Shell Selection in the Hermit Crab Clibanarius signatus Heller, 1861 from the Larak Island in the Persian Gulf

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1 Journal of the Persian Gulf (Marine Science)/Vol. 6/No. 19/March 2015/07/21-28 Shell Selection in the Hermit Crab Clibanarius signatus Heller, 1861 from the Larak Island in the Persian Gulf Seyfabadi, Jafar 1 ; Zamani Jamshidi, Mohammad Mehdi 1 ; Mahvary, Alireza 2 ; Kheirabadi, Nabiallah 1* 1- Department of Marine Biology, Faculty of Marine Sciences, Tarbiat Modares University, Noor, Mazandaran Province, IR Iran 2- Marine Research Station, Hormuz Island, Hormozgan Province, IR Iran Received: October 2014 Accepted: February Journal of the Persian Gulf. All rights reserved. Abstract Shell selection indices of the dominant hermit crab Clibanarius signatus Heller, 1861, in the Larak Island were studied from September 2011 to June Among 739 sampled specimens, 41 different gastropod shell types were selected as shelters based on their abundance and local availability. A significant positive correlation (P<0/01) was found between the dimensions of the hermit crab, Clibanarius signatus and dimensions of the occupied gastropod shells. Keywords: Clibanarius signatus, Larak Island, Paguroidea, Shell selection behaviour 1. Introduction Hermit crabs which play an important role in the food chain, represent an important portion of many intertidal marine communities worldwide (Fransozo and Mantelatto, 1998). For this reason, many studies on various biological aspects of hermit crabs have recently been conducted worldwide, including systematic (Lemaitre, 2003; McLaughlin et al., 2010), reproduction (Scelzo et al., 2010), behavior (Billock and Dunbar, 2011), migration (Bell, 2009), physiology (Greenaway, 2003), and ecology (Laidre, 2011). Hermit crabs are decapod crustaceans that occupy empty gastropod shells to protect themselves from predation (Angel, 2000), osmotic pressure (Pechnik et al., 2001) and desication (Boride, 1999). Hermit crabs * nabi_kheirbadi@yahoo.com are mainly adapted to live on sandy and muddy substrates and coral regions, but also some species can survive on sandy substrates in low density (Hazlett, 1981). They have all types of feeding strategies including predation of smaller invertebrates, zooplanktonivorous, phytoplanktonivorous, deposited feeding, saprophyting and so on. Some kinds of fishes can prey hermit crabs especially at the high tide. Hermit crabs exist in tropical, subtropical and temperate oceans, but are absent from polar oceans because of their thermal adaptations (Hazlett, 1981). Studies on shell selection by hermit crabs have been conducted by many researchers (Fotheringham, 1976; Bertness, 1982; Blackstone, 1985; Hazlett, 1989, 1990, 1992; Sallam et al., 2008; Dominciano et al., 2009; Ismail, 2010). Several factors have been found to affect the shell selection by each hermit crab species, for 21

2 Seyfabadi et al / Shelll Selection in the t Hermit Crab, Clibanarius signatus example: availability of empty shells in the environment (Scully, 1979), size and shape of the shell (Blackstone, 1985; Koutsoubas et al., 1993) and gastropod shelll condition (McClintock, 1985). Hermit crabs in smalll shells have been found to be more vulnerable to predation (Hazlett, 1981) ), and lowered growth rates (Angel, 2000). Besides, heavy shells have negative influence on reproduction and growth (Bertness, 1981; Osorno, 1981) because of the high energy costs for locomotion. A few studies on utilizing of shells by hermit crabs have been conductedd in the Persian Gulf and the Gulf of Oman (Mirbagheri, 2010; ; Seyfabadi et al., 2013; Kheirabadi et al., 2015), but less on the Paguroids shell selection behavior in the Larak Island. This study was undertaken to invstigate the Larak Island hermit crabsshell selection behavior, taxonomy as well as the dimensions of the hermit crab and the occupied shells. In a survey on the hermit crabs of the t Larak Island, seven species s weree identified and Clibanarius signatus was found to be the dominant species along the intertidal zones of the island (Seyfabadi et al., 2013). 2. Materials andd Methods 2.1. Study Area The Larak Island covers an area aboutt 49 km 2 and is located in the southern coast of the Strait of Hormuz in the Persian P Gulff (26 51 N, E). Five stations in the intertidal region around the island weree selected for this investigation covering all the representative coastal c habitats (Fig.1,, Table 1). Intertidal region was furtherr divided vertically into high, mid and loww intertidal zones. Table 1: Location of sampling stations for hermit crab (Clibanarius signatus) in the Larak Island (Persian Gulf). Station name/(station number) Larak city/ (1) Larak Quay / (2) East coast/ (3) South coast/ (4) West coast/ (5) Latitude (N) N N N N N Longitude (E) E E E E E Station description Rocky and sandy shoress /Subtidal zone (coral reefs)/ Some covered by algae/city station s Rocky and sandy shores sandy shores/ Subtidal zone (coral reefs) r Sand and gravel shores sandy shores Fig. 1: Sampling stations in the Larak Island (Persian Gulf, Iran). 22

3 Journal of the Persian Gulf (Marine Science)/Vol. S 6/No. 19/March 2015/07/ Sampling and Surveying Specimens were collected between September 2011 and June 2012 from the intertidal sandy-rocky zones of the island using random quadrate (Wang et al., 2009). Also, hand picking was performed for some specimens that had selected the rare gastropod shells (Wang et al., 2009). Specimens weree placed in special plastic packets and preserved in 70% ethanoll and transported to the laboratory. Crabs were initially removed from their shells; the gastropod species weree identified using method of Bosch et al. (1995). Each hermit crab andd the occupied shell was measured to record the biometric quantities, which included the carapace (CL), shield (SL), cheliped (Ch.L) and cheliped width (Ch.W) for the hermit crabs and d shell (SL), shell width (SW), shell aperture (SAL), and shell aperture width (SAW) forr the occupied gastropod shells. Also, the weight of hermit crabs and the shells were measured. Furthermore, measurement of internal volume/weight (IV/W)) was based on the method of Osorno et al (1998). Measurement ts were carried out using a 1.0 mm Varnier caliper and weight was measured with a digital scale of o 0.1 g accuracy Statistical Analysis All statistical analyses were performed using SPSS Spearman correlation Test was applied to test the relation of o the crab biometric quantities and the shells biometric quantities. Degree of significance for all tests was set at p< Results Among 7399 sampled hermit crabs, the shells of 41 gastropod species were identified, majority of which belonged to Cerithium C caeraleum, Lunella coronate, Planaxis sulcatus, Conumurex persicus, Semiricinula konkanensis, Priotrochus kotschyi, Nassarius arcularia, Clypeomorus C persica, Thais savignyi, Conumurex sp., Nerita albicilla. Also, some of the occupied shells were only observed once (Fig. 2). Fig. 2: Diversity of occupied shell species by the hermit crab, Clibanarius signatus in thee Larak Island. 23

4 Seyfabadi et al / Shell Selection in the Hermit Crab, Clibanarius signatus Station 1 (Larak City) with 242 hermit crabs and Station 2 (Larak Quay) with 219 specimens and station 4 (South coast) with 38 specimen ranked the highest and the lowest number of hermit crab (Table 2). The average size of some biometric quantities of hermit crab C. signatus and their occupied shell is shown in Table 3. There was a significant positive correlation (P<0/01) between the dimensions of the hermit crab, Clibanarius signatus, with those of the gastropod shells, particularly with the shell, shell weight and the volume of shells (Table 4). Table 2: The number of hermit crabs (Clibanarius signatus) collected in five stations in the Larak Island (Persian Gulf). stations Total Clibanarius signatus Table 3. The biometric quantities (average size, weight and volume) of hermit crab C. signatus and their occupied shell in the intertidal zone of the Larak Island, Persian Gulf. (IV: Internal volume of shell. W: weight of shell). Biometric quantities Hermit weight Shield Cephalothorax Cheliped Cheliped width Shell Shell width Aperture Aperture width Shell weight Shell volume Average size, weight and volume 0.23±0.02 (g) 3.60±1.04 (mm) 6.29±1.81 (mm) 3.30±1.0 (mm) 1.70±0.49 (mm) 2.02±0.8 (mm) 1.36±0.21 (mm) 3.12±0.22 (mm) 6.80±1.13 (mm) 2.50±0.73 (g) 0.63±0.03 (ml) IV.W 0.26±0.02 Table 4: Correlation between the dimensions of the hermit crab, Clibanarius signatus with the dimensions of occupied shells. dimensions Shell weight Shell Shell width Aperture Aperture width Internal volume of shell Internal volume of shell/weight of shell Hermit crab weight 0.814** 0.642** 0.777** ** * ** ** Shield 0.808** 0.621** 0.813** ** ** ** ** Carapace Cheliped Cheliped width 0.824** 0.650** 0.811** ** ** ** ** 0.784** 0.633** 0.762** ** ** ** ** 0.800** 0.639** 0.790** ** ** ** ** *Correlation with significant degree 0.05 **Correlation with significant degree

5 Journal of the Persian Gulf (Marine Science)/Vol. 6/No. 19/March 2015/07/ Discussion The shells of 41 gastropod species were found to be occupied by the hermit crab, Clibanarius signatus. Majority of the occupied shells in the current study belonged to Cerithium caeraleum, corraborating findings by Ismail (2010), but Thais lacera was found to dominate the occupied shells along the coasts of Hormuz Island (Kheirabadi et al., 2015). The diversity of the occupied gastropod shells and correlation analysis between the dimensions of the hermit crab with those of different shells showed that the shells were selected based on their abundance and local availability. This result is similar to the earlier findings from the area (Moradmand and Sari, 2007; Mirbagheri, 2010; Kheirabadi et al., 2015). In contrast, Clibanarius virescens was found to mainly occupy two gastropod shells, and the most determining factor on shell selection of this crab was the type of shells and not the abundance or availability of shells (Nakin and Somers, 2007). Both abundance and dimensions of shells have been reported as the most important factors (Mantelatto and Garcia, 2000; Sallam et al., 2008). There was a significant positive correlation between the dimensions of the hermit crab, C. signatus with the dimensions of gastropod shells. It is concluded that C. signatus selects its shells with high accuracy. In this, study, a higher correlation was observed between the crab s dimensions with the shell, shell weight and the shell volume (Table 4); This contrasts higher correlation observed between crab s weight with the shell weight and internal volume of the shell by Dominciano et al., (2004). The higher correlation between the crab s dimensions with the shell width and aperture width (Table 4) are reliable indication that the shell width and aperture width were more important factors for shell selection than shell and aperture. The correlation among the various dimensions also revealed that the sampled shells were suitable for the hermit crabs biological sustenance as reported by Sallam et al., (2008) and Kheirabadi et al., (2015). This study confirms findings of other investigators on the selection of different shells (Moradmand and Sari, 2007; Mirbagheri, 2010; Ismail, 2010; Kheirabadi et al., 2015). Shell selection in the hermit crab, Clibanarius signatus from the Larak Island was mainly on the basis of abundance and local availability. Acknoledgements The authors express their gratitude to Prof. Fernando Mantelatto of Sao Paulo University, Dr. Mahmoud Ghasempouri and Mr. Abdulkhaled Khaleghi from Tarbiat Modares University for helping in several stages of this project. We also acknowledge the assistance received from Mr. Hassan Yousefi-Masoomabad, Mr. Hassan Rashed, Mr. Yaghoub Nickou and Mr. Y. Pooryousef during sampling as well as Zoological Museum, University of Tehran (ZUTC) for helping to confirm the identified species of the hermit crabs. This project was supported by Tarbiat Modares University, Faculty of Marine Science and Marine Environmental Research Station at Hormuz Island. References Angel J.E., Effects of shell fit on the biology of the hermit crab Pagurus longicarpus (Say). Journal of Experimental Marine Biology and Ecology. 243: Bell J.J., Hitching a ride on a hermit crab home: Movement of gastropod shells inhabited by hermit crabs. Estuarine, Coastal and Shelf Science. 85: Bertness M.D., Conflicting advantages in resource utilization: The hermit crab housing dilemma. The American Naturalist. 118: Bertness M.D., Shell utilization, predation pressure and thermal stress in Panamanian hermit crabs: an interoceanic comparison. Journal of 25

6 Seyfabadi et al / Shell Selection in the Hermit Crab, Clibanarius signatus Experimental Marine Biology and Ecology. 64: Billock W.L. and Dunbar S.G., Shell and food acquisition behaviours: evidence for contextual decision hierarchies in hermit crabs. Journal of Experimental Marine Biology and Ecology. 398: Blackstone N.W., Size, shell-living and carcinization in geographic populations of a hermit crab, Pagurus hirsutiusculus. Journal of Zoology. 217: Bosch D., Dance S.P., Moolenbeek R. and Oliver P.G., Seashells of Eastern Arabia. Motivate Publishing. 296P. Brodie R., Ontogeny of shell related behaviours and transition to land in the terrestrial hermit crab Coenobita compressus H. Milne Edwards. Journal of Experimental Marine Biology and Ecology. 241: Dominciano L.C. C., Sant'Annab B.S. and Turra A., Are the preference and selection patterns of hermit crabs for gastropod shells species- or sitespecific? Journal of Experimental Marine Biology and Ecology. 378: Fotheringham N., Effects of shell stress on the growth of hermit crabs. Journal of Experimental Marine Biology and Ecology. 23: Fransozo A. and Mantellato F.L., Population structure and reproductive period of the tropical hermit crab Calcinus tibicen (Decapoda, Diogenidae) in the Ubatuba Region, São Paulo, Brazil. Journal of Crustacean Biology. 18: Greenaway P., Terrestrial adaptations in the Anomura (Crustacea: Decapoda). Memoirs of Museum Victoria. 60: Hazlett B.A., The behavioural ecology of hermit crabs. Annual Review of Ecology, Evolution, and Systematics. 12: Hazlett B.A., Shell exchanges in the hermit crab Calcinus tibicen. Animal Behavior. 37: Hazlett B.A., Shell exchange in Hawaiian hermit crabs. University of Hawaii Press, Pacific Science. 44: Hazlett B.A., The effect of past experience on the size of shells selected by hermit crabs. Animal Behaviour. 44: Ismail T.G., Distribution and shell selection by two hermit crabs in different habitats on Egyptian Red Sea Coast. Acta Oecologica. 36: Kheirabadi N., Seyfabadi J., Owfi F. and Mahvary A., Effective factors on shell selection behavior in hermit crab Clibanarius signatus in the coasts of Hormuz Island. Journal of Fisheries. 8 (4): (In Persian) Koutsoubas D., Labadariou N. and Koukouras A., Gastropod shells inhabited by Anomura Decapoda in the North Aegean Sea. Biosystematics. 1: Laidre M.E., Ecological relations between hermit crabs and their shell-supplying gastropods: Constrained consumers. Journal of Experimental Marine Biology and Ecology. 397: Lemaitre R., A new genus and species of hermit crab (Crustacean: Anomura: Paguridae) from Taiwan. Memoirs of Museum Victoria. 60: Mantelatto F.L. and Garcia R.B., Shell utilization pattern of the hermit crab Calcinus tibicen (Diogenidae) from southern Brazil. Journal of Crustacean Biology. 20: McClintock T.S., Effects of shell condition and size upon the shell choice behaviour of a hermit crab. Journal of Experimental Marine Biology and Ecology. 88: McLaughlin P.A., Komai T., Lemaitre R. and Rahayu D.L., Annotated checklist of Anomuran Decapoda Crustaceans of the World (Exclusive of the Kiwaoidea and families Chirostylidae and Galatheidae of the Galatheoidea) Part I Lithodoidea, Lomisoidea and Paguroidea. The Raffles Bulletin of Zoology. 23: Mirbagheri Z., Density and Distribution of Hermit crabs in the Gulf of Chabahar. M.Sc thesis, Khoramshahr Marine Science and Technology University. Iran. 119 P. 26

7 Journal of the Persian Gulf (Marine Science)/Vol. 6/No. 19/March 2015/07/21-28 Moradmand M. and Sari, A., Littoral hermit crabs (Decapoda: Anomura: Paguroidea) from the Gulf of Oman, Iran. Iranian Journal of Animal Biosystematics. 3: Nakin M.D. V. and Somers, M.J., Shell availability and use by the hermit crab Clibanarius virescens along the eastern cape coast, south Africa. Acta Zoologica Academiae Scientiarum Hungaricae. 53: Osorno J.L., Fernández-Casillas L. and Rodríguez- Juárez C., Are hermit crabs looking for light and large shells? Evidence from natural and field induced shell exchanges. Journal of Experimental Marine Biology & Ecology. 222: Pechenik J.A., Hsieh J., Owara S., Wong P., Marshall D., Untersee S. and Li W., Factors selecting for avoidance of drilled shells by the hermit crab Pagurus longicarpus. Journal of Experimental Marine Biology & Ecology. 262: Sallam W.S., Mantelatto F.L. and Hanafy M.H., Shell utilization by the land hermit crab Coenobita scaevola (Anomura, Coenobitidae) from Wadi El-Gemal, Red Sea. Belgian Journal of Zoology. 138: Scelzo M.A., Fantucci M.Z. and Mantelatto F.L., Spermatophore and Gonopore Morphology of the Southwestern-Atlantic Hermit Crab Pagurus exilis (Benedict, 1892) (Anomura, Paguridae). Zoological Studies. 49: Scully E.P., The effects of gastropod shell availability and habitat characteristics on shell utilization by the intertidal hermit crab Pagurus longicarpus Say. Journal of Experimental Marine Biology & Ecology. 37: Seyfabadi J., Motazedi M., Khodabandeh S., Kheirabadi N. and Safaei M., Shell selection in the land hermit crab, Coenobita scaevola (Forskål, 1775) from the Larak Island, Persian Gulf, (Decapoda: Coenobitidae). Zoology in the Middle East. 59: Seyfabadi J., Zamani Jamshidi M.M. and Mahvary Habibabadi A., Littoral hermit crabs (Crustacea: Decapoda: Anomura) of the Larak Island, Persian Gulf, Iran. Iranian Journal of Animal Biosystematics. 9: Wang X., Li X., Li B. and Wang H., Summertime community structure of intertidal macrobenethos in Changdao Archipelago, Shandong Province, China. Oceanology and Limnology. 27: Seyfabadi et al / Shell Selection in the Hermit Crab, Clibanarius signatus Journal of the Persian Gulf (Marine Science)/Vol. 6/No. 19/March 2015/07/21-28 Journal of the Persian Gulf (Marine Science)/Vol. 6/No. 19/March 2015/07/

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