
Shell use; shell quality; terrestrial hermit crab

Introduction

Land hermit crabs are the most common crustaceans in many tropical and subtropical coastal areas and islands in Western Atlantic, Indo-Pacific, and Eastern Pacific regions (Page and Willason, 1982; Wolcott, 1988; Morrison, 2005). These hermit crabs function as generalist scavengers in coastal ecosystems, accelerating the recycling of nutrients and transfer of energy in food chain (Laidre, 2013). In addition, land hermit crabs are a critical component in the supralittoral zones of coastal and insular areas (Morrison and Spiller, 2006).

Land hermit crabs occupy discarded shells as mobile shelters to protect their soft and fragile abdomens from environmental stresses (Wolcott, 1988). Therefore, shells are crucial resources for land hermit crab life. The benefits of using shells as refuges by these crabs include protection from desiccation and predators (Greenaway, 2003). Additionally, land hermit crabs are able to replenish water into internal space of their occupied shells to maintain body moisture, allowing them to forage further inland (Wilde, 1973).

Several studies have reported correlations between occupied shell characters and hermit crab morphological characteristics (e.g. shell size and weight, aperture size, internal volume) (Hazlett, 1981; Boneka et al., 1995; Sallam et al., 2008; Bundhitwongrut et al., 2015). Empty shells probably are a limiting resource for certain hermit crab populations (Fotheringham, 1976; Kellogg, 1976; Laidre, 2012). In addition, occupied shells possibly affect growth, reproduction, and risk of predation (Blackstone, 1985; Osorno et al., 2005; Sallam et al., 2008; Contreras-Garduno et al., 2009; Sallam, 2012). Furthermore, shell resources for hermit crabs in different areas influence particular characteristics of their populations, such as abundance, size and reproduction (Fotheringham, 1976; Sallam et al., 2008).

The shell utilization patterns of land hermit crabs have been studied in several areas of the world: e.g. the western Atlantic by Morrison and Spiller (2006); the eastern Pacific by Abrams (1978), Guillen and Osorno (1993) and Laidre and Vermeij (2012); North Pacific by Willason and Page (1983) and Szabo (2012); the western Pacific by Boneka et al. (1995); Red Sea by Volker (1967), Sallam et al. (2008) and Sallam (2012); and the western Indian Ocean by Barnes (1999; 2001; 2002). Although a recent investigation by Bundhitwongrut et al. (2015) was carried out on shell use by Coenobita rugosus H. Milne Edwards, 1837 at Cape Panwa of Phuket Island in the Andaman Sea, eastern Indian Ocean, little is known about shell occupation by other land hermit crabs in this area. There are 382 gastropod mollusc species recorded from the Andaman coast of Thailand including Cape Panwa (Tantanasiriwong, 1978). However, intense shell exploitation and trade in both local and imported mollusks have been reported from Phuket Island (Aungtonya and Tantichodok, 1991; Aungtonya and Hylleberg, 1992; Aungtonya and Khokiattiwong, 1992; Bussarawit, 1995). In addition, unoccupied shells in good condition are scarce in the supralittoral zone of this site (Bundhitwongrut et al., 2015). These situations presumably influence shell resources for land hermit crabs in the area.

Seventeen valid species of land hermit crabs in the genus Coenobita Latreille, 1829 have been recognized throughout the world (De Grave et al., 2009; McLaughlin et al., 2010; Rahayu et al., 2016). Coenobita violascens Heller, 1862 is distributed in the Indo-Pacific region from the east coast of Africa to the Philippines and Japan (McLaughlin, 2007). McLaughlin (2002) reported the occurrence of C. violascens from coasts of the Andaman Sea and Gulf of Thailand. Coenobita violascens mainly inhabits beaches and areas associated with mangroves (Nakasone, 1988; McLaughlin et al., 2007; Doi et al., 2016). Limited information on the life history of C. violascens has been known and recorded. Only some recent studies on C. violascens have been recently reported, including functional morphology related to water uptake (Becchi et al., 2015), emigration behavior and molting during the sea-to-land transition (Hamasaki et al., 2015a), larval development under laboratory conditions (Hamasaki et al., 2015b; Kato et al., 2015), larval release and tree-climbing behavior (Doi et al., 2016) and thermal adaptation of embryos (Hamasaki et al., 2016). The objectives of the present study are to reveal shell occupation and the relationship between the characteristics of occupied shells and crab characteristics of C. violascens at Cape Panwa, Phuket Island, Andaman coast of Thailand.

Materials and Methods

Study area

The study site was Cape Panwa (7°48’26”N 98°24’35”E) in the southeast part of Phuket Island on the Andaman coast of Thailand. The climate is wet tropical and is influenced by the wet southwesterly monsoon from May to October and the dry northeasterly monsoon from November to April (Khokiattiwong et al., 1991). The study site is exposed to the semidiurnal tide with amplitude of 2.15-2.27 m at spring tide to 0.85-1.15 m at neap tide (Limpsaichol, 1981). The study beach was located in the supralittoral zone in the area of the Phuket Marine Biological Center (PMBC). This beach is behind the office of PMBC. The width of this beach is about 50 m and the distance between the mean sea level and the PMBC office is approximately 45 m. The beach is characterized by open sand scrub vegetation, consisting of rather coarse sand patches of shale or phylitte (Nielsen, 1976a). The inland side is covered with dense vegetation alternating with sparse vegetation in front of a steep cliff. A map of the study area and environmental data during the study period are given in Bundhitwongrut et al. (2014).

Specimen sampling and analysis

The sampling period was from January 2011 to March 2012. Coenobita violascens was collected three days per month. The hermit crabs were collected by hand by the same person (the author) at low tide from the supralittoral area in the early morning (Sallam et al., 2008). The sampling technique used in this study was multiple quadrat sampling (Barnes, 1999). Four temporary line transects were randomly placed at 15-m intervals perpendicular to the shoreline from the supralittoral zone to the inland area. Moreover, 16 temporary quadrats of area 1 m² were placed at 5-m intervals on transects from 5 m above the mean sea level to 45 m further inland. Five to six quadrats were sampled on each sampling day. Quadrats with 10-cm high walls were used to prevent the agile crabs from escaping.

All hermit crabs sampled were brought to the laboratory of PMBC. Each hermit was carefully pulled out of its occupied shell while holding the crab in the air and waiting until most of its body extended from the shell in order to investigate the crab and its inhabited shell characters. If the crab’s uropods still held onto inside the shell, especially those inhabiting shells with a long spire, a metal wire was used to tickle the crab’s abdomen to induce it to vacate the shell. To avoid negative impacts on native animals, removal of crabs from the population at the study area was not permitted according to the policy of the PMBC. Furthermore, the current sampling method prevented unnecessary hermit mortality in order to preserve this population of C. violascens. Consequently, all hermits were allowed to reinhabit their previously-occupied shells after the observations, and they were kept in several aquaria with food and water until the investigations were finished in each sampling month.

The additional marking method following Bundhitwongrut et al. (2015) was used in this study. All sampled hermits were marked after investigation in each sampling month before being released into the natural habitat from where they were collected. To prevent cheliped and pereiopod autotomy, each hermit was gently held and marked after being pulled from its shell. The markings were made with a waterproof pen and then coated with nail varnish on the outer surface of both major cheliped of each hermit and the body whorl near the outer lip of its occupied shell. In every month, if recaptured hermits were found, they were marked again.

Measurement and investigation of characters of C. violascens were carried out, including cephalothoracic shield length (CSL) and width (CSW), major chela length (MCL) and width (MCW), weight (CW), sex and reproductive stage (male, non-ovigerous female and ovigerous female). Species of occupied shells were identified according to several references (Brandt, 1974; Nielsen, 1976b; Tantanasiriwong, 1978; Middelfart, 1997; Poutiers, 1998). Additionally, those shells were compared with specimens deposited in the reference collection of PMBC to confirm their identities. Quantitative shell characters were measured and examined, including shell length (SL) and width (SW), weight (WW), internal volume (SIV), aperture length (SAL) and width (SAW). The internal volume of shells was evaluated using a graduated syringe (Floeter et al., 2000). All quantitative measurements were recorded to the nearest 0.01 mm for size using digital vernier calipers, 0.01 g for weight using digital weighing scales, and 0.1 ml volume using graduated syringes.

Qualitative shell characters were examined, including shell shape, aperture shape and shell quality. The shell and aperture shapes were categorized following Bundhitwongrut et al. (2015). The categories of shell shapes consisted of biconical, conical, elongately conical, fusiform, globose, oval, pyramidal, pyriform, turban and vermiform. The categories of shell aperture shapes comprised elongately ovate, irregular, ovate, round and semicircular. The categories of shell damage were undamaged and damaged. Damaged shells were shells with a hole, a broken apex, damaged inner lip of the body whorl, or greater damage in a large portion of the shell (Barnes, 1999). Moreover, the value of shell internal volume per weight (SIV/W ratio) was calculated for each shell inhabited by individuals of C. violascens as a predictor of shell quality (Osorno et al., 1998).

Statistical analysis

If recaptured C. violascens were found, their data were excluded to avoid possible pseudoreplicates. Individuals of C. violascens were separated into groups according to sex and reproductive stage as male, female, non-ovigerous female, or ovigerous female. Hermits were categorized into 0.5-mm CSL size classes to facilitate the comparison in shell use as a function of hermit crab size according to Nakasone (2001) and Bundhitwongrut et al. (2014). Regression analysis was utilized to determine relationships between quantitative characters of hermit crabs and occupied shells using the power function equation (Y=a.X^b) (Sallam et al., 2008; Bundhitwongrut et al., 2015). The critical significance level adopted in all statistical tests was p < 0.05. SPSS Statistics 17.0 (SPSS Inc., 2008) was used to carry out all statistical analyses.

Results

A total of 47 individuals of C. violascens were collected, including 26 males (55.3%) and 21 females (44.7%) [19 non-ovigerous females (40.4%) and 2 ovigerous females (4.3%)]. The mean CSL size ± SD and size range (minimum-maximum) was 8.81 ± 3.43 (2.99-15.73) mm for all individuals, 9.69 ± 3.74 (3.39-15.73) mm for males, 7.72 ± 2.71 (2.99-11.77) mm for all females, 7.51 ± 2.77 (2.99-11.77) mm for non-ovigerous females and 9.70 ± 0.08 (9.64-9.76) mm for ovigerous females. The number of C. violascens collected in each monthly sampling varied from 0 (February 2012) to 6 (January and July to September 2011). No recaptured individual was found during the study period.

Diversity and groups of occupied shells

Coenobita violascens was found occupying 20 species of gastropod shells of 11 families in different percentages. Main species composition of occupied shells was marine gastropods (90%, 18 species), whereas only one species was a freshwater gastropod [Pomacea canaliculata (Lamarck, 1819)] and another species was a mangrove pulmonate gastropod [Ellobium aurisjudae (Linnaeus, 1758)]. The shell family with the highest number of species occupied by C. violascens was Muricidae (30%; 6 species), followed by Turbinidae (15%; 3 species).

Shell species occupied in relation to hermit reproductive groups

The shell occupation of C. violascens varied in relation to shell species (Tab. 1). The most-occupied shell species was Chicoreus brunneus (Link, 1807) (21.3 %), followed by Filifusus filamentosus (Röding, 1798) (14.9 %) and Laevistrombus canarium (Linnaeus, 1758) (14.9 %).

Table 1
Percentage and mean SIV/W ratio of shell species inhabited by Coenobita violascens at Cape Panwa, Phuket Island, from January 2011 to March 2012. The numbers in parentheses after the percentage of shells occupied are the numbers of crab individuals. SIV/W = shell internal volume/weight ratio as mean ± SD for species that N > 1 and as value for species that N = 1.

Shell species	Family	Males	Non-ovigerous females	Ovigerous females	Total	SIV/W
Angaria delphinus (Linnaeus, 1758)	Turbinidae	3.8 (1)	-	-	2.1 (1)	0.253
Bufonaria rana (Linnaeus, 1758)	Bursidae	3.8 (1)	-	-	2.1 (1)	1.008
Cantharus tranquebaricus (Gmelin, 1791)	Buccinidae	-	5.3 (1)	-	2.1 (1)	0.308
Cerithidea obtusa (Lamarck, 1822)	Potamididae	-	5.3 (1)	-	2.1 (1)	0.457
Chicoreus brunneus (Link, 1807)	Muricidae	7.7 (2)	36.8 (7)	50.0 (1)	21.3 (10)	0.213 ± 0.056
Chicoreus ramosus (Linnaeus, 1758)	Muricidae	7.7 (2)	-	-	4.3 (2)	0.785
Clypeomorus batillariaeformis Habe & Kosuge, 1966	Cerithiidae	3.8 (1)	5.3 (1)	-	4.3 (2)	0.366 ± 0.002
Drupella rugosa (Born, 1778)	Muricidae	7.7 (2)	10.5 (2)	-	8.5 (4)	0.269 ± 0.065
Ellobium aurisjudae (Linnaeus, 1758)	Melampidae	-	5.3 (1)	-	2.1 (1)	1.054
Filifusus filamentosus (Röding, 1798)	Fasciolariidae	23.1 (6)	5.3 (1)	-	14.9 (7)	0.492 ± 0.191
Laevistrombus canarium (Linnaeus, 1758)	Strombidae	15.4 (4)	15.8 (3)	-	14.9 (7)	0.870 ± 0.241
Menathais tuberosa (Röding, 1798)	Muricidae	3.8 (1)	5.3 (1)	-	4.3 (2)	0.454 ± 0.006
Mirabilistrombus listeri (Gray, 1852)	Strombidae	-	5.3 (1)	-	2.1 (1)	0.704
Monodonta labio (Linnaeus, 1758)	Trochidae	3.8 (1)	-	-	2.1 (1)	0.471
Murex trapa Röding, 1798	Muricidae	3.8 (1)	-	-	2.1 (1)	0.849
Pollia undosa (Linnaeus, 1758)	Buccinidae	3.8 (1)	-	-	2.1 (1)	0.725
Pomacea canaliculata (Lamarck, 1819)	Ampullariidae	3.8 (1)	-	-	2.1 (1)	4.604
Thalessa virgata (Dillwyn, 1817)	Muricidae	-	-	50.0 (1)	2.1 (1)	0.354
Turbo argyrostomus Linnaeus, 1758	Turbinidae	3.8 (1)	-	-	2.1 (1)	0.514
Turbo bruneus (Röding, 1798)	Turbinidae	3.8 (1)		-	2.1 (1)	0.193

Males occupied 15 shell species while females inhabited 11 shell species (Tab. 1). Both sexes occupied six shell species (30% of total shell species occupied), which were Chicoreus brunneus, Clypeomorus batillariaeformis Habe & Kosuge, 1966, Drupella rugosa (Born, 1778), F. filamentosus, L. canarium and Menathais tuberosa (Röding, 1798). Males mostly inhabited shells of F. filamentosus (23.1%), followed by L. canarium (15.4%). Females mainly occupied shells of Chicoreus brunneus (38.1%), followed by L. canarium (14.3%). Non-ovigerous females were found occupying 10 shell species and ovigerous females were found inhabiting 2 species (Tab. 1).

Shell species occupied in relation to hermit size

Shell occupation of C. violascens varied in relation to hermit size (Fig. 1). The high diversity of shell species inhabited was found in hermits at size 11.0-11.5 mm CSL (5 species), followed by 6.0-6.5 mm CSL (4 species), and 10.5-11.0 and 11.5-12.0 mm CSL (3 species). Hermits in other size classes (2.5-6.0, 6.5-8.5, 9.0-10.5, 12.0-14.0 and 15.0-16.0 mm CSL) occupied 1-2 shell species.

Figure 1
Shell occupation by Coenobita violascens as a function of hermit crab size.

The most-occupied shell species, Chicoreus brunneus, was inhabited by medium-sized hermits (6.5-7.5, 8.0-8.5, 9.0-10.0 and 11.0-12.0 mm CSL) (Fig. 1). Smallest hermits occupied shells of Clypeomorus batillariaeformis (2.5-3.5 mm CSL) and Drupella rugosa (3.0-4.5 mm CSL). Shells of L. canarium were occupied by small- (5.0-6.5 mm CSL) and medium-sized hermits (9.0-9.5 and 10.5-11.5 mm CSL), whereas F. filamentosus shells was inhabited by a wide range of size classes of hermits (4.0-4.5, 10.5-11.0, 11.5-12.5 and 15.0-15.5 mm CSL).

Shell occupation in relation to shell shape

Shell occupation of C. violascens varied in relation to shell shape (Tab. 2). All hermits occupied seven categories of shell shape, including biconical, elongately conical, fusiform, globose, oval, pyriform and turban. Biconical shells (53.2%) were the most-occupied shell shape, followed by fusiform shells (19.1%). Males were found occupying all seven shapes of shells, while females occupied fewer categories of shell shapes (4 shapes). Non-ovigerous females were found occupying four categories of shell shape (biconical, elongately conical, fusiform and oval) and ovigerous females were found inhabiting two shapes (biconical and oval).

Table 2
Percentage of shell shape categories occupied by Coenobita violascens at Cape Panwa, Phuket Island, from January 2011 to March 2012. The numbers in parentheses after the percentage of shells inhabited are the numbers of crab individuals.

Shell shape	Males	Non-ovigerous females	Ovigerous females	Total
Biconical	38.5 (10)	73.7 (14)	50.0 (1)	53.2 (25)
Elongately conical	3.8 (1)	10.5 (2)	-	6.4 (3)
Fusiform	26.9 (7)	10.5 (2)	-	19.1 (9)
Globose	3.8 (1)	-	-	2.1 (1)
Oval	3.8 (1)	5.3 (1)	50.0 (1)	6.4 (3)
Pyriform	7.7 (2)	-	-	4.3 (2)
Turban	15.4 (4)	-	-	8.5 (4)

Shell occupation in relation to shell aperture shape

Shell occupation of C. violascens varied in relation to shape of shell aperture (Tab. 3). All C. violascens occupied four categories of shell aperture shape, including elongately ovate, irregular, ovate and round. Shells with ovate apertures (74.5%) were the most-occupied by all crabs. Males and non-ovigerous females were found occupying all four aperture shapes and ovigerous females were found inhabiting one aperture shape (ovate).

Table 3
Percentage of aperture shape categories of shells occupied by Coenobita violascens at Cape Panwa, Phuket Island, from January 2011 to March 2012. The numbers in parentheses after the percentage of shells inhabited are the numbers of crab individuals.

Aperture shape	Males	Non-ovigerous females	Ovigerous females	Total
Elongately ovate	11.5 (3)	10.5 (2)	-	10.6 (5)
Irregular	3.8 (1)	10.5 (2)	-	6.4 (3)
Ovate	73.1 (19)	73.7 (14)	100.0 (2)	74.5 (35)
Round	11.5 (3)	5.3 (1)	-	8.5 (4)

Shell occupation in relation to shell damage

All C. violascens occupied undamaged shells (46.8%) slightly fewer than damaged shells (53.2%). Males and non-ovigerous females were found occupying both damaged and undamaged shells and ovigerous females were found inhabiting only undamaged shells.

Shell occupation in relation to SIV/W ratio

The range of SIV/W values of shell inhabited by C. violascens was 0.120-4.604 (Tab. 1). According to the ratio of SIV/W, the most-occupied shell species at the study area was not the lightest shell species. Chicoreus brunneus, the most-occupied shell species, had a SIV/W ratio (mean ± SD) equal to 0.213 ± 0.056, but had a very low ranking SIV/W ratio (19^th out of 20 shell species). However, the lightest-occupied shell species was P. canaliculata with a SIV/W ratio equal to 4.604, but ranked 8^th in terms of occupation by C. violascens.

Relationship between crab and shell characteristics

The relationship between characters of C. violascens and occupied shells are shown in Tab. 4. The values of the determination coefficient (r²) from the regression analysis ranged between 0.62 and 0.93. Strong correlations were observed between characters of hermits and internal volume and aperture width of occupied shells (r² > 0.91). Shell aperture width was the most correlated with hermit characters (r² > 0.92), whereas shell weight and aperture length were least correlated with characters of hermits (r² < 0.66), except for cephalothoracic shield width (r² = 0.83).

Table 4
The relationship between characters of hermit crab Coenobita violascens and the inhabited shells sampled represented by regression equations. r² = determination coefficient; CSL = cephalothoracic shield length; CSW = cephalothoracic shield width; CW = crab wet weight; MCL = major chela length; MCW = major chela width; SL = shell length; SW = shell width; WW = shell wet weight; SIV = shell internal volume; SAL = shell aperture length; SAW = shell aperture width; N = 47.

Relations	Y = aXb	r2
SL x CSL	SL = 8.105CSL0.807	0.74*
SL x CSW	SL = 11.057CSW0.745	0.77*
SL x CW	SL = 31.409CW0.274	0.77*
SL x MCL	SL = 7.028MCL0.738	0.74*
SL x MCW	SL = 8.905MCW0.701	0.74*
SW x CSL	SW = 4.471CSL0.854	0.79*
SW x CSW	SW = 4.675CSW0.974	0.83*
SW x CW	SW = 18.854CW0.285	0.80*
SW x MCL	SW = 3.841MCL0.781	0.79*
SW x MCW	SW = 4.98MCW0.738	0.78*
WW x CSL	WW = 0.158CSL1.834	0.63*
WW x CSW	WW = 0.154CSW2.273	0.83*
WW x CW	WW = 3.427CW0.621	0.66*
WW x MCL	WW = 0.116MCL1.67	0.63*
WW x MCW	WW = 0.202MCW1.577	0.62*
SIV x CSL	SIV = 0.021CSL2.412	0.91*
SIV x CSW	SIV = 0.047CSW2.325	0.93*
SIV x CW	SIV = 1.219CW0.803	0.93*
SIV x MCL	SIV = 0.013MCL2.227	0.92*
SIV x MCW	SIV = 0.028MCW2.093	0.92*
SAL x CSL	SAL = 2.771CSL0.879	0.62*
SAL x CSW	SAL = 3.248CSW0.849	0.83*
SAL x CW	SAL = 12.167CW0.293	0.63*
SAL x MCL	SAL = 2.334MCL0.81	0.63*
SAL x MCW	SAL = 3.095MCW0.759	0.62*
SAW x CSL	SAW = 1.138CSL1.037	0.93*
SAW x CSW	SAW = 1.397CSW1.087	0.92*
SAW x CW	SAW = 6.544CW0.343	0.93*
SAW x MCL	SAW = 0.947MCL0.948	0.93*
SAW x MCW	SAW = 1.286MCW0.899	0.93*

• *Statistically significant, p < 0.05

Discussion

Coenobita violascens was found sympatrically with C. rugosus and Coenobita brevimanus Dana, 1852 at the study site. The results from this study are the first record on shells occupation by C. violascens. This coenobitid species shows a tendency of occupying specific categories of shells in relation to shell species, shape and aperture shape. Coenobita violascens individuals probably occupy the shells of at least three different gastropod species during their lifetime. Moreover, other aspects of shell occupation by C. violascens compared to other congeneric species are also discussed.

Coenobita violascens was found occupying fewer shell species (n = 20) than sympatric C. rugosus (n = 63) studied by Bundhitwongrut et al. (2015). This probably implies that C. violascens possess more specific requirements or less plasticity of use of shell resources. At least, the evidence is that C. violascens were not found using shells of neritids of the genus Nerita Linnaeus, 1758 although these shell groups were usually encountered as living individuals and discarded shells in the study area, which were commonly occupied by sympatric C. rugosus in high numbers reported by Bundhitwongrut et al. (2015).

Coenobita violascens preferentially occupied shells of one gastropod species, as also noted earlier in other land hermit crabs (Sripathi et al., 1977; Abrams, 1978; Achituv and Ziskind, 1985; Guillen and Osorno, 1993; Walker, 1994; Barnes, 1999; Morrison and Spiller, 2006; Sallam et al., 2008; Laidre and Vermeij, 2012; Bundhitwongrut et al., 2015). The different proportions of occupied shell species may infer active behavior of C. violascens in shell selection (Sallam et al., 2008; Bundhitwongrut et al., 2015). This probably means C. violascens try to find the most appropriate shells available for them.

Different sized individuals occupied different shell species. It is possible that C. violascens at the study site inhabits the shells of at least three different gastropod species as they grow. For instance, the most-occupied shell species, Chicoreus brunneus, were inhabited by medium-sized individuals (6.5-12.0 mm). However, smaller individuals (2.5-6.5 mm) occupied other smaller-shell species (e.g. Clypeomorus batillariaeformis, Drupella rugosa), whereas larger individuals (> 12.0 mm) inhabited other larger species [e.g. Chicoreus ramosus (Linnaeus, 1758)]. This inference is similar to the previous studies on Coenobita clypeatus (Fabricius, 1787) by Morrison and Spiller (2006) and C. rugosus by Bundhitwongrut et al. (2015), in that these land hermit crab are required to use the shells of a few different gastropods during their lifetime. To preserve these hermit crabs, therefore, the conservation of shell diversity is necessary because these hermits need different sizes and types of shells to complete their life cycle (Bundhitwongrut et al., 2015).

Coenobita violascens occupied particular categories of shell and aperture shapes. Frequently occupied shell shapes were higher-spired shells, which were mid- and high-spired shells (e.g. biconical and fusiform shells). This pattern of shell shape use by C. violascens is similar to those of small Coenobita perlatus H. Milne Edwards, 1837 living on exposed sandy beach, reported by Willason and Page (1983), and Coenobita cavipes Stimpson, 1858 investigated by Barnes (1999). More available space inside high-spired shells retains water much better than that of low-spired shells, thereby providing more resistance to desiccation during exposure to thermal stress (Bertness, 1982; Willason and Page, 1983; Barnes, 1999). Conversely, C. rugosus at the study site more frequently occupied low-spired shells (Bundhitwongrut et al., 2015) due to its behavioral ecology as a burrowing species (Barnes, 1999). The most-occupied shell aperture shape by C. violascens at the study site was ovate aperture as previously reported in C. rugosus at the same location by Bundhitwongrut et al. (2015). This aperture shape may allow this land hermit crab to fully seal the aperture with the major chela to avoid desiccation like other coenobitid crabs (Szabo, 2012). Interestingly, there was no C. violascens found occupying shells with semicircular aperture. This aperture shape is the diagnostic character of intact neritid shells. This occurrence is relevant to that there was no occupation of neritid shells by C. violascens.

The proportions between damaged and undamaged shells occupied by C. violascens were not significantly different at the study site as previously reported in sympatric C. rugosus by Bundhitwongrut et al. (2015). However, most shells inhabited by C. violascens were in worn condition and had lost the columella (unpublished data) as previously recorded by Kinosita and Okajima (1968), Ball (1972), Sripathi et al. (1977), Laidre (2012), Szabo (2012) and Bundhitwongrut et al. (2015). The missing columella of occupied shells may be due to mechanical or chemical abrasion (Kinosita and Okajima, 1968), resulting in light-weight and more space inside shells available for hermit crabs. These shells may be used previously by other hermits over a period of many years (Ball, 1972; Abrams, 1978; Boneka et al., 1995). Moreover, available empty shells as limited resource were scant at the study site (Bundhitwongrut et al., 2015), as also recorded earlier in other locations (Ball, 1972; Morrison and Spiller, 2006; Laidre and Vermeij, 2012). Consequently, these old and worn shells may be the main shell resources, especially for adult hermit crabs as a result of shell facilitation rather than competition (Abrams, 1978).

According to the energy saving hypothesis proposed by Osorno et al. (1998), Chicoreus brunneus as the most occupied shell species by C. violascens in this study was not the lightest species. This finding is similar to shells inhabited by sympatric C. rugosus investigated by Bundhitwongrut et al. (2015). Although hermits occupying the lightest shell species available, P. canaliculata, might obtain some advantages such as saving energy and having more internal space, hermits are probably at risk because of the thin shell wall from potential predators, such as the rough red-eyed crab, Eriphia smithii MacLeay, 1838, which was often seen at the study site (Bundhitwongrut et al., 2014).

Morphological characters of inhabited shells and C. violascens were significantly correlated. This finding is similar to previous studies on other coenobitid crabs, including C. rugosus by Boneka et al. (1995) and Bundhitwongrut et al. (2015) as well as Coenobita scaevola (Forskål, 1775) by Sallam et al. (2008). These shell characters, especially internal volume and aperture width, seemingly comprise the main determinants for C. violascens shell occupation. The strong correlations between shell internal volume and hermit characteristics possibly means that internal volume is crucial for C. violascens in providing more space that may allow hermits to grow rapidly or retain more fertilized eggs during reproduction (Osorno et al., 1998). Moreover, spacious internal volume of inhabited shells provides more capacity for storing water inside to maintain body moisture that is very important for life on land (Wilde, 1973; Greenaway, 2003). Additionally, the strong relationship between shell aperture width and hermit characters possibly indicates that C. violascens can use the major chela and walking legs to effectively seal the aperture firmly when retreating into the shell, which provides more protection from desiccation and against predators (Ball, 1972; Abrams, 1978; Sanvicente-Anorve and Hermoso-Salazar, 2011).

The habitat type of this study area may have resulted in relatively small numbers of specimens of C. violascens in the samples because this coenobitid is mostly recorded from habitats related to mangrove and terrestrial areas near estuaries (Nakasone 1988; McLaughlin et al. 2007; Doi et al. 2016). The present study site is supralittoral sandy beach that is not the most preferred habitat of this species. Therefore, further study in its main habitat in estuarine areas is recommended. Furthermore, C. violascens probably has a more cryptic lifestyle than the most common species, C. rugosus, at the study site. The foraging period and other activities of C. violascens presumably occur at different times to reduce competition with other species. Consequently, other sampling methods may be more effective for collecting C. violascens in other habitats such as bait pitfall traps (Morrison and Spiller, 2006; Hsu and Soong, 2017).

Acknowledgements

The present study was financially supported by a Thai Government Science and Technology Scholarship of the National Science and Technology Development Agency (NSTDA), Ministry of Science and Technology of Thailand. I would like to thank PMBC and the staff for allowing me to use the facility for research throughout the study period. I wish to thank Miss Vararin Vongpanich (PMBC) for her help in checking recent scientific names of some gastropod shell species. My special thanks are given to Dr. Warren Y. Brockelman (BIOTEC) for constructive suggestions and grammatical review on the manuscript. I am deeply grateful to three anonymous reviewers, the associate editor and editor for their invaluable comments.

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Zoobank:

• Zoobank:

  http://zoobank.org/urn:lsid:zoobank.org:pub:F5B43091-3C78-44AD-9507-08EA128F959D

Publication Dates

• Publication in this collection
  2018

History

• Received
  23 June 2017
• Accepted
  13 Oct 2017