Gastropod shells recycled - an example from a rocky tidal flat in the northern Red Sea MARTIN ZUSCHIN AND WERNER E. PILLER

LETHAIA Zuschin, M. & Piller, W.E. 1997 06 15: Gastropod shells recycled - an example from a rocky tidal flat in the northern Red Sea. Lethaia, Vol. 30, pp. 127-134. Oslo. ISSN 0024-1164.

Gastropod recycling at a rocky intertidal flat in the Northern Bay of Safaga (Red Sea, Egypt) is a process of increasing encrustation, changing secondary inhabitants, and probably decreasing shell strength. Encrustation by coralline red algae starts in the living gastropods, with the aper- ture area staying free of epigrowth. The dead gastropod shells are colonized by hermit crabs, tend to be more heavily encrusted and show encrustation of the aperture. This justifies the description ‘pagurized’ and the conclusion that coralline red algae produce the same paguriza- tion features as predominantly suspension-feeding invertebrates. After the shells are aban- doned by inhabitants that carry them around, further growth of coralline algae leads to rhodo- liths, which are sometimes colonized by stomatopods. Secondary inhabitants therefore influence not only the taphocoenoses of gastropods but also the formation of rhodoliths. OGastropods, encrustation, secondary inhabitants, pagurization, rhodolith formation.

Martin Zuschin [nizu@pal.univie.ac.at] and Werner E. Piller [wep@pul.univie.ac.at], Institutfur Palaontologie, Universitat Wien, Geozentrum, Althanstra$e 14, A-1090 Wien, Austria; 19th November, 1996; revised 25th April, 1997.

Empty gastropod shells provide a habitat for a variety of secondary inhabitants (McLean 1983; Vermeij 1987; Walker 1990). Shells inhabited by hermit crabs are a well- known phenomenon, particularly for soft-sedimentary habitats (e.g., Stachowitsch 1980; Walker 1989), but also for hard substrates (e.g., Walker 1990, 1995; La Barbera & Merz 1992). Additionally, gastropod shells are a common substrate for various epi- and endobionts. Colonization sometimes occurs on living gastropods (e.g., Wells 1969; Palmer & Hancock 1973; Bottjer 1981), but preferentially on shells inhabited by hermit crabs.

Encrusting patterns on living gastropods and crab- inhabited shells are different. On the former the aperture, callus, columella, and siphonal canal are not colonized owing to the presence of the fleshy mantle (Wells 1969; Stachowitsch 1980; Walker 1988, 1990, 1992). Shells occupied by hermit crabs, however, have a range of dis- tinct features (e.g., encrustation in the aperture area) and are termedpagurized (Walker 1988, after Seilacher 1969); such shells can be recognized in the fossil record (e.g., Palmer & Hancock 1973; Walker 1988). Most described pagurization features, especially when massive, are pro- duced by suspension feeders (Walker 1992). Massive pagurization features have a record from the Jurassic; more subtle (non-massive) ones are considered to be con- servative from the Eocene to the present (Walker 1992).

On a rocky tidal flat in the Northern Bay of Safaga (Red Sea) (Fig. l ) , large numbers of gastropod shells occur, mostly of Cerithititii caeruleum. They sometimes show massive epigrowth of coralline red algae, which is present both on shells of living gastropods and on those with sec- ondary inhabitants, mostly hermit crabs. The indiscrimi- nate epigrowth of coralline algae provides an opportunity to compare (1) encrusting features between shells with living snails and secondary inhabitants, and (2) algal- encrusted shells with those overgrown by suspension- feeding invertebrates. Besides these variably encrusted gastropod shells, rhodoliths also occur which are sus- pected of being related to these gastropod encrustations.

Study area Within an integrated project in the Northern Safaga Bay (Red Sea, Egypt; Fig. l), bottom facies (Piller & Pervesler 1989), sediments (Piller & Mansour 1990; Piller 1994) and organisms with considerable fossilization potential were studied. These include foraminifera (Haunold et al. 1997), corals (Riegl & Piller 1997), coral-boring bivalves (Kleemann 1992), coralline algae (Piller & Rasser 1996; Rasser & Piller, in press), echinids (Nebelsick 1992), and molluscs (Zuschin & Piller, in press).

128 Mnrtirt Ztrschin d* Werner E. Piller LETHAIA 30 (1997)

Fig. I . Study area and sample location.

The Northern Bay of Safaga represents a shallow-water area with highly structured bottom topography reaching down to more than 50 m. The annual water temperature ranges between 2 1 and 29°C and salinity between 40 and 46%0, both without any obvious depth gradient because of complete water mixing. The tidal range is less than 1 m. Water energy is relatively weak, but a complex current pattern influences facies development (Piller & Pervesler 1989 ). Widespread rocky tidal flats are developed around the islands and along the main coast (Fig. 1); they repre- sent abrasion plains of fossil coral limestone.

Material and methods All quantitative and qualitative samples were taken dur- ing low tide in one afternoon in late May 1996 at a deep intertidal to shallow subtidal rocky substrate West of Tubya Al-Hamra (Fig. 1). This substrate exhibits a rugged surface with depressions and crevices and is covered with patches of ‘soft-algae’ (Fig. 2) .

Quantitative surface samples were taken at different sites of the rocky tidal flat using haphazard quadrats of 0.25 m?. Within each of seven quadrats, all shells and rhodoliths were collected. Additionally, non-quantitative

LETHAIA 30 (1997) Gastropod shells recycled 129

surface collections from the same area are used for this study. This qualitative sampling was carried out primarily to increase the number of massively encrusted shells.

The shells were taxonomically identified and those of Cerithium caeruleum were grouped into living gastropods and crab-inhabited shells. The amount of encrustation (slight or massive) and the condition of the aperture (clean or encrusted) of both groups were determined vis- ually. After weighting the proportions by observation numbers, the non-parametric Mann-Whitney U-test was performed on the amount of encrustation using the SPSS 6.1.3 program package (marketed by SPSS Inc., 1989- 1995). Thirty-one rhodoliths were cut in half using a rock-saw to identify their nucleus. Fig. 2. General setting of the rocky tidal flat in front of a vertical cliff

undercut by a notch at the western side of Tubya al-Hamra. Note patchy distribution of macroalgae and the mass occurrence of rhodoliths.

Results

The gastropod shells belong to six species, of which C. caeruleum is quantitatively by far the most important (Table 1 ) . In crab-inhabited shells, two species of pagu- rids are present, Calcinus latens (Randall 1840) and Cliba- narius signatus Heller 1861. Both C. cueruleurn and the two crabs are typically reported from intertidal to shallow subtidal hard substrates in the Red Sea (Lewinsohn 1969; Ayal & Safriel 1981; Taylor &Reid 1984; Houbrick 1992).

Regarding the quantitative samples EC-96- 17 to EC- 96-20, a total of 164 living and 45 crab-inhabited shells of C. caeruleum were recorded over a total area of 1.75 m’,

nevertheless a patchy distribution of both shell categories Fig. 3. Abundance and distribution of living gastropods and crab-inhab- This corresponds to a dense surface ‘Overing but ited shells of Cerithium caeruleum (arrow).

Table 1. Species composition and number of gastropod shells at the studied rocky intertidal flat. Columns in Roman denote living gastropods; columns in italics denote shells inhabited by hermit crabs.

Quantitative samples Qualitative sample EC-96-17 EC-96-18 EC-96-19 EC-96-20 Total EC-96-21

Cerithium cneruleunt 55 11 61 3 10 48 21 164 45 31 33 Drupella cornus 1 1 1 1 1 Muricodrupa fiscellum 1 1 0 1 Strombus sp. 1 0 1 Thaididae gen. et sp. indet. 3 3 0 Nassarius arcularia plicatus 1 0 1

Table 2. Number and density distribution of Cerithitrm caertrleum shells and rhodoliths for each studied quadrat.

Sample No.

Quantitative samples EC-96-17

EC-96-19 EC-96-20

Total

EC-96-18

Qualitative sample EC-96-21

Cerithiurn caeruleum Living Crab-inhabited

Sampledarea No. No./m’ No. No./m*

0.25 mr 61 244 3 12

1 m2 48 48 21 21

1.75 m2 164 128 45 29.25

0.25 m2 55 220 11 44

0.25 m’ 0 0 10 40

31 33

Rhodoliths

No. No./m’

0 0 2 8

187 748 25 25

214 195.3

36

LETHAIA 30 (1 997)

Tnblr 3. .Amount at encrustation 011 living and crab-inhabited shells ot CerIfhiio~i c m d e i i m .

Sample Nu. Living Slight encrust.

hldssiw encrust.

1 0 0 0 1 0.6 4

12.9

Crab-inhabited Slight Xlassive encrust. encrust.

1 1 0 3 0 8

19 41 4 91.1 8.9 70 I ? 60.6 39.4

7

>

[Fig. 3; Table 2 ). Rhodoliths occur almost exclusively as a mass occurrence in a very limited area (Figs. 2,4; Table 2) .

Shell encrustations are produced almost exclusively by coralline algae of only one species, Nropiiiolithori bras- siiri-jloridn (Harvey) Setchell & Mason 1943 (sensu Ver- heij 1994; = N. fosliei Heydrich 1897 of other authors). The rhodoliths are also built monospecifically by this species.

All of the collected gastropod shells are encrusted by coralline red algae. Based on a Mann-Ll'hitney C-test, the visual determination ofthe amount of encrustation shows a significant difference between living gastropods and crab-inhabited shells i n both the quantitative samples (EC-96-17-20) m d the qualitative sample (EC-96-21) (Table 3, Table 4) .

I n the quantitative samples, 8.9940 of the crab-inhabited Cerirliiuni shells are massively encrusted versus 0.6% of the living gastropods. In the qualitative sample. 39.-I0/o of the crab-inhabited shells are heavily encrusted versus 12.906 of the living gastropods. This difference between the quantitative and the qualitative material is due to a sampling bias towards heavily encrusted shells in the qualitative material.

Investigation of the aperture area shows striking differ- ences between the two shell categories: all of the crab- inhabited shells are encrusted in the aperture area (Fig. 5B), but none ofthe living gastropods are (Fig. 5A).

The 22 heavilv encrusted shells from the qualitative and quantitative samples were investigated with regard to abrasion features at the teleoconch due to dragging of the shell on the rocky bottom. Five living gastropods were

Fig -1. Atass occurrence otrhodoliths of N. brassica-]7orida and scattered pstropod shells in foreground (arrow).

considered to be heavily encrusted, four of which show distinct abrasion features. Of the 17 heavily encrusted crab-inhabited shells, 11 (64.7%) show a distinct 'pagurid facet' (after Walker 1988). These dragging features of crab-inhabited shells appeared to be larger and shifted slightly towards the apex compared to those of the living snails. However, the differences are not striking and the sample size is not large enough to allow a final conclusion.

Including both quantitative and qualitative material, a total of 250 rhodoliths was examined (Table 2). In 38 specimens, nuclei of gastropod shells were detected from surface observation (Fig. 5C). Of the remaining 212 rhodoliths, 31 (14.6%) were randomly chosen and cut; of these, 22 (71%) exhibit a gastropod shell or its remnants as a nucleus. Many of the cut rhodoliths show distinct asymmetrical growth (Fig. 6B), and 16 (51.6%) have an intact canal from the gastropod shell to the outer surface (Fig. 6A, B). The coralline-algal laminae bend distinctly inward along the margins of the canals. Three unidenti- fied stomatopod specimens were found nestling in rhodoliths.

The quantitative data on the cut rhodoliths are consid- ered to be minimum values. As observed in specimens cut in several planes, even if a shell nucleus is present a single cross section may fail to detect it because of its possible excentric position; the likelihood of cutting a canal is even lower.

Discussion

Presence o f encrustation. - All studied living gastropods show at least weak encrustation by coralline algae. This is in contrast to previous studies of encrustation of epizoites on living gastropods (e.g., Wells 1969; Bottjer 1981; Jones

LETHAIA 30 (1997) Gastropod shells recycled 13 1

Fig. 5. Different features and stages of encrustation. OA. Massively encrusted shell of living C. caernleurn, exhibiting no encrustations of the aperture area. Shell length 32 mm. OB. Massively encrusted crab-inhabited shell of C. caertileum, exhibiting encrustation of the aperture area. Shell length 31.5 mm. OC. N. brassica-florida rhodolith exhibiting a gastropod shell nucleus (arrow). Rhodolith length 38 mm.

Fig. 6. Cut rhodoliths with pagurized C. caeruleurn shells as nucleus. OA. The overgrown aperture margins and the opening to the surface (arrow) prove colonization by a secondary inhabitant (probably hermit crab). Rhodolith diameter 33 mm. OB. Asymmetric growth of coralline algae indicates a longer stable position of the rhodolith. Straight canal (arrow) is evidence for an inhabiting organism (probably a stomatopod) which did not transport the rhodolith, but used it as a stationary accommoda- tion. Rhodolith diameter 42 mm.

1984), in which algal encrustation was not reported. The epigrowth on living shells indicates that the hermit crabs take over shells that were already encrusted. A similar sequence is deduced empirically for bryozoan-encrusted shells in the French Jurassic (Palmer & Hancock 1973).

The degree of encrustation reflects the inhabitants: liv- ing snails inhabit slightly encrusted shells, while hermit crabs inhabit massively encrusted shells. This sequence is probably accompanied by decreasing shell strength due to a progressive loss of minerals and the accumulation of shell damage in hermit-crab inhabited shells (LaBarbera & Merz 1992), because secondary inhabitants are unable to repair breakage (Vermeij 1987). Experiments on a rocky intertidal flat show that crab-inhabited shells are damaged and abandoned by the crabs within nine months (unpublished data of Kuris, Carlton and Brody cited by Walker 1988 and Walker & Carlton 1995). Stachowitsch (1980) proposed a classification of hermit crab symbionts based on their role in strengthening or weakening the shell. For example, encrusting organisms may strengthen the shell, while bioeroders weaken it. He was the first to recognize that hermit crabs and their symbionts affect gastropod shell quality and longevity.

We suspect that the increasing weight of the heavily encrusted shell or its decreasing strength causes the her- mit crab to leave the shell. Further algal growth on the abandoned shell produces rhodoliths, which remain attractive for other inhabitants, e.g., stomatopods. The latter are only found in rhodoliths with shell nuclei and

132 Martin Ziischin & Werner E. PiIler LETHAIA 30 (1997)

were not observed to transport the rhodolith. This paral- lels the situation in the North Adriatic Sea, where Sta- chowitsch (1980, Fig. 11) observed the crab Piliirnnzis hirtelliis in snail shells abandoned by the hermit crab Pagiiristes oculatrrs. Recycling of a shell among many sec- ondary users is well known (McLean 1983), but stomato- pods as secondary inhabitants have never been described before (cf. McLean 1983; Vermeij 1987; Walker 1990).

Encrustation as indicator ofshell status. - Our results con- firm Walker’s (1992) conclusion that the amount of encrustation and the encrustation features around the aperture are both very well suited to distinguishing whether the gastropod was alive or whether shell was occupied by a hermit crab: many of those inhabited by hermit crabs but none of those of living gastropods show massive encrustations in the apertural area. Dragging fea- tures - a particular pagurid facet - are of limited value in our material, because living C. caerrileiini carry their shell with the long axis parallel to the bottom surface, as do hermit crabs. This produces similar abrasion features, which tend to be larger and slightly shift towards the apex on crab-inhabited shells (Fig. 5). However, distinct pagu- rid facets (e.g., Ehrenberg 1931; Palmer & Hancock 1973) are always due to a substantial change in shell orientation between the snail and the hermit crab.

The canals that cross the algal crusts from the shell to the outside show distinct features: the algal layers at the canal margin bend inward, proving that canal production was penecontemporaneous to algal growth. These canals are interpreted as being maintained by secondary inhab- itants. In fossil specimens, they indicate the former pres- ence of secondary inhabitants. Palmer & Hancock (1973) report similar features for massive encrusting bryozoans on pagurized gastropod shells.

Asymmetric algal growth (Fig. 6B) indicates a long sta- ble position for many rhodoliths. Some rhodoliths pre- serve evidence of a continuous colonization by secondary inhabitants (see above). Rather than transporting the rhodolith, however, these organisms used it as a station- ary accommodation ( Fig. 6A).

Transport. - The presence of C. cneriiletim and the two hermit crabs Calciniis latens and Clibanariiis signntiis at rocky intertidal environments throughout the Red Sea (Lewinsohn 1969; Ayal & Safriel 1981; Taylor & Reid 1984; Houbrick 1992) indicates that the shells stay in their original habitat after occupancy by the crabs, producing a paleontological bias [Walker 1989). The extremely patchy distribution of the rhodoliths is due to local hydrody- namic transport and accumulation.

Few empty shells were found in the study area, suggest- ing that empty shells are the limiting resource for hermit crab populations (compare Vance 1972; Kellogg 1976).

Pagiirizatiori features. - Most reported pagurization fea- tures are produced by invertebrates, typically suspension feeders (for a detailed review see Walker 1992). Subtle encrustation patterns of coralline red algae on crab- inhabited shells have been described from tropical, sub- tropical and temperate environments (e.g., Stachowitsch 1980; Walker 1988, 1990, 1992). There are several poten- tial explanations for the massive algal-encrustation and complete absence of suspension-feeding epizoites at the studied rocky tidal flat. One reason could be the generally low amount of nutrients (e.g., Reiss & Hottinger 1984) and poor productivity (Sheppard et al. 1992) in Red Sea waters, which favour the growth of photoautotrophic organisms. In contrast, massively encrusting suspension feeders are all described from more or less highly produc- tive areas (Vermeij 1987). Additionally, physical stress (high temperatures and high exposure to solar radiation) may affect the faunal composition of low latitude inter- tidal areas (Walker 1995). However, Neogoniolithon brtrssica-fZorida is apparently well adapted to this environ- ment, and the lack of competitive suspension feeders probably enables massive encrustations similar to those reported from invertebrates.

Benefits. - Protection is no doubt the primary function of a gastropod shell for secondary inhabitants (Vermeij 1987), but in intertidal habitats hermit crabs may prefer high-spired shells such as Cerithium because they hold more water and minimize thermal stress (Bertness 1981). Epifaunal encrustations are sometimes interpreted to provide protection or camouflage against would-be pred- ators, but larger epizoic growth decreases the mobility of both hermit crabs and gastropods (Wells 1969; Palmer & Hancock 1973; Stachowitsch 1979, 1980). A similar sce- nario of protection and camouflage versus movement- obstruction is also possible for shells encrusted with cor- alline red algae but remains speculative without addi- tional information. For suspension feeders, the mobility (Stachowitsch 1979) and the feeding and respiratory cur- rents generated by the hermit crab (Tomlinson 1969) are sources of water movements. In contrast, coralline red algae are independent of such food supply and are inter- preted to colonize for example the aperture area of crab- inhabited shells simply because it is vacant after the death of the gastropod. An advantage of colonizing gastropod or hermit-crab inhabited shells for coralline algae might be the relative stability of this substrate. Abrasion of car- bonate is considered to be high in this relatively high- energy, tidally influenced environment (Zuschin & Piller, in press), and free-living corallines will be frequently dis- turbed by water motion (compare Palmer & Hancock 1973; Stachowitsch 1980). The gastropod shells offer a suitable substrate for colonization; after death of the snail and abandonment by hermit crabs, the now free-living

LETHAIA 30 (1997) Gastropod shells recycled 133

coralline algae (as coating on the shells or as rhodoliths, sensu Steneck 1986) are stable enough for further growth.

Another aspect is the transported shell as a sediment- free substrate, which might favour the growth of various algae. In general, the slow-growing coralline red algae are well known for their competitive success in areas with high grazing pressure (e.g., Hay 1981; Freiwald 1993; Wehrmann et al. 1995), but grazers have not been observed at the study site. Other possible explanations for the success of coralline red algae are the anti-fouling effects of epithallial shedding (Keats et al. 1996) and the reduction of competitive diatoms and microalgae by the abundant algal-detritus feeding C. caeruleum (Taylor & Reid 1984; Houbrick 1992). On the other hand, many coralline red algae are known to require regular grazing to develop massive crusts (Steneck 1983, 1985). However, the ‘stability factor’ probably plays a more important role, as gastropod shells seem to be a preferred substrate for coralline red algae at the studied site.

Geological implications The fossilization potential of the described encrusting fea- tures is basically high because of the skeletal mineralogy of coralline red algae; this is indicated by the common occurrence of algal crusts and rhodoliths in the Cenozoic fossil record (Adey & Macintyre 1973; Steneck 1985). The aragonitic gastropod shells are usually dissolved when exposed to meteoric conditions, but encrusting red algae enable the formation of calcitic pseudomorphoses with considerable preservation potential. Arthropods in gen- eral and hermit crabs in particular have a very poor pres- ervation potential as body fossils (Hyden & Forest 1980; Plotnick 1986). Their presence in a fossil community, however, can easily be proved by the characteristic pagurization features (e.g., Walker 1992). The canals from the shells to the rhodolith surface also have a high fossilization potential and allow recognition of the former presence of additional secondary inhabitants, which used the rhodoliths as stationary accommodations.

A rocky tidal environment is very susceptible to disso- lution and abrasion, resulting in low preservation poten- tial (Boucot 1981). Crab-inhabited shells are significantly weaker than living gastropods (LaBarbera & Merz 1992) and are therefore even more vulnerable to destruction in this high-energy regime (Walker & Carlton 1995). Addi- tionally, the usually poor exposure of ancient rocky shores in the geologic record limits the access of paleon- tologists to preserved biotas (Johnson 1988). Therefore, the likelihood of preservation and discovery of rocky tidal organisms is probably higher if they have been trans- ported to surrounding shallow marine habitats. A fossil example from an environment with comparable low pres- ervation potential is known from a Late Miocene coral reef flat environment in Mallorca (Pomar et al. 1996):

numerous rhodoliths with pagurized gastropods (e.g., Conus sp.) as nuclei occur in protected depressions on the reef flat.

Conclusions Gastropod shells are reused after death of the gastropod by secondary inhabitants, for whom they provide protec- tion from both desiccation and predation. The shells also provide a stable substrate for encrusting red algae. Recy- cling ultimately results in the formation of rhodoliths because of the extended ecological lifespan of the shells. Encrusting patterns on the shells provide information on the former presence of secondary inhabitants. The exclu- sive occurrence of coralline red algae as encrusters rather than suspension-feeding organisms is due to the advan- tage of photoautotrophic organisms in the studied oligo- trophic subtropical environment and to physical stress of low-latitude intertidal areas. The fossilization potential of the encrusted shells and rhodoliths is high, especially if transport to surrounding shallow marine habitats occurs.

Acknowledgments.. -We thank M. Rasser (Vienna) and A.M. Mansour (Qena) for help with field work, P. Dworschak (Vienna) for the identi- fication of hermit crabs, R. Janssen (Frankfurt) for help with molluscs and J. Hohenegger (Vienna) for help with the statistical analysis. Thanks are due to M. Stachowitsch (Vienna) for fruitful discussions and R. Stan- ton (College Station, Texas) and S. Walker (Athens, Georgia) for their careful review of the manuscript. The study was performed within project P10715-GEO of the ‘Fonds zur Forderung der wissenschaftli- chen Forschung’ (FWF).

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