Shared Use of a Single Hermit Crab Sponge by Two Individual <I

BULLETIN OF MARINE SCIENCE, 69(3): 1239–1242, 2001

SHARED USE OF A SINGLE HERMIT CRAB SPONGE BY TWO INDIVIDUAL PAGURUS IMPRESSUS

Floyd Sandford

In the area of Dog Island, Florida, individuals of two hermit crab species, Pagurus impressus Benedict 1892 and Paguristes hummi Wass 1955, commonly use both sponge and shell shelters (Sandford, 1994, 1995; Sandford and Brown, 1997; Sandford and Kelly- Borges, 1997). Since 1992, studies of this hermit crab sponge-hermit crab association have been conducted every January in a N-facing bay at the Eastern end of Dog Island, the easternmost of a chain of barrier islands bounding the southern perimeter of Apalachicola Bay and St. George Sound in the northeastern Gulf of Mexico. These studies have involved daily shoreline surveys of the 960 m bay shoreline and of 3000 m of adjacent shoreline on either side of the bay. In addition 60 belt transect surveys of the bay’s intertidal zone from shoreline to within 6 m from shore were done. P. impressus prefer shell shelters (Sandford, 1995), and individuals in sponges often switch into available shells, abandoning the sponges. Many sponges, both empty and occupied, are found at shoreline on Dog Island, Florida, in January , beached by waves or stranded by receding tides, when juvenile P. impressus bring them close to shore (Sandford, 1994, 1995). Of 2092 hermit crab sponges collected and examined every January over a 10-yr period (1992–2001), 1017 (49%) were empty and 1075 (51%) were occupied by a hermit crab. Hermit crabs of other sympatric species (e.g., Pagurus pollicaris, Clibanarius vittatus) occasionally use sponge shelters, but in the 1074 occupied sponges, the crab occupant over 99.5% of the time was either P. impressus or P. hummi. P. hummi and P. impressus are typically sublittoral, but P. impressus moves into the intertidal zone in the winter months; 1027 (95.4%) of all 1074 crab-occupied sponges surveyed in January have con- tained individuals of P. impressus. Hermit crab sponges occur worldwide (see Sandford and Kelly-Borges, 1997). In North America they are known from only three locations, the Pacific Northwest (Kozloff, 1987), off the Carolina coasts (Wells et al., 1960), and in the Gulf of Mexico (Sandford and Kelly-Borges, 1997). The Carolina and Gulf sponges are the same species in disjunct populations. (Sandford and Kelly-Borges, 1997; Sandford, unpubl. data). The Florida hermit-crab sponge has a close morphological resemblance to sponges in the Family Suberitidae (Order Hadromerida). It was first erroneously named as Xestospongia halichondriodes by Wells (1969), identified as belonging to a new species, Spongosorites suberitoides, (Family Halichondriidae) by Diaz et al. (1993), and rediscribed under this name by Sandford and Kelly-Borges (1997). On the basis of molecular se- quencing of a 750 bp segment from the D3 region of the 28S rRNA gene in a range of halichondrid and hadromerid sponges McCormack and Kelly (in press) ascribed the sponge to a new genus Pseudospongosorites and transferred it to the hadromerid Family Suberitidae with all other hermit crab sponges reported worldwide. Hermit crab sponges typically grow on gastropod shells (Wells, 1969; Sandford, 1995; Sandford and Brown, 1997). As the sponge overgrows the shell, the hermit crab loses contact with the shell. It occupies a vestibule inside the sponge and maintains a sculpted opening to the outside (Fig. 1, sponge on the left). In the Dog Island area at least twenty

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Figure 1. Two Florida hermit-crab sponges, one (on left) with the usual single opening occupied by a juvenile Pagurus impressus, and the other (on right) with two openings, each occupied by a juvenile Pagurus impressus. different gastropod species are used by the sponge, but three—Cantharus cancellarius (Conrad, 1846), Nassarius acutus (Say, 1822), and Pyrgospira ostrearum Sterns (1872)— are the substrates found in 90% of dissected sponges (Sandford and Brown, 1997). Infrequently, a sponge with a single opening contains two embedded shells (Sandford and Brown, 1997). Of 2092 sponges collected since 1992, 953 (45.5%) have been dissected, and in five, two shells were found. In all cases the shells were deeply embedded in sponge tissue and not in contact with the hermit crab. How two shells come to be located in the same sponge is unknown but when two empty hermit crab sponges remain in contact with one another in a marine aquarium they can fuse to one another after several days (Sandford, pers. observ.). It seems unlikely that this would happen in nature. Of the 2092 sponges collected and examined to date, two had two discrete openings. The first hinted at the possibility of dual occupancy by two hermit crabs, but both openings were empty. In January of 1998 the second sponge with two openings was found, this one occupied by two juvenile P. impressus (Fig. 1, sponge on the right). Imafuku (1983) reported two hermit crabs, Pagurus filholi (De man, 1887) (as P. geminus McLaughlin, 1976), sharing the same shell. Imafuku reported three occurrences, the first in which both crabs occupied the same aperture, and the other two involving damaged shells where the second and smaller crab was occupying a hole in the shell. He suggested that such coexistence could be beneficial in situations of shell scarcity. This report documents, likely for the first time, the rare occurrence of two hermit crabs sharing the same hermit crab sponge shelter, each with a separate ‘natural’ opening. One can only speculate about the formation of a dual-occupied hermit crab sponge. In order to keep the sponge intact, it was x-rayed with a dental x-ray (Fig. 2). The results revealed a single Cantharus shell approx. 10 mm long lying adjacent to a large central NOTES 1241

Figure 2. x-ray of sponge, front view. The larger opening is on top and the outline of the central cavity occupied by the larger hermit crab is visible. To the left is the single embedded Cantharus cancellarius shell, its aperture positioned directly below the opening containing the smaller crab. cavity occupied by the body of the larger crab. The shell’s aperture is located near the sponge’s surface, directly below the opening occupied by the second and smaller crab. From this, a possible scenario for the formation of the sponge emerges. At one time the larger crab was the sole occupant of the sponge, with its abdomen located in the shell. As the shell became progressively overgrown by sponge tissue its relative position shifted. The shell became located nearby near the sponge’s surface, its aperture partly exposed and/or overgrown by only a thin layer of sponge. The crab lost contact with the shell and resided in the sponge cavity. The second, smaller hermit crab later took up occupancy of the shell. The shell is well overgrown by sponge, with both openings prominent and well sculpted, indicating that both crabs have occupied the sponge for an extended period of time. The position of both openings is such that both hermit crabs could contact the substrate and move together. The repeated happening in nature of the scenario as described is unlikely. Such dual occupancy is of neglible biological or ecological significance in resource use. Compared to those in shells, hermit crabs in sponges are less able to maneuver, more likely to be- come carried by currents, to be stranded by receding tides or washed ashore, and unable to bury in the substrate. The sharing of a single sponge by two hermit crabs is extremely rare and likely results in greater costs than benefits.

ACKNOWLEDGMENTS

I am grateful for the helpful comments of three anonymous reviewers, the advice of S. Sandford, and the assistance of G. Milden, D.D.S. 1242 BULLETIN OF MARINE SCIENCE, VOL. 69, NO. 3, 2001

LITERATURE CITED

Diaz, C., S. Pomponi and R. W. M. van Soest. 1993. A systematic revision of the central West Atlantic Halichondrida (Demospongiae, Porifera). Part III: Description of valid species. Scientia Marina 57(4): 283–306. Imafuku, M. 1983. Two hermit crabs inhabiting a single gastropod shell. J. Ethol. 1: 113–114. Kozloff, E. N. 1987. Marine Invertebrates of the Pacific Northwest. Univ. Wash. Press, Seattle and London. McCormack, G. and Kelly, M. (in press). New indications of the phylogenetic relationships of Spongosorites suberitoides Diaz et al. 1993 (Phylum Porifera, Class Demospongiae) as revealed by 28s rDNA. J. Nat. Hist. Sandford, F. and M. Kelly-Borges. 1997. Redescription of the hermit-crab sponge Spongosorites suberitoides Diaz, Pomponi and van Soest (Demospongiae: Halichondrida: Halichondriidae). J. Nat. Hist. 31: 315–328. ______and C. Brown. 1997. Gastropod shell substrates of the Florida hermit-crab sponge, Spongosorites suberitoides, from the Gulf of Mexico. Bull. Mar. Sci. 61: 215–223. ______. 1995. Shell/sponge switching by hermit crabs, Pagurus impressus. Invert. Biol. 14(1): 73–78. ______. 1994. The Florida hermit-crab sponge, a little known “mobile” sponge from the NE corner of the Gulf of Mexico, and its hermit crab associations. Pages 273–278 in R. W. M. Van Soest, T. Van Kempen and J. C. Braekman, eds. Sponges in space and time. Proc. IVth Int’l. Porifera Congr., Amsterdam, the Netherlands, 19–23 April 1993. Wells, H. W. 1969. Hydroid and sponge commensals of Cantharus cancellarius with a “false shell”. Nautilus 83(3): 93–102. ______, M. J. Wells and I. E. Gray. 1960. Marine sponges of North Carolina. J. Elisha Mitchell Soc. 76(2): 200–245

DATE SUBMITTED: December 18, 2000. DATE ACCEPTED: May 17, 2001.

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