Facies

, Volume 53, Issue 3, pp 319–327

Large gryphaeid oysters as habitats for numerous sclerobionts: a case study from the northern Red Sea

Authors

    • Department of PalaeontologyUniversity of Vienna
  • Christian Baal
    • Department of PalaeontologyUniversity of Vienna
Original Article

DOI: 10.1007/s10347-007-0110-8

Cite this article as:
Zuschin, M. & Baal, C. Facies (2007) 53: 319. doi:10.1007/s10347-007-0110-8

Abstract

The shell of a living specimen of the Indo-Pacific gryphaeid giant oyster Hyotissa hyotis was colonized by numerous encrusting, boring, nestling and baffling taxa which show characteristic distribution patterns. On the upper valve, sponge-induced bioerosion predominates. On the lower valve intergrowth of chamid bivalves and thick encrusting associations—consisting mostly of squamariacean and corallinacean red algae, acervulinid foraminifera, and scleractinian corals—provides numerous microhabitats for nestling arcid and mytilid bivalves as well as for encrusting bryozoans and serpulids. Such differences between exposed and cryptic surfaces are typical for many marine hard substrata and result from the long-term stable position of the oyster on the seafloor. The cryptic habitats support a species assemblage of crustose algae and foraminifera that, on exposed surfaces, would occur in much deeper water.

Keywords

Coral reefBioerosionEncrustationCryptic habitatsPalaeoecology

Introduction

Biogenic hard substrates include a broad variety of mineralized organic tissues (Taylor and Wilson 2003) which can be summarized as shellgrounds sensu Dodd and Stanton (1990). Such shell grounds are frequently colonized in modern and fossil marine environments (e.g., Stachowitsch 1980; Kidwell and Gyllenhal 1998; Zuschin et al. 1999). They can be infested during life or after death of the host, depending on whether the shell is external or internal and whether the life habit of the host is epifaunal or infaunal (Taylor and Wilson 2003). Hard substrata are frequently studied by palaeoecologists because encrusting and boring organisms retain their original positions on the substrate after fossilization and the problems of transport and assemblage mixing are minimized (Brett 1988). Distribution patterns of colonizing organisms, however, typically differ between exposed and cryptic surfaces of inorganic and biogenic marine hard substrata (e.g., Palmer and Fürsich 1974; Surlyk and Christensen 1974; Nebelsick et al. 1997; Richter et al. 2001). The presence of such differences can be used to infer life orientation of extinct fossil organisms if they were infested during their lifetime (e.g., Bordeaux and Brett 1990; Lescinsky 1995; Leighton 1998). Lack of such polarization, in contrast, is expected to occur on rolling hard substrata (Lee et al. 1997) or on frequently overturned substrata such as rhodoliths (Foster 2001).

Oysters are typical accessory components in fossil and Recent coral reefs (Crame 1986; Zuschin et al. 2001). The vast majority of such reef-associated bivalves are small (mostly in the size range of a few centimetres), but frequently colonized by sclerobionts (e.g., bryozoans, serpulids, crustose red algae; terminology after Taylor and Wilson 2002). The gryphaeid oyster Hyotissa hyotis (Linnaeus, 1758) occurs throughout the tropical and subtropical waters of the Indo-Pacific (Slack-Smith 1998; Zuschin and Oliver 2003a, b) and was recently introduced to the western Atlantic (Bieler et al. 2004). This species is exceptional in that it can reach a large size (up to several decimetres; Stenzel 1971). Although it is typically massively encrusted, its role as a habitat-providing structure for sclerobionts is unexplored. The colonizing organisms are differentiated into functional groups, including binding encrusters, destroyers, nestlers and bafflers (Fagerstrom 1987). The present study investigates the role of this large-sized bivalve as an ecosystem engineer (sensu Jones et al. 1994), which provides a substratum for the attachment of epibionts and refuges from predation, physical or physiological stress to other organisms (Gutiérrez et al. 2003).

Material and methods

One living specimen of H. hyotis was taken in May 1996 from a shallow-water site (6 m water depth) in the Northern Bay of Safaga (Fig. 1). The study site was dominated by the soft coral Sarcophyton sp., and the oyster was attached to a dead and degraded massive coral colony (Fig. 2). The total dry weight of the encrusted shell is 7,219 g; three quarters of the weight (5,450 g) are made up of the massively encrusted lower valve (Fig. 3). The upper (right) valve has an anterior-posterior length of 22 cm and a dorsal-ventral height of 27 cm. The corresponding values for the lower (left) valve are 22×29 cm. The size of the adductor muscle scar is 7.5×6 cm (Fig. 4a, b). The maximum thickness of the upper valve is ca. 4.5 cm, that of the lower valve (in the area of the ventral end of the ligament) exceeds 10 cm. The annual growth increments in the ligament area can be used to infer the ontogenetic age of oysters (Stenzel 1971) and suggest an age of more than 40 years for this specimen (Fig. 5). The sclerobiont infestation of this shell has been evaluated semi-quantitatively from visual inspection of the in situ shell at the seafloor, from investigations and photo documentation of the wet surface of the still living oyster immediately after collecting, and from the dry shell of the dead oyster. Encrusting associations have been studied in thin-sections. Of special interest are differences between the lower and upper valve regarding taxonomic composition and density of the sclerobionts.
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Fig. 1

Location map, general bathymetry of the study area (after Piller and Pervesler 1989), and collection site of H. hyotis in the southwest channel of the Northern Bay of Safaga

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Fig. 2

H. hyotis attached to a dead and degraded massive coral colony in an environment characterized by the soft coral Sarcophyton sp. Cb Chama brassica; S unidentified sponge; Sa Sarcophyton sp.; Xe Xenia sp

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Fig. 3

Ventral view of freshly collected wet shell, showing densely encrusted lower valve. Cb Chama brassica; Lp Lima paucicostata; S unidentified sponge; Tm juvenile Tridacna maxima. Anterior-posterior length of shell is 22 cm

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Fig. 4

Internal views of dry shell. a Upper (right) valve. b Lower (left) valve. Ams adductor muscle scar; C crustose algae; Cb Chama brassica; Cl clionid boreholes; M Montipora cf. informis; P Porites sp.; Se unidentified serpulid. Scale in centimetres

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Fig. 5

Cross-section of lower valve showing growth increments and dense incrustation. Acc accretion of encrusting associations; Cb Chama brassica; Cl clionid boreholes; L ligament area; Li lithophagine borehole; M myostracum of the adductor muscle scar. Note annual growth increments

Results

The main encrusting binders on the oyster are peyssonneliacean and corallinacean red algae, bivalves, serpulid worm tubes, and vermetid gastropod shells. The main destroyers are boring sponges and bivalves (Table 1). The upper and the lower valve of the oyster, however, are colonized by different taxa in different intensities. As a general feature, the upper valve shows only scattered and thin calcareous crusts. Bioerosion is a dominant feature of the upper valve and consists mainly of ubiquitous clionid boreholes and a single lithophagine borehole (Fig. 6a, b). In contrast, calcareous organisms densely encrust the lower valve (Fig. 7b). The thickness of these crusts is highly variable but exceeds 6 cm at some places (Figs. 5 and 7). As is obvious in the cross-section (Fig. 5), the ubiquitous clionid boreholes on the lower valve are mainly covered by encrusting epizoobionts, except for marginal parts of the shell (Fig. 7b). Lithophagine boreholes are more abundant than on the upper valve and preferentially occur in the encrusting associations (Fig. 8).
Table 1

Colonizing organisms assigned to functional groups on the upper and lower valve of the shell

 

Upper valve

Lower valve

Encrusting binders

 Red algae

  Peyssonnelia sp.

+++

  Sporolithon ptychoides

+++

 Foraminifera

  Acervulina inhaerens

+++

  Haddonia sp.

++

  Planorbulinoides cf. retinaculata

++

 Sponges

  Unidentified sponge colonies

+

+

 Corals

  Porites sp.

+

  Montipora cf. informis

+

++

  Blastomussa loyae

++

 Bryozoans

  Smittina sp.

+

 Serpulids

  Unidentified species

+

++

 Mollusks

  Juvenile Hyotissa

++

  Chama brassica

+

+++

  Unidentified vermetid gastropods

++

Destroyers (borers)

 Cyanophyceae

  Microborings

 

+

 Sponges

  Clionid traces (Entobia sp.)

+++

+

 Bivalves

  Lithophaga nigra

+

++

Nestlers

 Foraminifera

  Planorbulinella cf. larvata

+

  Sorites orbiculus

+

 Bivalves

  Barbatia cf. parva

+

  Septifer forsskali

+

+

  Lima paucicostata

++

  Ctenoides annulata

++

  Tridacna cf. maxima

+

Bafflers

 Corals

  Xenia sp.

+

  Sarcophyton sp.

+

− absent, + rare, ++ common, +++ abundant

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Fig. 6

External view of upper valve. a Freshly collected wet shell. b Dry shell. Note ubiquitous clionid boreholes on the dry shell. Cb Chama brassica, Li Lithophaga boring, M M. cf. informis, S unidentified sponges, Tm juvenile T. maxima, Ve unidentified vermetid gastropods. Scale in centimetres

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Fig. 7

External view of lower valve: a freshly collected wet shell; b dry shell. Cb Chama brassica; Lp Lima paucicostata; S unidentified sponges, Se serpulid worm tubes. Note dense calcareous crusts on dry shell. Scale in centimetres

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Fig. 8

Thin-section of encrusting associations of lower valve. Ai A. inhaerens, Li Lithophaga nigra bore hole, M M. cf. informis, P Peyssonnelia sp., Se serpulid worm tubes, Sm Smittina sp., Sp Sporolithon ptychoides

Vermetid gastropods and sponges are the main colonizers of the upper valve (Fig. 6). Calcareous crusts are very thin and rare, but filamentous green algae are abundant. Semisessile soritid and planorbulinellid foraminifera and calcareous tubes of polychaetes are found in low numbers, along with a single degraded valve of an encrusting chamid bivalve. A xeniid soft coral colony inhabited this valve (Figs. 2 and 3), and a small colony of the scleractinian coral Montipora sp. occurred on the dorsal part in association with a nestling mytilid bivalve (Septifer forskali). A juvenile T. maxima was byssally attached to the ventral part of the upper valve (Fig. 6a, b).

The lower valve, in contrast, is densely covered with chamid bivalves (Chama cf. brassica) and a thick, extensive layer of additional encrusters (Fig. 7a, b). The latter consist of squamariacean and corallinacean red algae, acervulinid foraminifera and scleractinian corals, with subordinate contributions by the cheilostome bryozoan Smittina sp., serpulids and small oysters (Fig. 8). The intergrowth of chamid bivalves and these other encrusters produced a highly irregular, rugged surface, which is densely covered with serpulid tubes and offers many microhabitats for crevice-dwelling limid bivalves (Lima paucicostata, Ctenoides annulata). Empty serpulid tubes are occasionally settled by the nestling mytilid bivalve Septifer forskali, and some of the lithophagine boreholes are colonized by the nestling arcid bivalve Barbatia cf. parva. Other epizoozoans on the lower valve include a few vermetid gastropods and several small, unidentified sponge colonies.

Discussion

Oysters, due to their epifaunal life habit and high preservation potential, are among the most frequently colonized molluscan substrata for sclerobionts in modern and ancient marine ecosystems (Taylor and Wilson 2003). Most oysters in fully marine environments, however, do not exceed a few centimetres in size. In the Northern Bay of Safaga, the comparatively few large oysters mainly occur in areas associated with localized high suspension load, for example where slowing longshore currents accumulate particulate organic matter from upstream seagrass beds and coral carpets (Riegl and Piller 1997). Such large Hyotissa shells are typically densely colonized by numerous zoobionts (this study; pl. 12, Fig. 2 in Slack-Smith 1998; Fig. 3 in Bieler et al. 2004, personal observations at the Seychelles, February 2002). It has been suggested that nutrient levels determine the degree of fouling in living molluscs (Voight and Walker 1995). However, shell size also strongly affects infestation in that larger shells typically support a higher diversity and density of fouling species than smaller shells (see Gutiérrez et al. 2003 for a review). Moreover, cemented oysters also provide a stable hard substratum for a long period of time, which increases the likelihood of colonization (for review see Taylor and Wilson 2003).

The quantitative difference among bioeroders and encrusters between the upper, exposed and lower, cryptic valve agrees with results from other studies on marine hard substrata (e.g., Nebelsick et al. 1997; Richter et al. 2001). This can be related to the stable position of the oyster on the seafloor, which yields different colonization patterns according to ecological preferences of the respective taxa. Illumination and water turbulence are probably the main factors controlling their distribution, followed by competition for space and food, and predation (Jackson and Winston 1982; Martindale 1992).

The main destroyers on the studied oyster shell are boring sponges and bivalves, which are generally among the most important bioeroders in Cenozoic coral reef environments (Hutchings 1986; Kleemann 1996; Perry 1998). Clionid boreholes strongly dominate on the upper and lower valve of Hyotissa, whereas lithophagine boreholes are more important on the lower valve. Apart from vermetids, binding encrusters were mostly found on the lower valve. Crusts of coralline red algae are dominant components of modern shallow-water coral reef environments (Hay 1981), where they typically form thick crusts on exposed surfaces (e.g., Martindale 1992). Such crusts are ubiquitous in Safaga (Rasser and Piller 1997), where they can be found on shells of living gastropods and hermit crab-inhabited shells and where they frequently overgrow dead molluscs (Zuschin and Piller 1997; Zuschin et al. 2000). The low abundance of calcareous crusts on the upper valve of the studied Hyotissa therefore requires explanation and could be due to massive infestation by bioeroding clionid sponges. A more likely explanation, however, is that the common filamentous green algae outcompeted crustose algae, which are more sensitive to sedimentation on exposed surfaces in this near-shore, turbid area (Fabricius and De’ath 2001).

Encrusting associations typically show a zonation of species in response to water turbulence and light, and strong taxonomic differences between exposed and cryptic habitats are therefore the norm (Riedl 1966; Martindale 1992). Filter feeders in the Northern Red Sea, for example, have a much higher biomass in cavities than on the reef surface (Richter et al. 2001). With respect to light penetration, cryptic habitats therefore support communities that would occur on exposed surfaces in much deeper water (Fagerstrom 1987). This is particularly true for the extensive encrusting associations on the lower valve of Hyotissa and three of their dominant components: Peyssonnelia sp., Sporolithon ptychoides, and A. inhaerens. On exposed surfaces, these taxa occur at depths below 20–40 m in Safaga (Rasser and Piller 1997); A. inhaerens was also reported from shallow-water cryptic habitats in the Northern Red Sea (Reiss and Hottinger 1984). Among binding scleractinian corals, Blastomussa loyae seems to prefer turbid water, shaded bottoms and cryptic conditions (Head 1978; Sheppard and Sheppard 1991; Veron 2000a). On the other hand, M. cf. informis, is a very common coral on reef slopes between 5 and 20 m depth, with no reported preference for cryptic habitats (Sheppard and Sheppard 1991; Veron 2000b). Chamid bivalves are among the most prominent encrusters of exposed dead hard substrata in the northern Red Sea (Zuschin et al. 2001; Zuschin and Stachowitsch 2007), but are even more abundant in cryptic, more sheltered habitats (personal observations). Other binders on the lower valve include cheilostome bryozoans and serpulids; although they were not identified down to species level, in coral reef environments, these taxa generally seem to prefer cryptic and semicryptic, downward-facing, sediment-free habitats (Martindale 1992). In contrast, solitary-loosely aggregated vermetid gastropods were mainly found on the upper valve. Such vermetid gastropods can be quantitatively important components of Recent intertidal to shallow subtidal coral reefs and are typically found on exposed surfaces (e.g., Hadfield et al. 1972; Zuschin et al. 2001) because they prefer more agitated water conditions for their suspension-feeding life habit (Hughes and Lewis 1974, Kappner et al. 2000).

Nestlers are represented almost exclusively by byssate pteriomorph bivalves and mostly preferred the microhabitats on the lower valve of H. hyotis: limid bivalves were found in crevices of the rugged surface, and small arcids and mytilids occurred in empty serpulid tubes and lithophagine boreholes. Such cryptic life habits are typical for these taxa (Hadfield 1976; Morton 1983; Zuschin and Oliver 2003a). In contrast, the zooxanthellate bivalve T. maxima is light-dependent (Goreau et al. 1973) and was therefore found on the upper valve of Hyotissa. Bafflers, finally, are only of very subordinate importance and include soft-bodied octocorals (Sarcophyton sp. and Xenia sp.) on the oyster’s upper surface.

Acknowledgements

Abbas Mansour, Werner Piller and Michael Rasser helped with fieldwork. Thanks are due to Karl Kleemann, Graham Oliver, Michael Rasser and Michael Stachowitsch for helpful discussions. Karl Kleemann and Norbert Vavra assisted with species identifications. The review of Franz T. Fürsich improved the mansuscript. Financial support was provided by FWF project P10715Geo to F.F. Steininger and by project H-140/2000 of the Hochschuljubiläumsstiftung der Stadt Wien to M. Zuschin.

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© Springer-Verlag 2007