Chapter 18. Razorfish and scallops

CHAPTER 18. RAZOR FISH AND SCALLOPS

ALAN BUTLER

CSIRO Marine and Atmospheric Research, Hobart, Tasmania 7001. Email: [email protected]

Figure 1. Razorfish bicolor near seagrass, Posidonia sp. The individual in foreground shows some recent, rapid growth at the posterior margin of the shell and an epifauna mainly of serpulids but with a gastropod, a few bryozoans, and a small colony of a didemnid ascidian beginning to overgrow the bryozoans. The shell in the background is dead, may have been there for a decade, and has a well-developed epifauna, mainly of bryozoans with a couple of sponge colonies.

Introduction

This chapter outlines some ecological studies of bivalve molluscs in (GSV) waters. It is eclectic, not attempting to cover all studies of bivalves, but mainly those of several large species—the ‘razor fish’ Pinna bicolor, and the scallops Mimachlamys asperrima and Equichlamys bifrons—which are conspicuous, and have proven instructive not only for understanding the ecology of these sorts of (sessile filter-feeders, with broadcast spawning, external fertilisation and a long larval period), but of the dynamics of the Gulf ecosystem and of the relationships between species.

A vast amount has been written about the ecology of bivalves worldwide (e.g. Wilbur & Yonge 1964- 1966; Bayne 1976; Yonge & Thompson 1976; Purchon 1977; Wilbur 1983-1988; Suchanek 1985; Ludbrook & Gowlett-Holmes 1989; Beesley et al. 1998), and no attempt is made to summarise it here.

238 Chapter 18. Razorfish and scallops

Razor fish

‘Razor fish’ are bivalve molluscs, not fish. The —pen shells, fan shells, wing shells, and commonly known in (SA) as razor fish—is a tropical and subtropical family (Butler 1998), only a few species occurring in temperate zones. Two, Pinna bicolor Gmelin and the less common Atrina tasmanica (Tenison Woods), occur in Gulf St Vincent (GSV). I discuss only the former here, because we have very little information on the latter. Pinna bicolor thrives in the SA gulfs, but, like a number of other subtropical organisms (mangroves, blue swimmer crabs), is not found much further south. Razor fish have a triangular or fan-shaped shell, up to 45 cm long, and live with the pointed, anterior end buried in the sediment and attached by to stones and shell fragments, with the posterior gape at or above the surface of the sediment (Fig. 1). When they protrude above the surface, razor fish are quite conspicuous at low or to a diver in the subtidal. When the posterior margin is at sediment level, however, there is a risk of cutting your bare feet on the sharp edge of the shell—hence the name ‘razor fish’—this is not one of the ensid bivalves called ‘razor shells’ or ‘razor clams’ elsewhere.

Scallops

The family Pectinidae (scallops) are the familiar, disc-shaped, fairly symmetrical bivalves with a straight, usually “winged” hinge. Some are free-living, some attached by byssus either when young or throughout life, and some are cemented to a hard substratum or embedded in coral. Members of the family occur from shallow depths to 7 000 m and they extend from the equator to polar regions, though they are best represented in warmer waters. Most have separate sexes, and the free-living species are noted for swimming by clapping the valves with most of the opening sealed, and expelling water near the hinge—i.e., they swim by jet propulsion (Beesley et al. 1998).

Three species of scallops are (or were) common in the Gulf—the doughboy scallop Mimachlamys asperrima (Lamarck), the queen scallop Equichlamys bifrons (Lamarck), and Pecten fumatus Reeve. Pecten fumatus is the commercial scallop of southern Australia, and has been discussed by Olsen (1955) and Dix & Sjardin (1975). Another species of scallop (Mesoplepum tasmanicum) can be found beneath rocks, for example at Edithburgh Jetty. I discuss only the first two here.

Distribution

The distribution of Pinna bicolor in SA was described by Butler & Keough (1981), who reported that it is ‘patchy’ on large and small scales—they can be locally very abundant, but are also absent from apparently suitable sites, and within a site will be found in localised patches that change with time, apparently due in part to spatially patchy recruitment (Butler 1987). They are, however, widespread on sheltered shores or in deeper water (from a little above low-water down at least to 20 m). Within GSV, P. bicolor was recorded at many sites between 1964 and 1969 by Shepherd & Sprigg (1976). Their survey was revisited in 2000-2001 by Tanner (2005), who found Pinna at fewer sites. In particular the ‘Malleus-Pinna assemblage’ identified by Shepherd & Sprigg (1976) in the SE section of the Gulf was essentially missing in 2000-2001, only scattered individuals remaining. Pinna distribution remained relatively unchanged in the northern part of the Gulf.

The doughboy scallop, M. asperrima, is widespread in the Gulf. They live attached by byssus to hard substrata such as rock, jetty pilings and notably the shells of Pinna bicolor (Fig. 2). They are commonly found in tight aggregations of up to 50 individuals. Typically, each individual has a coating of sponge on the shell, discussed further below. M. asperrima is not entirely sessile; sequential photographs show that they move, partly by progressively re-attaching the byssus (as mussels do) but also by breaking the byssus and swimming, which they will do when disturbed. Given their frequent attachment to the shells of Pinna or to other hard surfaces that elevate them from the seafloor, and noting from Tanner (2005) that many areas formerly occupied by Pinna and Malleus had become bare sand, it seems possible that the distribution and abundance of M. asperrima have been reduced along with those of Pinna (above).

Queen scallops, E. bifrons, (Fig. 3) are medium-sized (up to 130 mm shell length), and found free-living on soft sediments at depths of 2-50 m. They will swim when disturbed, much more readily than M. asperrima. In many places, both species occur together. Equichlamys bifrons has been historically

239 Chapter 18. Razorfish and scallops widespread and abundant in the Gulf (Shepherd & Sprigg 1976) but its distribution and density seem to have been reduced in the past 30 years. Both Shepherd & Sprigg (1976) and Tanner (2005) refer only to ‘scallops’ but from my observations this must refer primarily to E. bifrons with an unknown but lesser proportion of P. fumatus. Tanner (2005) found that the abundance of scallops in the central eastern section of the Gulf had decreased markedly since Shepherd & Sprigg’s (1976) survey—from densities of 0.5-4 m-2 to densities far below 1 m-2. Only at a few locations near the western shore of the Gulf and one in the south-east were they still abundant.

The Ecology of Razor Fish

Pinnidae are unusual amongst bivalves and have some interesting adaptations. They have basically an ‘epifaunal’ bivalve design—like a mussel, adapted to living attached to a hard surface—but have adopted an ‘infaunal’ habit, living in soft sediment; this is associated with adaptations such as their unique mechanisms for clearing sediment from the mantle cavity (Butler 1998). Pinna bicolor is widely-distributed in the Indo- Pacific, from the equator to the latitude of southern Australia. Published work on its ecology comes from the warm temperate regions of southern Australia (Rosewater 1961; Shepherd & Sprigg 1976; Butler & Brewster 1979; Butler & Keough 1981; Butler 1998). It occurs in the Gulf from the intertidal to 20 m, but is locally patchy; typical densities are 2-5 m-2.

Clearly from our observations, Pinna must be understood as existing in metapopulations (i.e. patchy systems with more or less dispersal between patches; e.g. Sinclair 1988; Hanski 1999). In such a system the nature of the dispersal between patches is crucial to understanding the dynamics within any patch as well as the whole population system (see Kritzer & Sale 2006).

Pinna bicolor reaches sexual maturity by 1+ yr (Butler 1987). The sexes are separate and gonads mature seasonally (Butler & Keough 1981; Roberts 1984; Butler 1987). Pinna have external fertilisation—eggs and sperm are simply released into the water. For a spawning the chances of successful fertilisation must depend on the proximity of other Pinna spawning at the same time, as well as on other factors, especially water movement. This has been studied in scallops in SA (see below). We have no data on fertilisation success for Pinna, but it seems likely that a failure of fertilisation would become a significant problem when a population becomes sparse. They are commonly clumped (e.g. Fig. 4). This might be important in areas such as the SE section of the Gulf, where Tanner (2005) found the former ‘Malleus-Pinna assemblage’ had disappeared and that only few, scattered Pinna remained.

Following fertilisation, a veliger larva develops. It will presumably be denser than water and will sink unless it swims actively. Many Pinnidae, including P. bicolor, have teleplanic larvae, capable of being transported for long distances (Scheltema 1977; Scheltema & Williams 1983) but this does not imply that they always are; the patterns of currents, and larval behaviour, could limit the distance travelled.

In addition to dispersal itself, the feeding and mortality of larvae are important, and virtually unknown in Pinnidae. Food supply may be crucial for a -feeding larva and, in the of P. bicolor, nutrients are limited and plankton not generally very dense. There are, however, variations in plankton density and these may be important in determining the survival of larvae.

Thus, a combination of limited, irregular dispersal and variable larval survival may explain what we clearly do know for this species, namely that recruitment to local populations is highly variable (Butler & Keough 1981). Small juveniles are found in sand (the adult habitat), commonly in or near seagrass beds. Soon after settlement, the new benthic Pinna is extremely small and fragile. At settlement the postlarva is a little over 1 mm in length; even at 1-2 cm the shell is very fragile and the attachment weak. At this stage the animals are vulnerable to a range of risks, including those of being swallowed by deposit feeders such as holothurians, of being eaten by predators such as naticid gastropods (moon shells), octopods, asteroids (sea stars) and fish, and of being unable to feed effectively because of movement of the sediment, or (as for the planktonic larvae) because the supply of suspended food is too dilute. Water movement close to the sediment is slight even in a high- area. The nutrition of very small benthic Pinna is unknown.

240 Chapter 18. Razorfish and scallops

Figure 2. ( top left) Typically aggregated, sponge-coated Mimachlamys asperrima on piling, Edithburgh jetty.

Figure 3. (top right) Equichlamys bifrons.

Figure 4. (centre left) A cluster of adult Pinna bicolor showing recent growth at posterior shell margins, and typical epibiota. Predatory seastar Uniophora granifera in foreground.

Figure 5. (centre right) Blenny sheltering in dead shell of Pinna.

Figure 6. (above left) Scallop, Equichlamys bifrons, about to swim in response to the predatory gastropod Pleuroploca Australasia.

Figure 7. (above right) Mimachlamys asperrima amongst colonial ascidians, sponges and other sessile fauna on piling, Edithburgh jetty.

241 Chapter 18. Razorfish and scallops

We know most about the animal from juvenile through to adult stages. Survivors of the early benthic stages, beyond a shell length of about 2 cm, grow rapidly (Butler & Brewster 1979; Butler 1987), but they are typically about 10 cm in shell length before the posterior gape of the shell is significantly elevated above the sediment. After this stage, they can begin to adopt the adult ‘strategy’, below. The shell increases rapidly in length and thickens. Growth is indeterminate (i.e. growth slows, but does not stop with age), rapid when small and slow after 2 yr, and can be approximated by a seasonally adjusted von Bertalanffy growth curve (Butler & Brewster 1979; Roberts 1984; Butler 1987). This kind of curve of length plotted against age flattens out but never quite reaches a maximum length of ~ 45 cm, which is approached after 4-7 yr. Longevity is up to 18 yr, with the rate of mortality approximately constant after 2 yr (Butler 1987). Over a period of two or more years the animal becomes much less vulnerable to many of its enemies, although again we have limited data. For instance, Butler (1987) recorded no attacks by naticid gastropods on animals above 29.3 cm in length. Adults do harbour macroscopic commensals or parasites, the effect of which is unknown. We have seen none during extensive studies of Pinna in SA, but they are known in P. bicolor in the tropics (Hipeau-Jacquotte 1974; Butler 1987), and Hale (1927) records a species of shrimp, Anchistus inermis from “Pinna inermis” in GSV. (Pea crabs——which are perhaps named for being commensal in Pinna and certainly occur in them elsewhere, are recorded from scallops, but not Pinna in the Gulf—Styan 1991).

Other aspects that have been studied include the following. There is a tendency for shells to be oriented with the current at some sites (unpublished data). Shell morphology varies with age and perhaps between populations; the spines are variable, more pronounced in the young (Butler & Brewster 1979, Butler unpublished data). The animals and plants attached to the shell (epibiota; Figs 1, 4; Chapter 21 Fig. 3) have been recorded by Butler & Brewster (1979), Keough & Butler (1983), Butler (1991), and especially by Kay & Keough (1981), and Keough (1984 a,b). Keough used the epibiota of P. bicolor as a model system to study the ecology of patchy (Connell & Keough 1985—and see Chapter 21). One common member of the epibiota is the small abalone Haliotis cyclobates studied by Stevenson & Melville (1999). Pinna shells continue to be occupied by epibiota after death, when the interior of the shell also becomes available as a shelter for small crustaceans, fish (Fig. 5) and the blue-ringed octopus Hapalochlaena maculosa (Hoyle).

Like many filter-feeding molluscs, razor fish accumulate heavy metals. This, and the effects of heavy metals on the epifauna of Pinna and on other species, has been investigated in Spencer Gulf by Ward and colleagues (Ward & Young 1983, 1984; Ward et al. 1984, 1986) and more recently surveyed by Corbin & Wade (2004). Pinna has features that make it a useful ‘sentinel accumulator’—that is, the amount of cadmium, lead and zinc accumulated in its tissues can be clearly related to the in its environment. However, these heavy metals—in a complex interaction with sediment characteristics and other variables—were shown to affect different species of epifauna attached to Pinna in different ways.

Butler et al. (1993) discussed ‘tradeoffs’ in Pinna—raising more questions for future research than they could answer! They suggested that the cost of rapid growth when young, and rapid repair at any age, might be a reduction in the number of gametes produced (compared with other bivalves, Pinna show low gonad volume for their size). Further, the environmental conditions for Pinna are variable. There appear to be times when conditions are especially good for feeding by the adults, survival of larvae, or survival of newly settled juveniles, leading to a good recruitment which (because of the long adult life) supports the population for a long time by the ‘storage effect’ (Chesson 1984; Butler 1987). The relatively large (Yonge 1953) water transport and filtering structures of Pinna are arguably dimensioned for generally low densities of food in water (Jorgensen 1966, 1975). Pinna bicolor pumps actively both day and night, except when disturbed or when the tide is out, consistent with the hypothesis that food is not superabundant. The large posterior extension of the shell and mantle cavity in Pinna is essentially a pair of wide ‘siphons’, supported and protected by the shell and able to extend above the sediment and beyond the boundary layer (the water layer close to the sediment surface where flow is quite slow). This may enable the animal to maintain a fairly high pumping rate at low energetic cost, but carries the disadvantage that the mantle cavity is vulnerable to the entry of sediment. Pinna has specialised adaptations for cleaning both chambers of the mantle cavity (Yonge 1953; Butler 1998), but there must be some cost for these adaptations, and indeed Pinna is absent from areas of severe disturbance of the sediment, such as surf beaches, where only siphonate, infaunal bivalves occur. In GSV it is intertidal on the calmer western side but only subtidal off the wave-exposed beaches.

242 Chapter 18. Razorfish and scallops

The Ecology of Scallops

The ecology of scallops in the Gulf has been studied from two perspectives: firstly, the interactions between scallops, their predators, and the epizoic sponges on M. asperrima; secondly reproductive dynamics, especially the relationship between density and fertilization success, in E. bifrons.

It is obvious to the most casual observer that most doughboy scallops, M. asperrima, are covered with brightly coloured sponge (Fig. 2) whereas queen scallops, E. bifrons, are not (Figs 3, 6); they may have a few gastropods, serpulids, barnacles or red algae attached to the shell but are commonly fairly clean. Although both can swim (scallops swim by clapping the valves and expelling water near the hinge), E. bifrons does so much more readily when disturbed by a shadow, a knock, or by chemical wafting from a nearby starfish, and will do so more times than M. asperrima. The one shown in Figure 6 is about to swim, attempting to escape the predatory whelk Pleuroploca australasia (Perry). A cage experiment showed that M. asperrima with sponge coating was less vulnerable to predation by the sea-star Coscinasterias muricata Verrill than those without sponge, and about as vulnerable as free-swimming E. bifrons. The presence of sponge on the shell was also associated with differences in shell structure (Pitcher & Butler 1987). Small scallops are more vulnerable to predators than larger ones, but sponge cover is more important than size (Chernoff 1987). So, the sponge protects M. asperrima from predation, about as well as swimming protects E. bifrons. It may do this by its toxicity, by camouflage, or by inhibiting the adhesion of the tube feet of starfish. But is there an advantage for the sponge—is this a case of mutualism? This is still an open question. Both species (scallop and sponge) are safer if they are higher above the seabed—the scallop from predators and the sponge from abrasion (Chernoff 1987; Fig. 7). The sponge clearly gains a substrate on which to grow (a resource in short supply for sessile suspension feeders—see Chapter 21), and it gains transport. More than that, we are guessing. If this is a mutualism, it is not obligate—each partner can be found without the other. How do the scallops get their sponges in the first place? An experiment suggested that arrival of sponges by water-borne larvae is a rare event (Pitcher 1981). Scallops are gregarious, and newly-settled juveniles are often attached close to adults and tend to have sponge of the same species as that on nearby adults; so it seems likely that the vegetatively-growing sponge is simply transferred from one scallop to another by contact (the scallop shell has fine hooks).

The reproductive cycles of M. asperrima and E. bifrons were studied at Edithburgh and Largs Bay by Styan & Butler (2003a). The timing of gonad ripeness differed between sites and between species; broadly, E. bifrons spawns in late summer (but there may be several spawning events through summer), and M. asperrima in spring (but there may be a mid-winter spawning). Only one spawning event was directly observed. This was enough to tell us that scallops are not synchronous spawners—not all of them spawn at one time—and that spawning was spatially patchy, but it left many questions unanswered. In particular, it remains unclear how asynchronous spawning is within a local patch. This is important for fertilisation success.

Both E. bifrons and M. asperrima are dioecious—having separate male and female individuals—and both are free-spawners—eggs and sperm are released into the water, where fertilisation occurs to produce a veliger larva. The larvae have been described by Dix (1976) and Rose & Dix (1984). The question “how close must two free-spawning scallops be to achieve successful fertilization?” sounds disarmingly simple, but turns out to be very complicated. Spawning success obviously depends on spacing of individuals, the nature of water movement, and the concentrations of sperm and eggs in the water (Styan & Butler 2000). But then there are complications, such as egg size, the rates and timings at which different individuals release sperm and eggs (Styan & Butler 2003b), the likelihood of polyspermy—suggesting that an egg’s chance of encountering a sperm can be too good!—and whether all male/female combinations are viable (Styan 1998a). This fascinating story is too detailed to explain here, and not yet finished, but as a rough rule of thumb, males and females need to be within 50 cm of one another to overcome the dilution of gametes in the water, and thus to have a reasonable chance of fertilisation (Styan 1998b). Thus scallops at low density on the seafloor are effectively non-reproducing. This can lead to what ecologists call the Allee effect, where the growth rate of a population decreases at low density. It means that exploitation (e.g. fishing) or other damage to a population (e.g. by the effects of prawn trawling) can effectively destroy a population’s capacity to recover even though it may not take out all the animals. This may partly account for the notorious fluctuations of exploited scallop populations. Unless the animals are strongly aggregated, most of the

243 Chapter 18. Razorfish and scallops densities recorded by Tanner (2005) appear too low for reproductive success by this simple rule of thumb— perhaps the only viable scallop populations left in the Gulf are in a few sites near the east coast.

Some research has also been done on the parasites of scallops in SA. There are castrating trematodes that infect the gonads of scallops. The work of Hutson et al. (2004) suggests that at least two types or species of bucephalid trematodes infect all three main species of scallops in SA; their second intermediate, and definitive, hosts are probably fish but the species are not yet discovered. Andrews et al. (1988) showed that a larval nematode species found in all three species of scallops has Port Jackson sharks as definitive hosts.

Threats

Direct and indirect effects of fishing

The exploitation of bivalves, and its management, is too large and complex a subject to treat here but it must be noted that ‘fishing’ is a clear threat to razor fish and scallops in GSV. Pinna in particular, and scallops to some extent, appear to be committed to a life-history in which a relatively great proportion of the animal’s resources is devoted to maintaining adult survival and relatively little to reproduction. Recruitment is strong in embayments where, presumably, a high proportion of larvae are entrapped (e.g. P. bicolor in Streaky Bay, Keough & Butler unpublished observations), but otherwise it is weak and variable compared with other bivalves in the same locations at the same times (e.g. other pterioids, unpublished data). An important consequence is that human activities that shorten adult life cannot be compensated for by an immediate response of the population. Such a response has classically been assumed in fisheries management, and is supposed to arise because some kind of on recruitment is lifted by the removal of adults. There is no evidence for that in Pinna or scallops in SA. Both can readily become locally depleted by collection—many biologists, fishers and divers have observed this in the Gulf. Note, especially in the case of the long-lived Pinna, that exploitation will selectively remove those individuals that have grown large enough to be relatively invulnerable to other risks—the part of the population that provides the ‘storage effect’. Thus it is plausible that these species simply cannot adapt to an increase in adult mortality. One might suggest that any proposal to exploit such species must be accompanied by an effective hatchery and restocking program. This is being investigated in France for the large Mediterranean species Pinna nobilis (Butler et al. 1993; N.Vicente pers. comm.), which is apparently more valuable and more threatened than P. bicolor.

Tanner (2005) found that the ‘Malleus-Pinna assemblage’ identified by Shepherd & Sprigg (1976) in the SE section of the Gulf was essentially missing in 2000-2001. As Tanner points out, this represents a significant change for species that depend on the complex habitat-forming structures provided by Pinna and Malleus (the ‘hammer oyster’, another pterioid—Butler 1998). Tanner’s findings suggested that this massive change to the nature of assemblages on the seafloor is accounted for by prawn trawling. Research in the Gulf (Drabsch et al. 2001) and the northern Great Barrier (Poiner et al. 1998) has shown that trawling can have only minor effects, particularly on “infauna” (animals living buried within the sediment). However, this depends on the gear used and the frequency of trawling, and effects are likely to be harmful for species like Pinna and Malleus which are not truly “infauna”—they are secondary soft-sediment dwellers, having “epifaunal” body-plans. They protrude from the sediment and the shell readily breaks when struck. Although practices have now changed, bottom-contact trawling can hardly be benign for animals like Pinna and Malleus whose life-history strategy (above) arguably depends on their long adult life. Coupled with the effect of low density on reproductive success (discussed above for scallops, but likely to apply in a similar way to Pinna), this suggests that human activities that disturb the seafloor remain a significant threat for these species, and for those (such as M. asperrima and the abalone H. cyclobates) that are associated with them.

Discharges of pollutants

Other potential threats could include point-source discharges of pollutants, non-point (diffuse) discharges, sedimentation, collection, and the effects of introduced species. Point-source discharges do not seem to be a problem in GSV, barring the possibility of shipping accidents. Off the Adelaide beaches, the effects of sewage discharges have dramatically altered seagrass assemblages (see Chapter 11); Pinna and scallops are

244 Chapter 18. Razorfish and scallops still present in de-vegetated areas, and we have no data to tell us whether the outfalls have influenced their dynamics.

Diffuse discharges include the possibility of influences from anti-fouling treatments. It is known that antifoulants like TBT (Nias et al. 1993) and copper (Johnston & Keough 2003) can influence when in high , but there is no evidence about the effects of such compounds on bivalves in the Gulf.

Introductions

In high densities, effects of introduced species on native bivalves are possible (e.g. Talman & Keough 2001). A potentially harmful introduction, the sabellid polychaete Sabella spallanzanii (Gmelin, 1791), has been recorded from a number of sites in GSV (see Chapter 17), and is present in the habitat of these bivalve species at least near the eastern shore of the Gulf (Styan & Strzelecki 2002). Clapin & Evans (1995) and Lemmens et al. (1996) argued that this species may have significant effects on soft-sediment fauna in WA, but its dynamics and potential ecological effects are not yet well understood. The findings of Holloway & Keough (2002a,b) on hard substrata in Victoria suggested that at high densities it may affect soft-sediment bivalves, especially by preventing larval settlement. O’Brien et al. (2006) studied the effects of S. spallanzanii on soft sediment assemblages in Victoria using real and artificial clumps of worm tubes. They found that it can affect the underlying soft-sediment macrofauna. It can reduce the abundance of larvae, including those of bivalves, reaching the seafloor, but its direct and indirect effects on post-colonisation processes might be more important. The impacts of this and other introduced species remain important subjects for research.

Conclusions

It is tempting to suggest that the environment of the Gulf is not unlike that of the surrounding land— nutrient-poor, and variable. We have in Gulf waters several species of bivalves that are beautifully adapted to this situation in ways that we now partially understand—in their anatomy and biomechanics, and in their population dynamics, which feature long life and fluctuating recruitment. In turn, they have interactions with other species—their predators, commensals and epibiota—that we only dimly understand so far. All of these aspects present many fascinating questions for further research. Yet these species, precisely because of the suite of attributes that allow them to persist in the variable environment of the Gulf, may not be able to sustain changes to the system, such as excessive collection or excessive physical disturbance.

Acknowledgements

Thanks to Jan Macpherson Butler and Rachel Harm for their help in the preparation of this chapter, to Craig Styan for photographs (Figs 1-8), and to Kirsten Benkendorff and Craig Styan for comments on the manuscript.

References Andrews, R.H., Beveridge, I., Adams, M. & Baverstock, P.R. (1988) Identification of life cycle stages of the nematode Echinocephalus overstreeti by allozyme electrophoresis. Journal of Helminthology 62, 153-157. Bayne, B.L. (1976) ‘Marine Mussels: Their Ecology and Physiology’ (Cambridge University Press, Cambridge). Beesley, P.L., Ross, G. J. B. & Wells, A. (1998) ‘: The Southern Synthesis. Fauna of Australia Volume 5 - 2 parts’ (CSIRO Publishing, Melbourne). Butler, A.J. (1987) Ecology of Pinna bicolor Gmelin (Mollusca: ) in Gulf St Vincent, South Australia: Density, reproductive cycle, recruitment, growth and mortality at three sites. Australian Journal of Marine and Freshwater Research 38, 743-69. Butler, A.J. (1991) Effect of patch size on communities of sessile invertebrates in Gulf St Vincent, South Australia. Journal of Experimental and Ecology 153, 255-280. Butler, A.J. (1998) Order Pterioida. In ‘Mollusca: The Southern Synthesis. Fauna of Australia Volume 5 – Part A)’. (Eds P.L. Beesley, G.J.B. Ross & A. Wells) pp 261-267 (CSIRO Publishing: Melbourne). Butler, A.J. & Brewster, F.J. (1979) Size distributions and growth of the fan-shell Pinna bicolor Gmelin (Mollusca: Eulamellibranchia) in South Australia. Australian Journal of Marine and Freshwater Research 30, 25-39. Butler, A.J. & Keough, M.J. (1981) Distribution of Pinna bicolor in South Australia, with observations on recruitment. Transactions of the Royal Society of South Australia 105, 29-39. Butler, A.J., Vicente, N. & de Gaulejac, B. (1993) Ecology of the pterioid bivalves Pinna bicolor Gmelin and Pinna nobilis L. 3, 37-45.

245 Chapter 18. Razorfish and scallops

Chernoff, H. (1987) Factors affecting mortality of the scallop Chlamys asperrima (Lamarck) and its epizoic sponges in South Australian waters. Journal of Experimental Marine Biology and Ecology 109, 155-171. Chesson, P.L. (1984) The storage effect in stochastic population models. Lecture Notes in Biomathematics 54, 76-89. Clapin, G. & Evans, D.R. (1995) ’The status of the introduced marine fanworm Sabella spallanzanii in Western Australia: a preliminary investigation’. Centre for Research on Introduced Marine Pests. Technical Report No 2. 34 pp. (CSIRO Division of Fisheries, Perth). Connell, J.H. & Keough, M.J. (1985) Disturbance and patch dynamics of subtidal marine animals on hard substrata. In ‘The Ecology of Natural Disturbance and Patch Dynamics’ (Eds S.T.A. Pickett & P.S. White) pp. 125-151 (Academic Press, Orlando). Corbin, T. & Wade, S. (2004) “Heavy metal concentrations in razorfish (Pinna bicolor) and sediments across northern Spencer Gulf” (Environment Protection Authority, Adelaide). Dix, T.G. (1976) Larvae of the queen scallop Equichlamys bifrons. Australian Journal of Maine and Freshwater Research 27, 399-403. Dix, T.G. & Sjardin, M.J (1975) Larvae of the commercial scallop, Pecten meridionalis, from Tasmania. Australian Journal of Marine and Freshwater Research 26, 109-112. Drabsch, S.L., Tanner, J.E., & Connell, S.D. (2001). Limited infaunal response to experimental trawling in previously trawled areas. ICES Journal of Marine Science 58, 1261-1271. Hanski, I. (1999) “Metapopulation ecology”. (Oxford University Press, Oxford). Hipeau-Jacquotte, R. (1974) Etude des crevettes Pontoniinae () associées aux mollusques Pinnidae à Tuléar (Madagascar). Archives de Zoologie expérimentale et générale 115, 359-386. Holloway, M.G. & Keough, M.J. (2002a) Effects of an introduced polychaete, Sabella spallanzanii, on the development of epifaunal assemblages. Marine Ecology Progress Series 236, 137-154. Holloway, M.G. & Keough, M.J. (2002b) An introduced polychaete affects larval abundance and recruitment of sessile invertebrates. Ecological Applications 12, 1803–1823. Hutson, K.S., Styan, C.A., Beveridge, I., Keough, M.J., Zhu, X., Abs EL-Osta, Y.G., & Gasser, R.B. (2004) Elucidating the ecology of bucephalid parasites using a mutation scanning approach. Molecular and Cellular Probes 18, 139- 146. Johnston, E.L. & Keough, M.J. (2003) Competition modifies the response of organisms to toxic disturbance. Marine Ecology Progress Series 251, 15-26. Jorgensen, C.B. (1966) ‘Biology of Suspension Feeding’. 357 pp. (Pergamon Press, Oxford). Jorgensen, C.B. (1975) Comparative physiology of suspension feeding. Annual Review of Physiology 37, 57-79. Kay, A.M. & Keough, M.J. (1981) Occupation of patches in the epifaunal communities on pier pilings and the bivalve Pinna bicolor at Edithburgh, South Australia. Oecologia (Berlin) 48, 123-130. Keough, M.J. (1984a) Effects of patch size on the abundance of sessile marine invertebrates. Ecology 65, 423-437. Keough, M.J. (1984b) The dynamics of the epifauna of Pinna bicolor: Interactions between recruitment, predation, and competition. Ecology 65, 677-688. Keough, M. J. & Butler, A. J. (1983) Temporal changes in species number in an assemblage of sessile marine invertebrates. Journal of Biogeography 10, 317-330. Kritzer, J.P. & Sale, P.F. (eds) (2006) “Marine Metapopulations”. (Academic Press, Amsterdam). Lemmens, J.W.T.J., Clapin, G., Lavery, P. & Cary, J. (1996) Filtering capacity of seagrass meadows and other habitats of Cockburn Sound, Western Australia. Marine Ecology Progess Series 143, 187-200. Ludbrook, N.H. & Gowlett-Holmes, K.L. (1989) Chapter 11: Chitons, gastropods and bivalves. In ‘Marine Invertebrates of Southern Australia Part II’ (Eds S.A. Shepherd & I.M. Thomas) pp. 504-724 (South Australian Government Printing Division, Adelaide). Nias, D.J., McKillup, S.C., & Edyvane, K.S. (1993) Imposex in Lepsiella vinosa from Southern Australia. Marine Pollution Bulletin 26, 380-384. O’Brien, A.L., Ross, D.J & Keough, M.J. (2006) Effects of Sabella spallanzanii physical structure on soft sediment macrofaunal assemblages. Marine & Freshwater Research 57(4), 363-371. Olsen, A.M. (1955) Underwater studies on the Tasmanian commercial scallop, Notovola meridionalis (Tate) (Lamellibranchiata, Pectinidae). Australian Journal of Marine and Freshwater Research 6, 392-409. Pitcher, C.R. (1981) ‘Some mutualistic aspects of the ecology of the scallop Chlamys asperrima (Lamarck) and its epizoic sponges. B. Sc. (Hons) thesis’. (University of Adelaide). Pitcher, C.R. & Butler, A.J. (1987) Predation by asteroids, escape response and morphometrics of scallops with epizootic sponges. Journal of Experimental Marine Biology and Ecology 112, 233-249. Poiner, I.R., & 10 co-authors (1998). ‘Final report on the effects of trawling in the Far Northern Section of the : 1991–1996’. CSIRO Division of Marine Research, Cleveland, Australia. Purchon, R. D. (1977) ‘The Biology of the Mollusca’. (Pergamon Press, New York). Roberts, D. (1984) A comparative study of Lasaea australis, Vulsella spongiarum, Pinna bicolor and Donacilla cuneata (Mollusca: Bivalvia) from Princess Royal Harbour, Western Australia. Journal of Molluscan Studies 50, 129-136. Rose, R.A. & Dix, T.G. (1984) Larval and juvenile development of the doughboy scallop Chlamys (Chlamys) asperrimus (Lamarck) (Mollusca: Pectinidae). Australian Journal of Marine and Freshwater Research 35, 315-323. Rosewater, J. (1961) The family Pinnidae in the Indo-Pacific. Indo-Pacific Mollusca 1, 175-217.

246 Chapter 18. Razorfish and scallops

Scheltema, R.S. (1977) Dispersal of marine invertebrate organisms: palaeobiogeographic and biostratigraphic implications. In ‘Concepts and Methods of Biostratigraphy’. (Eds E.G. Kauffman, & J.E. Hazel), pp. 73-108. (Dowden, Hutchinson & Ross Inc., Stroudsburg, Pennsylvania). Scheltema, R.S. & Williams, I.P. (1983) Long-distance dispersal of planktonic larvae and the biogeography and evolution of some Polynesian and western Pacific mollusks. Bulletin of Marine Science 33, 545-565. Shepherd, S.A & Sprigg, R.C. (1976) Substrate, sediments and subtidal ecology of Gulf St Vincent and Investigator Strait In ‘Natural History of the Adelaide Region’ (Eds C.R. Twidale, M.J. Tyler & B.P. Webb) pp. 161-174 (Royal Society of South Australia, Adelaide). Sinclair, M. (1988) ‘Marine Populations: an Essay on Population Regulation and Speciation’. (University of Washington Press, Seattle). Stevenson, J. & Melville, A. (1999) Settlement and recruitment of the abalone Haliotis cyclobates Péron, 1816. Marine and Freshwater Research 50, 229-234. Styan, C.A. (1991) ‘Sibling species and host specificity of pea crabs (Pinnotheridae: Decapoda) in South Australia’. B.Sc. Hons thesis. (University of Adelaide, Adelaide). Styan, C.A. (1998a) Polyspermy, egg size, and the fertilization kinetics of free-spawning marine invertebrates. American Naturalist. 152, 290-297. Styan, C.A. (1998b) ‘The reproductive ecology of the scallop, Chlamys bifrons, in South Australia’. Ph.D. thesis. (University of Adelaide, Adelaide). Styan, C.A. & Butler, A.J. (2000) Fitting fertilisation kinetics models for free-spawning marine invertebrates. Marine Biology 137, 943-951. Styan, C.A. & Butler, A.J. (2003a) Asynchronous patterns of reproduction for the sympatric scallops Chlamys bifrons and Chlamys asperrima (Bivalvia: Pectinidae) in South Australia. Marine and Freshwater Research 54, 77-86. Styan, C.A. & Butler, A.J. (2003b) Scallop size does not predict amount or rate of induced sperm release. Marine and Freshwater Behaviour and Physiology 36, 59-65. Styan, C.A. & Strzelecki, J. (2002) Small scale spatial distribution patterns and monitoring strategies for the introduced marine worm, Sabella spallanzanii (Polychaeta : Sabellidae). Transactions of the Royal Society of South Australia 126, 117-124. Suchanek, T.H. (1985) Mussels and their rôle in structuring rocky shore communities. In ‘The ecology of Rocky Coasts’ (Eds P.G. Moore & R. Seed, R.) pp. 70-96 (Hodder & Stoughton, London). Talman, S.G., & Keough, M.J. (2001). The impact of an exotic clam, Corbula gibba, on the commercial scallop, Pecten fumatus, in Port Phillip Bay, south-east Australia: evidence of resource-restricted growth in a subtidal environment. Marine Ecology Progress Series 221, 135-143. Tanner, J.E. (2005) Three decades of habitat change in Gulf St Vincent, South Australia. Transactions of the Royal Society of South Australia 129, 65-73. Ward, T.J., Correll, R.L. & Anderson, R.B. (1986) Distribution of cadmium, lead and zinc amongst the marine sediments, seagrass and fauna and the selection of sentinel accumulators near a lead smelter in South Australia. Australian Journal of Marine and Freshwater Research 37, 567–585. Ward, T.J, Warren, L.J. & Tiller, K.G. (1984) The distribution and effects of metals in the marine environment near a lead-zinc smelter, South Australia. In ‘Environmental Impacts of Smelters’ (Ed. J. Nriagu) pp.1-73 (John Wiley & Sons, New York). Ward T.J. & Young P.C. (1983) The depauperation of epifauna of Pinna bicolor near a lead smelter, Spencer Gulf, South Australia. Environmental Pollution (Ser A) 30, 293-308. Ward T.J. & Young P.C. (1984) Effects of metals and sediment particle size on the species composition of the epifauna of Pinna bicolor near a lead smelter, South Australia. Estuarine Coastal and Shelf Science 18, 79-85. Wilbur, K.M. (editor-in-chief) (1983-1988) “The Mollusca” (12 volumes, various editors) (Volumes 1-5, 7: Academic Press, New York) (Volumes 6, 8-10: Academic Press, Orlando) (Volumes 11-12: Academic Press, San Diego). Wilbur, K.M. & Yonge, C. M. (1964-66) “Physiology of Mollusca” - 2 Volumes (Academic Press, New York). Yonge, C.M. (1953) Form and habit in Pinna carnea Gmelin. Philosophical Transactions of the Royal Society of London Ser B. 237, 335-374. Yonge, C. M. & Thompson, T. E. (1976) ‘Living Marine Molluscs’. (Collins, London).

247