CHAPTER 21. FAUNA OF JETTY PILES, ARTIFICIAL REEFS AND ... · FAUNA OF JETTY PILES, ARTIFICIAL REEFS AND BIOGENIC SURFACES ALAN BUTLER C.S.I.R.O. Marine Research, Hobart, Tasmania

Chapter 21. Fauna of jetties and artificial reefs

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CHAPTER 21. FAUNA OF JETTY PILES, ARTIFICIAL REEFS AND BIOGENIC SURFACES

ALAN BUTLER

C.S.I.R.O. Marine Research, Hobart, Tasmania 7001. Email: [email protected]

Figure 1. Piling of Edithburgh jetty showing sponges, ascidians and bryozoans. (CAS)

Introduction

This chapter is not a comprehensive description or natural history of the fauna of all jetties, artificial reefs and biogenic surfaces in Gulf St Vincent (GSV) and its approaches. It is about studies done on certain jetties, etc., in the Gulf, using them as experimental systems to increase our understanding of the larger ecosystem of which they are a part. I think of the fauna attached to pilings, artificial reefs and biogenic surfaces as a window on that larger system. Pilings have been convenient places to do experiments and make repeated observations. It has to be remembered, however, that the organisms we are studying on such surfaces are part of larger populations. They have dispersive larvae which may travel short to long distances with the currents; they have predators that move about; the assemblage on one jetty is thus connected to assemblages on other jetties and reefs. We can learn a great deal by observations and experiments at the small scale, but ultimately it only makes sense if we can successfully ‘scale up’—understand these habitats in the context of the system in which they are embedded. I say more, at the end, about this ‘scaling up’. Also, the jetties etc. are artificial—a type of substratum that was not present during the millions of years of evolution of these organisms—and are, in various respects, different from their ‘natural’ habitats. This does not mean we cannot usefully study them as a window on the whole system—and in any case, they are now part of the system—but it is important to remember that a jetty is not the same as a reef. Even though it may house many of the same species, their relative abundances, recruitment rates, growth rates, or behaviour may be


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different, although one can find similar faunal compositions where conditions are similar—e.g. steep rock walls, caves and overhangs.

I will talk mostly about assemblages on surfaces that are sufficiently deep or shaded to be dominated more by animals than by plants. I will concentrate on sessile or sedentary animals and say almost nothing about the motile organisms such as fishes associated with these structures although they are the main attraction for anglers and are the topic of many studies (e.g. Cappo 1995; Chapter 22). The animals attached to hard substrata such as jetty piles are predominantly suspension feeders or ‘filter-feeders’. They may pump water through their feeding structures (active suspension feeders, e.g., bivalves, sponges, ascidians) or largely depend on external currents to bring food to them (passive suspension feeders, e.g. gorgonian soft corals). This means that the fauna on pilings, rocky reefs etc. tends to vary according to the current regime. Some suspension feeders thrive in slow currents; some need a strong uni-directional or bi-directional current, but may still not be capable of surviving violent water movement; and others not only need plenty of water movement, but are so armoured against rough conditions that they find a niche where other species cannot survive. The relationship between sessile fauna and water movement is a fascinating and accessible topic for an observant underwater naturalist (Vogel 1983; Warner 1984; Denny 1988). There is some obvious variation between major taxonomic groups, and even within a group (e.g., ascidians) there are species adapted to different conditions.

Water movement as a source of food is not everything, however, for a sessile suspension feeder. Space to attach to the substratum is paramount, and there is intense competition for it. There is disturbance during rough weather, there are predators, and larvae arrive at different times and need to find space to settle and grow. The ecology of these assemblages involves a complex, fascinating interaction between all these factors (Butler 1995). It means that you find different assemblages on different jetties, wrecks, artificial reefs and biogenic substrata, and the reasons for the differences are not obvious.

Distribution

Assemblages of sessile suspension-feeders are found wherever there are hard substrata, natural or artificial. My former students and I have studied their dynamics at a number of jetties around the SA Gulfs, especially at Rapid Bay, Ardrossan, Port Giles, Edithburgh and Stenhouse Bay.

There is enormous taxonomic and functional diversity in these assemblages (Keough 1999). The predominant groups are usually sponges, ascidians, bryozoans, hydroids and corals but there are bivalves, polychaetes, crustaceans and so on (Fig. 1). Within a group, the species-diversity is often exceptionally high in southern Australia (Poore 1995 - e.g. ascidians, Kott 1997). Within the habitat-structure provided by these sessile organism, of course, there are many motile organisms (e.g. crabs, shrimps, seastars, and gastropods—Fig. 2).

The detailed composition of the fauna on pilings varies from place to place. Kay & Butler (1983) described apparently stable differences between the fauna of Rapid Bay and Edithburgh jetties, and these sites have remained distinctive long after the end of their study. The difference is not so much in the list of species present as in their relative dominance. Edithburgh could be loosely described as ‘sponge-dominated’ whilst at Rapid Bay the most conspicuous element is the hard coral Culicia sp. Butler (1986) confirmed these differences and documented different compositions at three other sites. The composition of the fauna also varies within one site, and a particular difference is that between large and small isolated patches. For example, Butler (1991) recorded differences between the fauna on pier pilings and on the shell of the razor fish Pinna bicolor (see Chapter 18) at three sites. Although the details differ from site to site, sponges occupy less of the space on Pinna than on pilings; bryozoans tend to occupy more on Pinna; serpulid tubeworms and barnacles are more abundant on Pinna. Another naturally occurring, patchy source of hard substrata is the shell of the scallop Chlamys asperrima. Unlike Pinna, however, C. asperrima is predominantly occupied by sponges (Pitcher & Butler 1987; Chernoff 1987; Chapter 18). These simple observations draw attention to the complex, interacting processes that determine the dynamics of sessile assemblages – for it is the ‘dynamics’, not a static description, that is interesting in these systems. A visitor sees little or no change on a single dive on a calm day, but these assemblages are constantly changing.


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Artificial reefs have been established in SA since the mid 1980s (Branden et al. 1994; McGlennon & Kinloch 1995; PIRSA 2005). SA has the largest number of officially endorsed artificial reefs in Australia (Pears & Williams 2005); with 19 listed by PIRSA (2005). Although artificial reefs have a wide range of (intended) uses worldwide (Pears & Williams 2005), in SA they have been intended mainly to enhance the experience of recreational fishers and divers, and so descriptions of their fauna tend to concentrate on fish, though some record information about algae and sessile invertebrates (Olsen et al. 1976; Reimers & Branden 1994). Reefs have been constructed from discarded tyres, but also by sinking derelict vessels. Data have seldom been recorded from these artificial reefs in a very systematic way, and there have been no experimental studies of their system-wide effects (Claudet & Pelletier 2004; Pears & Williams 2005). The evidence is that they do increase the number of fish available to recreational fishers, but there remains doubt as to whether they are increasing the biomass of fish in the system as a whole, or merely acting as ‘fish aggregating devices’. Despite some exceptions worldwide, it seems likely that in many cases they merely do the latter (see review of Pears & Williams 2005 with references to earlier reviews). This raises the possibility that they may actually increase pressure on fish stocks, and the construction of new artificial reefs is accordingly now discouraged by government. Our focus here, however, is on artificial reefs as habitats for sessile fauna.

Figure 2. The gastropod Thais orbita, itself a substratum for bryozoans, laying eggs on a piling of Edithburgh jetty. (MJK)

Anecdotally, the sessile, suspension-feeding fauna seems to be better developed on sunken vessels than on tyre reefs. Svane & Petersen (2001) reviewed studies of artificial reefs worldwide, and specifically attempted to view artificial reefs in the context of hard-substratum ecology, since most attention had previously been paid to fish. They asked whether artificial structures (artificial reefs, also jetties, etc.) actually increase the biomass of sessile assemblages in the system as a whole. Since such assemblages are generally space-limited, they may do so; and clearly a stable structure such as a jetty or a wreck does locally increase the production of sessile assemblages. Unfortunately, there are no studies of the dynamics of sessile fauna of artificial reefs in the SA Gulfs.

Experimental Studies of Sessile Assemblages in the Gulf

Ecology needs both observational studies (with time-series, not merely single snapshots) and experimental studies (Keough & Butler 1995) designed to test hypotheses that may explain the patterns seen in the observations. The fauna (and to a lesser extent, the flora) of jetty piles and biogenic hard substrata in the Gulf have been particularly valuable as an experimental system to understand the processes that control the ecology of hard-substratum assemblages.


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Here the neutral term assemblage is preferred, rather than community, or biocoenosis, in agreement with Svane & Petersen (2001), who use ‘assemblage’, to describe co-occurring organisms and reserve the term ‘community’ for assemblages where a higher level of organisation has been demonstrated. In practice it is not really possible to distinguish between an assemblage and a community, and our studies do show that there is strong interaction here.

Many of the organisms in these assemblages are modular—they are colonies of small, repeated units or modules (called zooids in ascidians and bryozoans, polyps in corals). They are distinguished from unitary organisms such as bivalve molluscs, barnacles, fish and people where one fertilised egg leads to one individual. In sponges, modules are less easy to define than in bryozoans or ascidians, and the sponge has more organisation within the colony than most other modular groups; but for various reasons it is best to think of sponges as modular organisms. Modular organisms replicate their modules asexually to grow the colony, so each colony is a clone. But they also produce larvae, usually sexually, which disperse and settle to begin new colonies. Colonies can take on a wide variety of shapes and this morphological flexibility is a feature that distinguishes modular from unitary animals. They may split or be damaged without being killed. Thus, a clone produced from an original settled larva may be very long-lived, but, unlike most unitary organisms, its size and shape are little guide to its age. Size, does, however, often matter in ecological interactions. Most of the modular organisms in our system, in addition to ‘budding’ to produce more modules, also produce swimming larvae. Some of them (e.g. sponges) have several kinds, some sexually and some asexually produced. Some unitary organisms, such as anemones, can also reproduce asexually and produce clones with some of the ecological attributes of modular organisms. So, the population dynamics of clonal organisms generally are an important part of the dynamics of hard-substratum assemblages (Hughes 1989).

These assemblages are rich in species. For example, Kay & Butler (1983) recorded 64 species on the Edithburgh and Rapid Bay jetties, and later work showed that this was an underestimate. The taxonomy of some groups is not well known, but even where it is well known, identification is often difficult in the field. For these reasons, much of our description and our studies of dynamics have been cast at the level of higher taxa (families, classes or phyla) and growth forms (e.g., encrusting sponges, mound-forming sponges; Connell & Keough 1985). This can be defended (Butler 1986; 1991)—higher taxa do have different body plans and different ecological characteristics from one another, different feeding modes, ways of growing, ways of defending themselves—and similarly growth forms make an ecological difference (Jackson 1979). The effects of pollution can be detected at the level of higher taxa (Warwick 1993; Warwick & Clarke 1993). However, Vanderklift et al. (1996) have shown that the reduction of taxonomic resolution in a study of the effects of a pollution gradient on infaunal assemblages does influence the interpretation of patterns in complex ways. And of course there are many ways in which the differences between genera and species really matter in ecological processes (Kareiva & Levin 2003). So, I discuss here a number of studies cast at these higher levels, but with the proviso that it will be necessary to move to finer levels of taxonomic resolution to answer certain questions. (Indeed, to resolve some problems, genetic variation below the species level is important.) Ecology is a multi-scale science, not only with regard to space and time, but also with regard to biological diversity.

Many variables may be important in determining the likelihood that an individual sessile animal or colony survives, grows and reproduces—and these variables will interact in complex ways to determine the dynamics of a whole assemblage. They can be classified in many ways. Here, I discuss processes under a rather heterogeneous series of headings that have wide currency in writings about hard-substratum ecology. I consider first the ‘stability’ of these assemblages, then the importance of dispersal and recruitment, competition, predation, chemical interactions between organisms, water movement, patch size and finally some comments on the idea of ecological ‘strategies’. Various aspects of these processes have been studied, eclectically, in GSV over the years; for readers who may wish to pursue the details, Table 1 lists the studies done at various sites, and the processes investigated.

Stable but Dynamic

Ecologists debate at length what we mean by ‘stability’ in ecological systems. Kay & Butler (1983) showed that the assemblages on two jetties (Edithburgh and Rapid Bay) were reasonably constant over time according to a technical criterion. This kind of situation has been observed in many other ecological systems;


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if you view the system on a very small scale you find constant change—organisms die, wave action damages them and clears space, larvae settle and grow, etc.—but on a larger scale (e.g., the whole jetty) the composition of the assemblage and the relative abundance of species stays about the same through time, and it remains different from other sites.

Table 1. Studies of processes controlling structure and dynamics of assemblages on subtidal, artificial or biogenic, hard substrata in the SA Gulfs. The table (modified after Keough & Butler 1995) indicates the location of each study, its scales of space and time, and the processes investigated. Only experimental ecological studies published in refereed journals and books are listed.

Location and habitat Type Time/

Space Process Reference

Edithburgh Pilings SM 10/1 SCPWQD

N

Kay & Keough 1981; Kay & Butler 1983; Davis 1988a,b, 1989a,b; Davis et al. 1991; Butler 1986, 1991; Keough 1983; Butler et al. 1996.

Edithburgh Bivalve shells S 3/1 SCPDQ Keough 1984a,b; Chernoff 1987;

Pitcher & Butler 1987. Gulf St Vincent Pilings S 1/5 SCDQ Butler 1986, 1991.

Rapid Bay Pilings S 10/1 SCPWQ Kay & Butler 1983;

Keough & Butler 1979 Gulf St Vincent Pilings, reef Asc 3/2 DCWQ Davis 1987, 1988a,b;

Davis & Butler 1989. Spencer Gulf Pilings S 13.5/1 SCDHQ Butler & Connolly 1995, 1999.

Key to table: Location and habitat: Pilings include other human-made structures; bivalve shells as substrata are Pinna bicolor or Chlamys asperrima. Type of organisms: S: sessile animals; M: motile animals; Asc: the ascidian Clavelina moluccensis. Time period: given in years if a pattern-descriptive study; Space: given as a number of separate locations (e.g. different jetties). Process: S, stability/scale; C, competition; D, dispersal and recruitment; H, human impacts; N, natural products, chemical ecology; terrigenous nutrient inputs; P, predation; W, water movement, wave action; Q, disturbance, patch dynamics.

One case of viewing the system on a small scale was Keough’s (1981) study of the epibiota of shells of razor fish (Pinna bicolor—Chapter 18 Figs 1,4; Fig. 3). The shells of Pinna had been chosen as a case study of an ‘island’ system―an assemblage occupying small, separate patches to which it was considered the theory of island biogeography (MacArthur & Wilson 1967) should apply. Keough & Butler (1983), using the same technical measure of constancy or equilibrium used by Kay & Butler (1983), found that the epibiota on Pinna shells could not be usefully considered as in equilibrium—they fluctuated widely. Dominance by strong competitors for space (especially colonial ascidians) was important in these fluctuations, and could be influenced by predation (by small fish) on the dominant competitors when newly settled. Kay & Keough (1981) compared the occupation of patches on Pinna with that of artificially-created patches of similar size on pilings at Edithburgh. On pilings, most reoccupation of patches was by the vegetative (asexual) growth of neighbouring colonies. Larval recruitment1 did contribute to the occupation of patches, but newly recruited individuals of unitary species (e.g. serpulid tubeworms) and small colonies of modular species tended to be overwhelmed by the growth of established neighbours. There was, however, a large amount of variation between patches—another illustration of the dynamic nature of these assemblages when viewed at fine scale.

1 The larvae of sessile animals have a complex and fascinating ecology (McEdward 1995). They disperse with the currents, settle on a new substratum, metamorphose into the sessile form, but are still very tiny and are vulnerable to a number of risks before surviving long enough to be observed by an investigator. At this point they are called ‘recruits’ (the precise definition of which varies between investigations) to the local population. Fascinating work on the behaviour and physiology of larvae of Gulf St Vincent animals, beyond the scope of this chapter, has been done by Havenhand and his students at Flinders University (e.g. Bolton & Havenhand 1988).


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Figure 3. Razorfish Pinna bicolor in sandy bottom near seagrasses. Pinna provides spatially isolated substrata for sessile animals, which colonise it by larval dispersal. This one has been colonised by serpulid tubeworms, perhaps by barnacles, and later by a bryozoan that has overgrown many of the worms. (CAS)

The differences between Edithburgh and Rapid Bay seemed consistent through time. Butler (1986) found differences between the assemblages on five piers in the Gulf and Investigator Strait, some of them not far apart (Stenhouse Bay, Edithburgh, Port Giles, Ardrossan and Rapid Bay). The patterns at Edithburgh and Rapid Bay had changed little since Kay & Butler (1983). So, there seems to be some stability through time and distinct spatial differences, at the scale of the ‘jetty’.

Dispersal & Recruitment

Recruitment in the fouling assemblages of GSV is highly variable. This is noted also for bivalves in Chapter 18 and we have observed it in sessile animals recruiting to test panels on all scales of space and time examined (Keough 1983; Butler 1986).

In contrast to intertidal systems, many subtidal systems are thought to have relatively localised recruitment (McShane et al. 1988; Sammarco & Andrews 1988; Butler & Keough 1990; Stoner 1992)— that is, the larvae do not travel far before settlement—but nevertheless they must be viewed only as semi-closed systems. For example, the ascidian Clavelina moluccensis (Figs 1, 4, 5) has short-distance larval dispersal (Davis & Butler 1989)—most larvae settle within metres of their parents. Most, but not all; in our investigations the ones that did not settle within about 15 m were lost. But during in vitro experiments, larvae of this species can remain viable for an hour or more (Butler & van Altena, unpublished observations), during which time the tidal current could carry them many hundreds of metres. It is no surprise, then, that recruitment in Clavelina is variable in space and time (Davis 1987, 1988a, 1989a,b). Clearly, when a new structure is submerged, it is eventually colonised, and not only by the species noted for their abundant and long-distance dispersal. When I dived there in 1988, C. moluccensis was observed on the wreck of the Zanoni in the middle of GSV but not on a barge sunk 1 nm away directly downstream in a strong tidal current. The Zanoni had been there for 120 years, the barge for about 2 years. Thus occasional long-distance dispersal may be a significant part of the way these systems function.

Variable dispersal and recruitment, in space, time, and between individuals within a species, is clearly a feature of the natural history of the Gulf fauna, and may be a key part of the mechanisms that facilitate coexistence amongst many competing, and ecologically fairly similar, species (Butler & Chesson 1990 - below).

Recruitment requires, as one of its steps, that the larva, once it has reached the developmental stage where it is competent to settle, encounters and recognises a suitable substratum. The process of recognition is complex, involving cues from biofilms and from previously settled animals as well as aspect, current speed, light intensity, etc., but some aspects form part of the burgeoning field of chemical ecology and natural products chemistry, which is mentioned below.

Competition

Competition, especially when it is thought of as primarily for food, is a seriously overworked idea in ecology (White 1993). For a sessile, suspension feeding animal, however, space for attachment to the


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substratum is a critical resource, with not enough to go around, and organisms compete for it. Unless there is strong physical disturbance (wave action, or simply instability of the substratum), most subtidal hard surfaces are crowded with sessile animals (and plants, where there is sufficient light).

Competition for space is a key process determining the composition of assemblages. It interacts strongly with recruitment (see above), predation and disturbance and the size and discreteness of patches of substratum (see below). Kay & Keough (1981) and Keough (1984b) studied the occupation of cleared patches on pilings at Edithburgh, and the epibiota of Pinna shells. They found that many of the modular species were competitively equivalent—who would win a given encounter was a random process, perhaps dependent on relative sizes. This has been found in other systems (e.g. Sebens 1985) and is potentially important in explaining the apparently ‘stable’ coexistence of so many species (see below). A related idea that has been invoked to explain coexistence is that of competitive ‘networks’ (e.g. Russ 1982). Sessile animals compete for space by various different mechanisms; some bryozoans have ‘bird-beak’ structures (avicularia; Bock 1982) which can nibble neighbours or settling larvae; sponges have a range of chemicals that are toxic to other species; some colonial ascidians grow faster than most other species and smother them. As a result we might expect the situation where Species A can beat Species B, Species B can beat Species C, but C can beat A; thus, there is no clear winner in the competition. Kay & Keough (1981) did not document any clear cases of such ‘networks’, but they did find a number of cases where A beats B, B beats C but A and C are about equivalent. Again, it means there are no clear winners.

Despite the ‘competitive equivalence’ of many species, higher taxa showed fairly consistent differences in their capacity for overgrowth, in the order ascidians>sponges>bryozoans>serpulids (Chapter 18 Fig. 4; Figs 1, 6, 7, 8). This, given that rates of larval recruitment tended to be in the opposite order, meant that there was a (statistically) predictable sequence of colonisation of patches—bryozoans and tubeworms would be likely to invade first but tunicates and sponges would exclude them and eventually dominate the patch. This led to some predictions about the effect of the size and isolation of a patch of substratum on its fauna (below).

The idea of competitive equivalence becomes particularly important when we recognise that these assemblages are spatially structured. A model (whether expressed in words or in mathematics) that assumes that any individual in the system can interact with any other is a misrepresentation of the system. The organisms are fixed to the substratum and, except by sending out dispersive propagules (usually larvae), can interact only with near neighbours. It turns out that models that explicitly represent this spatial structure have different outcomes and different stability properties from a model without spatial structure (Tilman & Kareiva 1997; Chesson 2000, 2003).

Predation

The effects of predators on assemblages of sessile organisms have been extensively studied in the intertidal zone and some of the same experimental approaches (using fences or other devices to exclude or enclose predators) have been used subtidally in GSV. Sea-stars are major predators in some intertidal situations but Keough & Butler (1979) found that, although they do feed on some common sessile species, sea-stars were unimportant in influencing the composition of the assemblage at Edithburgh. In the Gulf, the search for a gross effect of predation similar to that described for some intertidal systems (Paine 1994) and some other subtidal systems (Estes et al. 1978; Estes & Duggins 1995) has not been rewarding. There may be subtle effects, such as those of nudibranchs that specialise in feeding on sponges, but these have not been studied. Sea urchins are important predators, influencing the structure of rocky reef assemblages in other regions, but they are usually not abundant on pilings. In GSV, they do not seem to be important even on rocky reefs, where the common urchin, Heliocidaris erythrogramma, does not have the major effect on macro-algae recorded for Strongylocentrotus spp. in the north Pacific (Estes & Palmisano 1974) or for Centrostephanus rodgersii in SE Australia (Andrew & Underwood 1989; Hill et al. 2003).


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Figure 4. (left) The colonial ascidian Clavelina moluccensis (blue). (CAS)

Figure 5. (right) Colonial ascidians: Botrylloides leachii (yellow) in competition with Clavelina moluccensis (blue). (MJK)

Figure 6. (left) Space competition between didemind ascidians (grey, at right) and bryozoans Celleporaria sp. (grey and yellow, at left). (MJK)

Figure 7. (right) Sponges, ascidians and bryozoans competing for space, Stenhouse Bay jetty. (MJK)

Figure 8. Sponge (yellow) overgrowing the bryozoan Mucropetraliella sp. (red). (MJK)


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Chemical Interactions

Recruitment requires, as one of its steps, that the larva, once it has reached the developmental stage where it is competent to settle, encounters and recognises a suitable substratum. The process of recognition has attracted much attention, including some in GSV. There are cues that stimulate larvae to settle, sometimes associated with members of their own species (e.g. Burke 1986; Morse 1990). There are also cues that inhibit settlement. For a sessile animal that suffers competition for space and needs to keep its own feeding structures clear, there is an obvious potential disadvantage in having other species settle nearby or on the animal’s body surface. So it is not surprising that many sessile animals have means of discouraging larval settlement. Some of these are mechanical, or depend on flexibility of growth form, but many are chemical. Of course, chemical defences may not only function to discourage larval settlement; they may also discourage predation, serve as a weapon in competition between adult colonies, or discourage infection, and a given chemical may have more than one advantage (Paul 1992; Pawlik 1992). So, sessile animals are fertile ground in the search for natural products, which are both of ecological interest and of possible practical value e.g. anti-fouling for human-made structures, anti-viral, anti-bacterial, and anti-cancer agents (Davis et al. 1989).

Davis et al. (1991) observed that whilst 63% of the larvae of the ascidian Clavelina moluccensis (Figs 1, 4, 5) settled on their first contact with a substratum, the rest made up to 10 or more contacts with substratum prior to settlement. Certain sessile animals, especially sponges, were consistently rejected by settling larvae. Davis et al. (1991) showed that crude chemical extracts from two of these species deterred larval settlement. Butler et al. (1996) isolated a pure compound, lyso-Platelet Activating Factor, from one of these sponges, Crella incrustans, and showed that it inhibits settlement by C. moluccensis larvae. Of course, this leaves many questions unanswered about the ecological significance and evolution of the compound, and the initial observation—of settlement deterrence by a number of sessile species—will lead to continuing investigation both in chemistry and in field and experimental biology (e.g. van Altena & Miller 1989; van Altena et al. 1999).

Another sideline from the ecology of sessile, modular fauna concerns self-recognition processes. It has been known for some time that, in some species of colonial ascidians, there are genetically determined ‘fusion types’, rather like blood types in humans. Colonies of compatible genotypes will fuse on contact and become one integrated colony; yet other genotypes of the same species will not. This could have ecological implications, given that colony size is a key determinant of mortality. But the fusion and non-fusion of colonies raises a question; how do they know? How do these animals distinguish ‘self’ from ‘not-self’? Coombe (1983; Coombe et al. 1984) investigated this question in the ascidian Botrylloides leachii at Edithburgh, leading to insights into invertebrate, and vertebrate, cell-recognition processes.

Water Movement

Water movement is important to suspension feeding animals in that the rate of water movement and its turbulence are important to their feeding mechanisms—the relationship being different in different phyla and species (Vogel 1983; Warner 1984; Denny 1988). In the Gulf, an underwater naturalist can rapidly discern some of the effects of this—gorgonian fans where there are moderate, bidirectional movements due to wave surge; sponges and ascidians in calm areas but also (different species) prospering in areas of high current speed; and so on. There has been some investigation of the relationships between water movement and animal orientation and feeding in the Gulf. For example, the bivalve Pinna bicolor and the large solitary ascidian Phallusia obesa in areas of moderate, unidirectional or bidirectional currents, tend to be oriented so that their feeding currents may be augmented by the prevailing current (unpublished data; Jamieson 1988), but there are many unanswered questions about these processes.

More attention has been given to the importance of water movement—wave action—as a source of disturbance than as an aid to feeding. For example, Kay & Butler (1983) recorded that 10-20%―sometimes more—of the space on pilings at Edithburgh and Rapid Bay was occupied by a different species after every three months. Some of this turnover was due to animals being torn from the piling surface by wave action and then being replaced by overgrowth from neighbours, and to a lesser extent from larval settlement. This process may be less important on rocky reefs (Sebens 1985) or on pilings that are more commonly exposed to waves (as at Port Giles), where only robust and firmly attached organisms can survive, but damage by


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wave action is a well known component of the normal dynamics on natural substrata at least in the intertidal (Denny 1988; Paine 1994). In subtidal assemblages, where many of the dominant organisms are modular, wave action will often cause colony damage rather than death, and colonies will regenerate from surviving fragments (e.g. Davis 1988b). This is the basis for much of what I say below about the dynamics of these assemblages.

Patch Size

It is obvious that, as our ideas about processes influencing assemblages on hard substrata have developed, we have always had to think about interactions between different processes. Some of our ideas about those interactions were made testable by some propositions about the effect of the size of a patch and its isolation from other patches of hard substratum, on the sessile assemblage that is likely to develop on it.

The limited applicability of the equilibrium theory of island biogeography to Pinna viewed as small isolated patches of hard substratum (Keough & Butler 1983) is mentioned above. Kay & Butler (1983) found much turnover on jetty piles; so, we are talking of a highly dynamic system, in which animals come and go. When Kay & Keough (1981) compared the fauna on pilings (large patches) and on Pinna (small patches) at Edithburgh, they found big differences; for example sponges were much more abundant on pilings than on Pinna (Figs 1, 3; Chapter 18 Figs 1, 4). They could begin to explain this in terms of the relative competitive and dispersive abilities of different taxa, although the time-series was short and there were other variables to be considered. Keough (1984a) confirmed, as Kay & Keough (1981) had found, that patches cleared within the fauna on pilings were reoccupied mainly by vegetative overgrowth and that the eventual composition reflected the competitive abilities of the different taxa, regardless of patch size (Figs 9, 10). On isolated patches, however (not on the piling surface but surrounded by water), size was important. Larval colonization determined the occupancy of isolated patches (Fig. 11), and most of those larvae were bryozoans. So, small patches were generally occupied only by these poor competitors with superior larval colonisation. If a superior competitor (ascidian or sponge) did happen to arrive on the patch, it would dominate (this process is just beginning in Fig. 11). On larger patches, the likelihood of this occurring was greater, so a greater proportion of large patches was dominated by superior competitors. However, this simple model is not the whole story; bryozoans actually settled preferentially on small patches and ascidians on larger ones; these preferences could be interpreted as evolved responses to patch-size-dependent fitness. Keough (1984b) examined the dynamics on Pinna shells in more detail. Given that most were occupied by bryozoans and serpulids (Fig. 3; Chapter 18 Fig. 1), not by sponges and ascidians, most of the competitive interactions were between bryozoans, and there were many equivalent species-pairs; competitive interactions rarely resulted in exclusion. Predators rarely influence the outcomes of competition, an exception being that predation by small fish (juvenile leatherjackets, Monacanthidae) on newly-settled colonial ascidians (strong competitors) favoured the survival of the weak competitors (bryozoans and tubeworms)—all of this (the recruitment of ascidians and the number of fish present) varied through time. The overall result was that Pinna shells appeared to be a refuge for inferior competitors for space, fairly persistently through time, and that recruitment was the dominant process determining the composition of the assemblage on them.

All of this work was done at Edithburgh and, in discussing it, Keough (1981) noted that Edithburgh appeared to be a site of rather low recruitment of many species, compared with sites studied elsewhere. He discussed ways in which the relationship between patch size and assemblage composition should change with changes in recruitment rate and other variables. Without going into the details, if recruitment (particularly of good competitors) is higher, then patch size will make less difference. In this way a proposition about the effect of patch size became a way of testing our understanding, at the time, of a number of interactions within these assemblages. Butler (1986, 1991) set out to test the model. To do so, I had first to seek areas with different levels of recruitment (Butler 1986 estimated recruitment at five sites) and then choose sites (Edithburgh, Port Giles and Ardrossan) characterised over-simply as having low (Edithburgh & Port Giles) and high (Ardrossan) recruitment. At these chosen sites I compared the development of assemblages on (isolated) plates of different sizes and also extended the comparison between Pinna and pilings to more sites.


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Figure 9. (left) Clearing on piling at Edithburgh jetty, beginning to be recolonised by vegetative growth of surrounding colonies. (MJK)

Figure 10. (right) Clearing on piling at Edithburgh, recolonised entirely by vegetative growth from surrounding colonies. (MJK)

Figure 11. Experimental patch at Edithburgh jetty, isolated from overgrowth by being slightly raised from its surroundings. Colonised by larval settlement. (MJK)

In the comparison of Pinna and pilings, predictions were confirmed for some organisms that are ‘good competitors but poor recruiters’, such as colonial ascidians, bryozoans and the coral Culicia sp., and for ‘poor competitors that are good recruiters’ (bryozoans, tubeworms and barnacles), but not for sponges (the archetypal ‘good competitors but poor recruiters’). In the case of some ‘good competitors’, the proposed mechanism did not fully explain the results. In the plate experiment, predictions were confirmed for most but not all groups.

Over the time-scale of the experiment, it appears that pre-emption of space by very heavy recruitment of bryozoans at Ardrossan was important in determining the composition of the fauna. This was not envisaged in formulating the model—we expected that higher recruitment by organisms like bryozoans would give them an advantage on small and isolated patches but not that it would prevent recruitment by other species, even including good competitors, throughout the system.

This short-term experiment could only examine trends in the direction predicted by the model; so a different rate of approach to the final result would confound the experiment. Perhaps, with more time, the effect postulated in the model would have become clearer, but also it would have required very much greater resources to make a more effective test of the model underlying this work, which involved complex population structures and spatial, temporal and spatio-temporal environmental variation. Meanwhile, the study raises questions worthy of study at smaller scale; these concern the population structure and dynamics of particular species, and the responses of major animal groups to variations in food and physical conditions.

All models of nature are simplifications and the idea tested in this example is no exception. For example, the proposition that there are sites with consistently higher and lower recruitment across a number of ecologically different taxa was always at best an approximation to aid our thinking. What we really knew was that recruitment is highly variable (see above). Indeed, there is a theoretical argument that this variability, in itself, is part of the mechanism allowing a large number of competing and quite similar species to coexist (Butler & Chesson 1990; Chesson 2000), and recent work is developing ways of testing the importance of such mechanisms (Chesson 2003). Of the three kinds of variability important in such


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mechanisms—spatial, temporal and spatio-temporal—two were necessarily ignored in this study. Similarly, variation between organisms, at all levels from individual, through specific to phyletic, was glossed over in the groupings of ‘good competitors that are poor recruiters’, etc. We would need very large resources to test the model more effectively using the kinds of experiments reported here.

Although conducted in Spencer Gulf, not GSV, the study of Butler & Connolly (1995, 1999) at Port Bonython is worth mentioning. They used the development of the assemblage on the newly-constructed steel pier there to test the ideas outlined here. The pier was monitored for over six years and then revisited after 13.5 years. The GSV model led us to predict that the very large, black-painted steel pilings would first be colonised by ‘good recruiters’ (which tend to be ‘poor competitors’) but that, over time, ‘poor recruiters’ (good competitors) would eventually arrive and, having arrived, would steadily overgrow and displace the ‘poor competitors’. We might, thus, expect an initial dominance of the fauna by unitary animals such as serpulid tubeworms, barnacles and bivalve molluscs, but an eventual dominance by modular forms such as sponges, bryozoans and corals, with the poorer competitors still present but not very abundant, and only able to occupy small patches temporarily cleared by predation, senescence or disturbance. These predictions were not fulfilled after 6.5 years. Although over 50% of the piling surface was covered after 6 years by encrusting and mound-forming modular organisms, solitary forms such as bivalves and solitary ascidians persisted in great abundance. After 13.5 years some 80% of the piling surface was occupied by modular organisms, but solitary forms were still abundant and the composition of the assemblage, which differed at different points along the pier, may still have been changing through time. The explanation for differences from GSV, and indeed between different points along the Port Bonython jetty, seemed to lie in significant physical differences between the environments—again, in processes at the level of body form, physiology, feeding mechanisms etc.

Another study, related to the idea about patch size and isolation, was that of Pitcher, who studied epizoic sponges on the scallop Chlamys asperrima. At Edithburgh, where we developed the original model that large patches are sponge-dominated and small ones (like Pinna shells) are refuges for poor competitors, the coating of sponge on C. asperrima seemed an aberration. Pitcher investigated the benefits for the scallop and the sponge (Pitcher & Butler 1987; see Chapter 18), but the point for our present discussion is the discovery that the most probable way of the scallops gaining their sponge was by direct contact with other scallops. Thus, scallops were effectively not a small patch, isolated from overgrowth and able to be colonised only by larval dispersal. Scallops were an ‘exception that proved the rule’.

Linkages

It might be anticipated (Davis et al. 1982) that assemblages on hard substrata will have significant influence on the surrounding system. Hence, on the one hand, removal of hard substrata (as in the loss of Pinna and Malleus beds in the SE part of the Gulf—Tanner 2005), and, on the other hand, addition of substrata (as in sinking a vessel to create an artificial reef) will have an effect on surrounding benthic and pelagic assemblages. There has been no investigation of this in the Gulf, although we can make some observations. Shading by large structures like jetties is an obvious local effect. Fish aggregation is another (from a large structure, fish will move out to feed, influencing the surrounding assemblages; conversely, large structures may aggregate fish, increasing their vulnerability to fishing—see remarks on artificial reefs above).

But the main thing to stress about ‘linkages’ is that the system we are considering (assemblages of organisms attached to hard substrata) is, itself, characterised by and dependent on linkages. The fauna on your favourite jetty is not self-contained; it would not be the way it is without its connections with its surroundings, some operating continuously (e.g. supply of suspended food) and others episodically (e.g. bursts of larval settlement, destructive storms, arrival of a school of juvenile fish).

Threats

Threats to hard-substratum assemblages include: point-source and non-point (diffuse) discharges of pollutants, sedimentation, collection, the effects of introduced species, and the effects of bottom-contact fishing.


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Point-source and diffuse discharges

Point-source discharges do not seem to be a problem in GSV barring the possibility of shipping accidents. The effects of a discharge of heated seawater on fouling fauna in Angas Inlet, Port Adelaide, were investigated by Host (1977). 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 sessile fauna when in high concentration, but there is no evidence about the effects of such compounds in the areas we have studied, although many of them are of course foci for shipping.

Introductions

Introduced (exotic) species form a major part of many assemblages on subtidal hard substrata, especially in ports (such as Port Adelaide) and marinas. The assemblages studied by Russ (1977, 1982) and Webb (2000) were almost entirely composed of exotic species. They are less abundant in more open parts of the coast, even including the jetties which are heavily frequented by ships. However, some of the species in our assemblages are considered cosmopolitan and were possibly introduced by early shipping; they are called ‘cryptogenic’—of unknown origin (Chapter 17). Examples are the ascidians, Botrylloides leachii (Savigny, 1816) (Figs 1, 5) and Botryllus schlosseri (Pallas, 1766), and bryozoans Schizoporella sp. There is no way to identify any effects of introduced species as such on these assemblages. A potentially harmful introduction, the sabellid polychaete Sabella spallanzanii (Gmelin, 1791), has been recorded from Port Adelaide and from near the eastern shore of the Gulf (Styan & Strzelecki 2002) but not yet at the jetties discussed here. Its dynamics and potential ecological effects are not yet well understood, but it may have significant effects on sessile assemblages (Clapin & Evans 1995; Holloway & Keough 2002a,b; Lemmens et al. 1996, Chapter 17).

Bottom-contact fishing

Tanner (2005), repeating the survey reported by Shepherd & Sprigg (1976), found that their ‘Malleus-Pinna assemblage’ in the SE section of the Gulf was essentially missing in 2000-2001. This represents a significant change for species that depend on the complex habitat-forming structures provided by Pinna and Malleus, a significant component of the spatially structured sessile fauna of the Gulf as a whole, in the view outlined here. As noted in Chapter 18 it seems likely that this massive change to the nature of assemblages on the seafloor was due to prawn trawling. Although practices have now changed, bottom-contact trawling must still alter the dynamics of animals like Pinna and Malleus, and therefore remains a significant threat for the sessile assemblages that interact with them.

Conclusions and Environmental Management Implications

In a modern view of natural history we no longer want to ask questions such as ‘how can so many similar species coexist?’ in a simple form—species do coexist and we have a list of mechanisms that can explain it. The interesting questions are quantitative ones about the joint dynamics of many species—how and why their abundances fluctuate—how and why they differ from place to place and through time—which mechanisms are important for coexistence in a given case.

It would be naïve to suppose that the understanding we seek will be simple in the sense that it involves few variables or processes. I have chosen to mention a few above, but immediately had to discuss interactions between them, and to mention that there are others as yet unstudied. And it would be naïve to suppose that they can be studied exclusively at any one scale. Animals and plants exist in what Andrewartha & Birch (1984) called a ‘natural population’ and Levins (1970) a ‘metapopulation’ (see Kritzer & Sale 2006). Andrewartha & Birch’s idea of a natural population is one that consists of a set of local populations, within which most of the interactions take place, but between which there is limited dispersal. Much research on sessile assemblages—and most of the work outlined above, done in GSV—has been concerned with how organisms interact within the area of the local population, but not how that affects the dynamics of the metapopulation or, when considering a large number of interacting species, the ‘metacommunity’ (Hanski 1999; Holyoak et al. 2005).

Throughout this chapter I have referred to three kinds of environmental variation—spatial, temporal and spatio-temporal—in addition, of course, to the individual variation so familiar to all naturalists, and to a


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number of processes that do not depend on variation. Theoreticians are still working on including all these processes together within models and on how small-scale models can be scaled up to explain the dynamics of ‘metacommunity’ systems (Chesson et al. 2005). The formal testing of such models is a challenging idea (Butler & Chesson 1990; Steinberg & Kareiva 1997; Chesson 2003). For field ecologists, however, it means we need to collect the kind of data that will allow such models to be evaluated. It means that it will rarely get us much further to study one process in isolation—better to study the interactions between several processes. And it will rarely be enough to work on one scale or at one place—in whatever processes interest us, we want to know what is happening at several places, and through sufficient time, so that we learn about all three kinds of variation. Our studies, outlined above, often suffered in this regard—resources were short, spatial scales were small, and times were short.

The emphasis laid here on the three kinds of variation amounts to a sophisticated version of the common plea of ecologists for long-term studies. That has always meant implicitly that we want to know the temporal distribution of something in order to understand it properly. I am emphasising here that we also want to know about variation in space and the interaction between spatial and temporal variation. We need studies to be done not only over a long time, but also in multiple places on different scales!

The conceptual model outlined above—the sessile fauna of the Gulf as a spatially structured ‘metacommunity’ system characterised importantly by individual, spatial, temporal and spatiotemporal variation—has implications for the management of human activities that impinge on the system. Firstly, it means that when monitoring for changes, perhaps as a result of human activities, we should monitor variation, not just averages; changes in the nature of the variation might be important (Butler & Smith 1992). Secondly, notwithstanding the clear relevance of ecological theory to practical problems (e.g. Shea & Chesson 2002), it means that the system is so complex that it is not feasible to develop a tractable model that predicts with high confidence the effect of a human activity (or of climate change, for example). Therefore, management advice must be given with specified uncertainty, ‘best possible’ and precautionary decisions must be made, and an adaptive approach must be taken to management. ‘Adaptive’ here does not merely mean ‘flexible’ but is intended in the sense used by Walters (1986) and Gunderson & Holling (2002) as a planned, formally experimental approach to management under uncertainty.

Acknowledgements

Thanks to Jan Macpherson Butler and Rachel Harm for their help in the preparation of this chapter, and to Peter Chesson, Andy Davis and an anonymous referee for comments on the manuscript. Photo credits: CAS = Craig Styan; MJK = Mike Keough.

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~ ~

Hulks

A ship on the sea Is a living thing,

Its heart— Diesels;

Its corpuscles— People rushing through the corridors.

A derelict Is dead, Its heart

And corpuscles Stilled.

Or is it dead? What birds?

What barnacles? What thousand fouling things?

What ghosts? As the old hulks

Slowly decay In their mangrove graveyard, What weekend resurrection—

As children Explore.

Brian Brock from ‘Catharsis’ 1975.

Night Dive Edithburgh

Encumbered divers Lumber down the steps

And plunge into the splashing blackness Torches shaft the water

And prop snorkellers at the surface.

Greens and reds and browns of marine weeds Surge and sway.

Nereid segmented worms Snake their way

Up the ladder of light To the plankton cloud

At the glass of my underwater torch.

A cuttlefish Backs deeper into its algal lair.

A spotted stingray Mimics a stone in humped stillness.

Sponge crabs Lift their hats

As they promenade on the pylons.

Flecked by ‘Firefly’ light We slowly leave the water.

Brian Brock February 1986.

CHAPTER 21. FAUNA OF JETTY PILES, ARTIFICIAL REEFS AND ... · FAUNA OF JETTY PILES, ARTIFICIAL REEFS AND BIOGENIC SURFACES ALAN BUTLER C.S.I.R.O. Marine Research, Hobart, Tasmania

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