Journal of Aquatic Ecosystem Stress and Recovery 7: 273297, 2000. M.J. Attrill (ed.

), Stress in Marine Communities, Part 2. 2000 Kluwer Academic Publishers. Printed in the Netherlands.

273

Impacts of anthropogenic stress on rocky intertidal communities

T.P. Crowe1, , R.C. Thompson1, S. Bray2 & S.J. Hawkins1,2
1 Biodiversity

and Ecology Division, School of Biological Sciences, University of Southampton, Bassett Crescent East, Southampton SO16 7PX, U.K. 2 Centre for Environmental Sciences, University of Southampton, Higheld, Southampton SO17 1BJ, U.K.

Key words: anthropogenic stress, community, harvesting, human impact, introduced species, pollution, rocky shore, siltation, trampling

Abstract Rocky shores provide a harsh environment for marine organisms and we briey discuss natural sources of variation in community structure before considering anthropogenic impacts in detail. We review impacts caused by (a) acute disturbances: oil spills, toxic algal blooms and (b) chronic disturbances: nutrient pollution, oil, heavy metals, pesticides, antifouling paints, collecting, trampling/habitat degradation, siltation and introduced species. Community level effects are emphasised throughout and illustrative examples are drawn from eld-based case studies. Particular attention is given to the lessons learned from oil spills and the effect of chronic pollution by tributyltin on dogwhelks, the impacts of which ranged from the biochemical to community levels of organisation. Impacts are placed in a global and historical perspective and the potential for the recovery of shores under appropriate management is discussed. Finally we consider the relative merits of the multivariate and univariate approaches to studying impacted communities and suggest priorities for future research.

1. Introduction Rocky shores occur throughout the coastlines of the worlds oceans. They are the most extensive littoral habitat on eroding wave-exposed coasts and are also a major habitat on more sheltered coastlines, such as fjords and rias. This already extensive natural habitat is further increased by the plethora of articial hard structures such as breakwaters, jetties, docks, groynes, dykes, sea walls which essentially function as articial rocky shores. Sheltered bays, fjords and rias are widely used as harbours which range in size from small shing ports or marinas up to major industrial ports. Articial shores generally occur in densely populated and often industrialised regions, while even in remote places, rocky shores can be impacted by a variety of activities ranging from subsistence collection of food through to mining waste and occasional catastrophic oil spills.
* Corresponding author: Phone: 023 80594386; Fax: 023

80594269; E-mail: tpc@soton.ac.uk

Thus many rocky shores are subjected to a variety of stresses caused by human activities. These anthropogenic stresses are superimposed on the stress caused by natural environmental factors such as emersion in air due to the tides and wave action (see Raffaelli & Hawkins, 1996 for review). In this review we start by briey considering terms and denitions. We then outline natural stressors that inuence rocky shore communities and the problem of separating their effects from those of anthropogenic stresses. We then consider acute and chronic anthropogenic stresses and review research into their impact on rocky shore communities. Special attention is focussed on the acute impact of oil spills and the chronic pollution caused by tributyltin in antifouling paints. We emphasise the need to integrate from individual responses up to the community level. The discussion provides a global and historical perspective. We consider the scales and relative importance of different impacts and examine the potential for recovery of rocky shore communities. Finally

274 we highlight gaps in our knowledge and point out priorities for future work. We concentrate on the intertidal zone of rocky shores; coral reefs and subtidal habitats are outside the scope of this review but are occasionally discussed, particularly in relation to processes that have received little attention on rocky shores. Many of the ideas and examples in this paper draw on publications in various conference proceedings (e.g. Hawkins & Southward, 1992; Hawkins et al., 1994; Hawkins, 1999a, b) and we have taken the opportunity to integrate and synthesise these into this review. inate among these alternatives, however, and impacts will be discussed by reference to the acute and chronic disturbances that caused them.

3. Separating natural and anthropogenic stress Rocky shore organisms are subject to two major natural gradients of physical stress (see Raffaelli & Hawkins, 1996 for review). First there is the vertical gradient of increasing stress with increasing exposure to air higher on the shore, due to the alternation of the tides. This gradient is essentially unidirectional for most marine organisms and is present on both microtidal (e.g. <0.5 m the Mediterranean and Baltic seas) and macrotidal shores (i.e. shores with tides of up to 10 m or greater). Second, there is a horizontal gradient due to differences in wave action between exposed headlands and sheltered bays or inlets. This gradient is not unidirectional as some organisms are naturally more abundant in wave swept conditions (e.g. suspension feeders such as mussels) others are more abundant in shelter (e.g. some large algae such as Ascophyllum). Within these two major gradients, conditions vary under the inuence of localised factors such as geology which in turn affects the topography of the shore, resulting in complex variation in microhabitat caused by pools, overhangs, crevices and boulders. On microtidal shores these may completely override the major gradients whilst on macrotidal shores they tend to modify the gradient locally, giving rise to patchy arrangements of physical conditions. The other major environmental gradient is that of salinity in estuaries, which also has a major effect on patterns of distribution and abundance. On a larger scale, there is an over-riding gradient of climate associated with geographic location. Many rocky shore organisms must therefore be tolerant of a wide range of stresses. Organisms usually occur well within their range of tolerance of physical conditions and are not stressed except under unusual conditions. To achieve this, they have mechanisms to deal with the stresses associated with alternating immersion and emersion in air (desiccation, osmotic stress, etc., see for example Newell, 1979; Davison & Pearson, 1996; Karsten et al., 1996). These mechanisms may often be effective for withstanding anthropogenic stresses. Of particular note are behavioural mechanisms to shut animals off from the environment coupled with ability to withstand anaerobosis

2. Terminology A variety of terms has emerged to describe environmental disturbances and their effects. The environment is contaminated by input of man-made substances, but pollution is only said to occur when the contaminant actually has an effect on a biological variable (Clark et al., 1997). Similarly stress is, broadly speaking, the response of a biological entity (individual, population, community, etc.) to a disturbance (or stressor). Hence anthropogenic stress is the response of a biological entity to an anthropogenic disturbance. Stresses at one level of organisation (e.g. individual, population) may also have impacts on other levels, for example causing alterations in community structure. These terms are difcult to dene precisely and have been used in many different ways (see Parker et al. (1999) for a detailed review). Inputs, disturbances or other sources of stress are generally described as being either chronic or acute. A chronic disturbance operates at a low level over a long period, while an acute disturbance is a discrete, usually large event. These terms are roughly analogous to the terms press and pulse which are used to describe environmental disturbances of long and short duration respectively (Bender et al., 1984). This latter terminology was recently rened by Glasby and Underwood (1996). Their classication distinguishes between the duration of the disturbance and the duration of the response of the target organisms or community (the impact). They recognised that, for example, a disturbance of either short duration (pulse) or long duration (press) could cause either no response, have a short term impact or cause a long term change in a population. Careful use of clearly dened terminology will aid well-designed research into human impacts on rocky shores. Few of the studies reviewed below were designed to discrim-

275 which are equally effective in avoiding short pulses of pollutant as spells of low salinity or emersion. Many organisms have well developed sensory mechanisms to detect and hence respond to stressors (e.g. Akberali & Davenport, 1982) and can also detect and respond to pollutants such as heavy metals (e.g. Redpath & Davenport, 1988). Many intertidal algae are equally resilient and are able to tolerate considerable uptake of heavy metals (Barreiro et al., 1993; Castilla, 1996) and withstand oil spills and dispersant application. Thus it is sometimes difcult to detect the effects of anthropogenic stress at the level of the individual organism. Impacts are more often investigated at a population or community level. Populations and communities exhibit considerable variability in space and time under the inuence of many physical and biological factors (e.g. Hartnoll & Hawkins, 1985; Underwood, 1985; Foster et al., 1988). On rocky shores, dramatic natural uctuations can be caused by factors such as extremes in temperature (Crisp, 1964), red tides (Southgate et al., 1984) and variations in recruitment success (e.g. Bowman & Lewis, 1977; Caffey, 1985; Gaines et al., 1985; Underwood & Fairweather, 1989). Against such a background of variation, it is often extremely difcult to detect reliably the additional effects of human activities. The difculties in detecting the comparatively minor effects of low-level chronic stress at the community level on rocky shores have been appreciated for some time (Lewis, 1976, 1977; Hawkins & Hartnoll, 1983; Hiscock, 1985). In most cases, for community level effects to be expressed and detected, the disturbance must either come from a point source (e.g. a large efuent) or a catastrophic event (e.g. an oil spill or the aftermath of a red tide). Recently the need for properly designed impact assessments has been emphasised (Underwood, 1992, 1994). Such designs involve repeated sampling and comparison with multiple control or reference sites enabling natural spatial and temporal variation to be objectively separated from putative impacts (see Underwood, 1992, 1994). The majority of work on rocky shore communities has tended to concentrate on selected prominent species or functional groups analysed in a univariate manner. Multivariate analysis of whole communities, which is common in research on soft sediment biota (e.g. Gray et al., 1990; Agard et al., 1993; Somereld et al., 1995), has not been so widely used (but see Hockey & Bosman, 1986; Fuji & Nomura, 1990; Lasiak & Field, 1995; Underwood & Skilleter, 1996; Coates, 1998; Lasiak, 1998, 1999). The large amount of experimental community ecology that has been done on rocky shores, however (Connell, 1972; Paine, 1977, 1994; Underwood et al., 1983, Hawkins et al., 1992), often allows good interpretation of likely impacts on particular species and, in some cases, communities.

4. Acute anthropogenic disturbances 4.1. Oil spills The best-recorded community level impacts of anthropogenic stress are from oil spills. These have been well documented on rocky shores (Clark et al., 1997). Details of selected major spills are summarized in Table 1. Most of these spills led to oil being washed onto rocky shores, but the major spill in the Arabian/Persian Gulf during the Iraq/Kuwait war impacted mainly depositing shorelines, although some rocky areas were affected (Watt et al., 1993; Jones et al., 1998). Where oil became stranded on low energy depositing shores or mangroves, recovery was generally slower than on more wave exposed rocky shores.
Table 1. Selected major oil spills (modied from Hawkins & Southward, 1992) Ship or installation Persian Gulf Ixtoc 1 Amoco Cadiz Torrey Canyon Braer Sea Empress Khark 5 Metula Exxon Valdez Urquiola Aragon Date Oil spilt (tons) Oil beached (tons) ? 12 000 80 000T 35 000 ? 515 000 ? 42 000 4 500 25 000 ?

Jan 91 >1million 3 Jun 79 500 000 16 Mar 78 233 000 18 Mar 67 100 000 5 Jan 93 85 000 21 Feb 96 72 000 19 Dec 89 70 000 9 Aug 74 51 000 24 Mar 89 38 000 2 May 76 30 000 30 Dec 89 25 000

Some costly early mistakes were made in cleaning up oil spills which often led to more damage being done during clean-up than caused by the oil itself (see Foster, et al., 1990 for review). For example, as a result of the Torrey Canyon oil spill in Cornwall, the

276 major damage was not caused by the 10 000 tons of oil which came ashore, but by excessive treatment with over 14 000 tons of rst generation dispersants. These were later shown to be very toxic to marine life (Corner et al., 1968). The dispersants killed the grazer Patella vulgata, and, to a lesser extent, other herbivores such as Monodonta lineata and Littorina spp. This reduction led to dense growth of ephemeral green algae followed by an equally dense growth of fucoids. This proliferation occurred on many of the exposed and moderately exposed shores of south-west Cornwall (see Smith, 1968; Southward & Southward, 1978; Hawkins et al., 1983; Hawkins & Southward, 1992; Hawkins et al., 1994 for further details). Similar, but more localised, ushes of ephemeral algae and fucoids were shown after the Braer (Newey & Seed, 1995) and Sea Empress spills (Moore, 1998). Some dogwhelks survived the Torrey Canyon spill and were able to reproduce locally under the shelter of the fucoid canopy (Bryan, 1969). Barnacles were only affected in areas that were cleaned repeatedly. Over the next few years, however, they succumbed to smothering by algae and predation from the now dense populations of dogwhelks. Of greatest signicance was the highly favourable environment for the settlement and early survival of Patella vulgata created by the fucoids. Patella depressa remained scarce in the area until the mid 1980s (see Southward & Southward, 1978; Hawkins & Southward, 1992). We now have over 20 yrs of observations on the recovery of the shores affected by the Torrey Canyon spill. We also have a good background knowledge of spatial and temporal variation of these systems to put the results into context (see Southward & Southward, 1978; Hawkins et al., 1992a). Recovery of key species to previously observed normal levels of spatial and temporal variation was judged to have occurred within 1015 yrs. This recovery was through a series of damped oscillations (Southward & Southward, 1978; Hawkins et al., 1983; Hawkins & Southward, 1992) and a similar pattern is starting to emerge since the more recent Exxon Valdez spill (Paine et al., 1996). Disruption of the community to such a vast extent resulted primarily from the widespread killing of Patella. These limpets can be considered a keystone species on moderately exposed and exposed shores throughout the northeast Atlantic because of the importance of their grazing (see Hawkins et al., 1992 for review; Mills et al., 1993; Power et al., 1996; Raffaelli & Hawkins, 1996; Hurlbert, 1997 for recent critiques of the keystone concept). Since the Torrey Canyon spill there has been much work on the impacts of other spills both large (e.g. Myers et al., 1980; Conan, 1982; Shaw, 1992; De Vogelaere & Foster, 1994; van Tamelen, 1997; Jones et al., 1998) and small (e.g. Bowman, 1978; Pople et al., 1990; Lopes et al., 1997; Smith & Simpson, 1998). Over the years various overviews and reviews have been written (e.g. Southward, 1982; Lewis, 1982; Hawkins & Southward, 1992; Suchanek, 1993) which summarize a diverse and often grey literature. Paine et al. (1996) and Petersen (in press) both ably summarize the explosion of literature following the Exxon Valdez spill. Oil spills have variable effects on the biota. Some species can be remarkably tolerant of oiling (e.g. barnacles, Southward & Southward, 1978; mussels, Newey & Seed, 1995), although generalization is difcult as the degree of mortality of a particular group of animals varies among locations and with oil type. For example, Smith (1968) and Southward and Southward (1978) showed oil tolerance in barnacles in south-west England to Kuwait oil following the Torrey Canyon spill whilst Newey and Seed (1995) demonstrated a decrease in cover due to Gullfaks Norwegian crude oil following the Braer spill. Newly settled spat have also been shown to be much more resilient than adults (Bonsdorff & Nelson, 1981). Other species have been impacted more by clean-up operations. Grazing molluscs seem to be particularly susceptible to oil, oil/dispersant mixtures and dispersant itself (e.g. Smith, 1968; Crothers, 1983; Newey & Seed, 1995). Encouragingly, the later generations of dispersants seem much less toxic than those used following the Torrey Canyon spill (e.g. Crothers, 1983). Worries about the application of toxic dispersants have led to widespread use of physical cleaning methods. These can also cause considerable disturbance and are made worse when high pressures or temperatures are used. For example, large areas of fucoid canopies (Fucus gardneri) were essentially destroyed by the combination of oil and clean up operations using high pressure hot water following the Exxon Valdez spill (De Vogelaere & Foster, 1994; Highsmith et al., 1996; Houghton et al., 1996; van Tamelen & Stekoll, 1996). Shaw (1992) ironically points out that mechanical beach cleaning following the Exxon Valdez oil spill caused destruction comparable to that of the highly toxic dispersants following the Torrey Canyon spill. Given the uncertainty about the impacts of actual oil spills it is surprising that so few replicated

277 eld trials of the impacts of oil and various treatments have been attempted (but see Nelson, 1981, 1982; Bonsdorff & Nelson, 1981; Bonsdorff, 1983; Crothers, 1983). In part, this is a reluctance of investigators to damage the environment by eld trials on the scale necessary to simulate oil spills. Crothers (1983) simulated oil spills in winter and summer on seaweed covered and limpet/barnacle dominated shores. The experimental treatments were oil alone, dispersants alone, oil plus dispersants and controls. This work showed minimal effects on a seaweed covered shore. On limpet-dominated shores, plots receiving a combination of oil and dispersant were most affected, followed closely by oiled plots. The effect of the dispersant (BP1100WD) alone was minimal. There was also greater decrease in barnacle cover in the oiled, and oil/dispersant plots than the controls and dispersant only plots. Bonsdorff and Nelson (1981) simulated oil spills (Ekosk crude oil) on the Norwegian coast. Mobile crustacea such as amphipods and isopods showed avoidance responses, but some were still killed. Spat of Semibalanus balanoides were shown to be very sensitive, in contrast to adults which were only affected at the highest levels of oiling. Turning to warmer climes, considerable effort has gone into assessing the impact of oil resulting from the 1991 Gulf War and subsequent recovery (e.g. Watt et al., 1993; Jones & Richmond, 1992; Abuzinada & Krupp, 1994; Jones et al., 1994; Readman et al., 1996). The account below is based on Jones et al., 1996. By seven months after the spill, most oil had been deposited high on the shore between high water neaps and high water springs, although it had clearly affected lower levels on the shore. During the rst 23 yrs there were considerable uctuations as new colonization of species such as barnacles occurred. There was a complete absence of most major species in the littoral fringe, and between 80% to 100% reduction in species diversity in the upper eulittoral zone. Much of the oil rapidly hardened into tar. This began to disappear in 19911992, a process helped by colonization by algal mats within a couple of months, which eventually peeled off with the oil. New recruitment began to occur within a year or two where the oil had weathered and peeled away. By 1994, diversity and abundance of individual species was still reduced from the midshore upwards by up to 50%, but normal diversity had returned to the lower eulittoral. The major high shore gastropods, Nodolittorina subnodosa and Plenaxis sulcatus only returned to the most badly affected shore studied in 1995. Various clean up methods were tried in the Gulf, including high pressure ushing on a rocky outcrop (Watt et al., 1993). No differences in recovery rate were apparent between treated and untreated rock and Watt et al. (1993) expressed concern that any further clean up might further decrease populations of snails with direct development such as Nodolittorina subnodosa and Plenaxis sulcatus. Work on several smaller oil spills (e.g. Lopes et al., 1997; Pople et al., 1990; Smith & Simpson, 1998) has also been undertaken. In Brazil, a crude oil spill caused no discernible differences after the spill when compared to before (Lopes et al., 1997). In contrast a spill of diesel on sub-Antarctic Macquarie Island caused widespread mortality of marine invertebrates over 2 km of shore, with reduced densities still apparent 1 yr later (Pople et al., 1998). Seven years after the spill, macrobiotic communities had recovered in the intertidal, but impacted kelp holdfast communities were still very different from uncontaminated controls. They were lled with sediment showing traces of diesel and the communities were dominated by opportunistic worms (Smith & Simpson, 1998). Interpreting the impact of oil spills is not easy when there is a lack of data from before the spill. This is compounded by problems in selecting adjacent control areas which are similar but not affected. It is also difcult to persuade regulatory authorities to leave some areas untreated to act as controls for comparison with cleaned areas. Resources tend to be deployed in excess during the immediate post-spill phase but as public interest wanes, so does funding for longer term studies. Sadly most oil spills provide a missed opportunity for extraction of information (see also comments in Foster et al., 1990; Paine et al., 1996). The initial bonanza of interest from the news media is followed by a phase of investigation by scientists from government agencies, industry, consultancies, nongovernmental organizations and universities. Funding is not always allocated to the most qualied teams as peer review processes cannot operate on the timescale needed to respond. Not surprisingly the quality of the research outcomes are often disappointing and several authors have urged better deployment of resources for the next spill to enable high quality research (e.g. Foster et al., 1990; Hawkins & Southward, 1992; Paine et al., 1996).

278 4.2. Toxic algal blooms Similar dramatic disruption of communities can occur after red tides of toxic planktonic algae (Smayda, 1997). These occur naturally, but in recent years it has been suggested that their frequency has increased because of eutrophication (Hallegraeff, 1993; Paerl & Whittall, 1999). Although their devastating effects on sh and aquaculture have been widely publicised, little has been published on their impacts on rocky shore communities. Southgate et al. (1984) documented the effects of a dinoagellate bloom on the coast of Ireland and its effect on the shore community. Robertson (1991) reported major toxic effects caused by a bloom of Chrysochromulina polylepsis off the Swedish west coast. This killed up to 99% of the dogwhelks from some areas of the coast and affected the reproductive output of the survivors in the following year. Similarly devastating effects were seen in several habitats in Norway (e.g. Bokn et al., 1990). Gastropods, urchins and starsh were severely affected, but mussels and oysters were more resilient. see Borowitzka, 1972; Fairweather, 1990; LpezGappa et al., 1990). Fairweather (1990) found that the animals dominant at control shores were replaced by ephemeral green algae near sewage outfalls in Sydney. Similarly, Lpez-Gappa et al. (1990) reported the total absence of the otherwise dominant mussel Brachidontes rodriguezi from the immediate vicinity of an outfall in Argentina and its replacement by cyanobacteria, diatoms and green algae. Limpets occurred in relatively low densities at a site close to the outfall and tended to grow markedly faster there than at a control site (Tablado et al., 1994). This pattern is similar to that observed at sites enriched with guano (Bosman & Hockey, 1988). Trends observed in the Baltic suggest that large scale eutrophication has had effects similar to those caused by point sources of nutrient pollution, causing the decline of diverse assemblages dominated by perennial algae (especially Fucus vesiculosus) and their replacement with species-poor turfs of green ephemerals (Schramm, 1996; Worm et al., 1999; see Bonsdorff et al., 1997; Diaz & Rosenberg, 1995). Large scale variations in natural nutrient levels have also been found to correlate with variations in the functioning of intertidal communities (e.g. Bustamante et al., 1995; Menge et al., 1997). Nutrientrich areas of coast had greater benthic microalgal productivity, greater biomass of grazers (Bustamante et al., 1995) and faster growth of lter feeders (mussels, barnacles; Menge et al., 1997) than areas with low concentrations of nutrients. These patterns remain correlative, however, and in the case of Menge et al.s (1996) study, evidence was derived from comparisons of only two sites. Small scale experimental investigations of the effects of nutrient enrichment on rocky shore communities have yielded mixed results. Wooton et al. (1996) found that the inuence of molluscan grazers on community structure was far greater than that of nutrients. Micrograzers were the only group to increase as a result of nutrient enrichment and there was no change in algal biomass. Worm et al. (1999), working in shallow subtidal Fucus beds, found that nutrient enrichment overrode grazer control of algal assemblages only where propagule banks had been left intact. 5.2. Hydrocarbons As the most visible and newsworthy form of pollution, the majority of attention to ecological effects of

5. Chronic anthropogenic disturbances Impacts caused by long-term, low level disturbances are summarised in Table 2 and described in detail below. 5.1. Nutrient pollution Chronic inux of excessive nutrients originates mainly from anthropogenic sources, particularly sewage outfalls and run-off of agricultural fertilizers (Clark et al., 1997; Raffaelli & Hawkins, 1996). It can also occur naturally, for example at seabird colonies (e.g. Bosman & Hockey, 1988; Wootton, 1991). On waveexposed rocky shores, where water movements are great, the effects of sewage efuent are usually localised to within about a hundred metres of the outfall (Fairweather, 1990), but effects are more pronounced in enclosed bays or harbours (Raffaelli & Hawkins, 1996). In California, assemblages which are usually dominated by large brown algae were replaced in the immediate vicinity of an outfall by cyanobacteria and omnivores and suspension feeders capable of feeding directly on the efuent (Littler & Murray, 1975). The diversity of the assemblage was signicantly reduced relative to controls (Littler & Murray, 1975;

279
Table 2. Summary of major impacts to rocky shore populations or communities caused by chronic disturbances. A selection of key papers presenting or reviewing evidence from eld studies is listed
Stress Nutrient enrichment Sewage outfall Sewage outfall Hydrocarbons Oil renery Heavy metals Copper mine tailings Antifouling paints Tributyltin (TBT) " Thermal pollution Power station Impact Location Reference

Large brown algae replaced by blue-greens Reduced diversity of assemblage Mussels replaced by algae Reduced density & rapid growth of limpets Reduced density and diversity of mollusc community Barnacle assemblage replaced by copper resistant green alga Imposex in stenoglossan gastropods Extinction of dogwhelks from many parts of range Mortality of macroalgae Displacement of native barnacles by exotic spp. Reduced diversity of assemblages in kelp holdfasts No effect on abundance; stable Catch Per Unit Effort Reduced size and abundance of target spp. Replaced by bare space or assemblages dominated by coralline algae, Gelidium or barnacles Reduced size and abundance of target spp. Growth of macroalgae " Reduced size and abundance of target spp. Increased access for grazers, so poor recolonisation of algae; if no grazers, opportunistic algae invade; loss of holdfasts and associated fauna Reduced abundance of barnacles and mussels Reduced abundance of macroalgae; indirect effects on other species Increased bare space Increased bare space; shift to opportunistic species

California Argentina " Curaao, Caribbean Chile World-wide Europe Maine, USA Swansea, UK Anglesey, UK KwaZulu-Natal, S. Africa Transkei, S. Africa Transkei, S. Africa Victoria, Australia Chile California, USA Chile Chile & S. Africa

Littler & Murray, 1975 L opez-Gappa et al., 1990 Tablado et al., 1994 Nagelkerken & Debrot, 1995 Castilla, 1996 Ellis & Pattisina, 1990 Gibbs et al., 1991a Vadas et al., 1978 Langford, 1990 Bamber, 1991 Kyle et al., 1997 Hockey & Bosman, 1986 Dye et al., 1994b Keough et al., 1993 Branch & Moreno, 1994 Lindberg et al., 1998 Castilla & Bustamente, 1989 Santelices & Grifths, 1994; Vasquez, 1995

Harvesting Mussels Mussels Mussels Molluscs Grazing gastropods Macroalgae

Trampling Oregon, USA Northumberland, UK & S. E. Australia S. E. Australia Northumberland, UK Eastern USA France, Australia, USA Brosnan & Cumrine, 1994 Fletcher & Frid, 1996; Keough & Quinn, 1998 Povey & Keough, 1991 Fletcher & Frid, 1996 Carlton, 1982, 1989 Walker & Kendrick, 1998

Introduced species Littorina littorea Undaria pinnatida

Altered community structure; displaced native mudsnail in places Replacement of dominant macroalga; shift in community structure

hydrocarbons has focussed on catastrophic oil spills (see Section 4.1). In terms of total volume, the input from low-level chronic sources such as urban run off and routine tanker and renery operations is much greater (Foster et al., 1988; Suchanek, 1993). Despite this, experimental knowledge of the effects of longterm chronic oil pollution on littoral systems is generally lacking (Southward, 1982). An exception is the mesocosm study of Bokn et al. (1993 and references therein) in which low doses of diesel oil were delivered to communities in large outdoor tanks for 2 yrs and changes compared with those of unpolluted controls. Although detailed inference was hampered by psuedoreplication, some clear trends were apparent. Populations of animals, particularly mussels, tended to be more susceptible than those of algae, a pattern

which is commonly observed in more acute spills (e.g. Stirling, 1977; Pople et al., 1990). There were no impacts on herbivores in the experiment, although loss of herbivores has been common after acute spills (Foster et al., 1988) and has been noted at some chronically affected shores (Southward, 1982). Similarly, the density and diversity of mollusc communities on tropical rubble shores impacted by oil terminals for >7 yrs were greatly reduced relative to unpolluted controls (Nagelkerken & Debrot, 1995). Southward (1982) suggested that affected shores are generally characterised by reduced abundance of herbivores and increased standing stocks of ephemeral algae. There is also some evidence that settlement of barnacles may be locally inhibited by even small quantities of oil (Crapp, 1971; Nelson, 1981).

280 Although further research is needed, effects on the settlement of intertidal species could lead to signicant modications in community structure. 5.3. Heavy metals The majority of heavy metals (copper, tin, mercury, cadmium, etc.) enter the marine environment via natural pathways such as the erosion of ore-bearing rocks and volcanic activity (Clark et al., 1997). Human sources include sewage (e.g. Anderlini, 1992), industrial discharges and dumping and urban run-off (Clark et al., 1997). Some trace metals are metabolically important but can be toxic at higher concentrations (Bryan, 1984). The toxicity of heavy metals and the limits of tolerance of many organisms have been examined in detail in laboratory studies (Mance, 1987). Many researchers have documented elevated concentrations of heavy metals in intertidal organisms (e.g. Barreiro et al., 1993; Blackmore et al., 1998) and used them as indicators of environmental contamination (e.g. Bryan, 1984; Haynes et al., 1997). There is, however, little published research on the effects of heavy metals on natural communities on rocky shores. Laboratory studies have shown that heavy metals can have complex effects on the growth of marine organisms such as mussels and fucoid algae such that different combinations and concentrations of metals can either promote or inhibit growth (Strmgren, 1982; Munda & Hudnik, 1986). Heavy metals can also affect aspects of larval development and are usually toxic to larvae at far lower concentrations than to adults (Beaumont et al., 1987; Fichet et al., 1998). Hoare et al. (1995) presented evidence that mussel embryos in polluted areas showed increased resistance to copper and indicated that this adaptation may have a genetic basis (see also Russell & Morris, 1970). Impacts on the structure of communities on rocky shores would only be likely in bays, inlets or estuaries with high residence time to allow concentration of the metals. Since heavy metals can affect the growth, reproduction and genetics of key species, elevated concentrations could potentially have farreaching effects, but these have yet to be examined in detail. One of the few exceptions is Castillas (1996) comparison of assemblages on four shores in Chile before and after two of them were impacted by copper mine tailings. There were no differences among the shores before the copper mining commenced. Within two years of the commencement of copper mining activities, however, the barnacle-dominated assemblage at the impacted sites was replaced by Enteromorpha compressa, an alga that is resistant to copper, with associated changes in the community relative to controls. With the cessation of dumping of untreated tailings, there was a steady increase over four years in the diversity at the formerly impacted sites. This indicates that the changes may be reversible (see also Correa et al., 1999). 5.4. Pesticides and antifouling paints The toxicity and sublethal effects of pesticides, such as organochlorines and organophosphates to rocky intertidal organisms has been explored in the laboratory (e.g. Sarojini et al., 1989; Lundebye et al., 1997), but to date there are no published eld studies of effects on populations and communities. Antifouling paints are essentially pesticides. The side-effects of their leachates were often ignored until the early 1980s. Since then many studies have highlighted the environmental impact of pollution caused by the biocide tributyltin (TBT) in antifouling paints (Figure 1; and see Rexrode, 1987; Bryan & Gibbs, 1991 for reviews). The magnitude of these effects was rst realised when the collapse of the French oyster shery in Arcachon Bay was attributed to increased use of TBT on boats in nearby harbours (Alzieu et al., 1986). Previously it had been thought that the concentrations of TBT present in the water posed no direct threat to marine organisms due to the large dilution factors involved (Bellinger & Benham, 1978). Although a multitude of organisms is susceptible to pollution from TBT, none is as sensitive or has such clearly dened responses as those which are seen in stenoglossan gastropods, such as the common dogwhelk, Nucella lapillus, which is susceptible to concentrations as low as 0.5 ng Sn l1 (Gibbs et al., 1988, 1991a). TBT induces the development of male sexual characteristics in female dogwhelks (Bryan et al., 1986, 1988) a phenomenon termed imposex (Smith, 1980). This response has now been reported in up to 45 species of stenoglossan gastropods worldwide (Ellis & Pattisina, 1990). The effects of TBT on Nucella lapillus are now well documented at the sub-cellular, individual and population levels (Figure 2). Biochemical changes responsible for the development of imposex are thought to be a consequence of an increase in the steroid hormone testosterone in the female (Gibbs et al., 1991b). The female develops a penis and vas deferens which leads to the occlusion of the genital

281

Figure 1. Sensitivity to tributyltin contamination (ng l1 ) of various marine organisms. The responses range from sublethal effects on individuals to acute direct effects on populations. Note the use of a logarithmic scale. Superscript numbers refer to references (1 Gibbs et al., 1988; 2 Chagot et al., 1990; 3 Thain et al., 1987; 4 Gibbs et al., 1988; 5 Johansen & Mhlenburg, 1987; 6 Salazar & Salazar, 1991; 7 Beaumont, 1988; 8 Beaumont & Newman, 1986; 9 Pettibone & Cooney, 1986; 10 Uren, 1983; 11 Paul & Davies, 1986 and Davies et al., 1986). From Hawkins et al., 1994.

papilla. Egg capsules subsequently build up in the capsule gland, effectively rendering the female sterile. The build up eventually causes the capsule gland to rupture, resulting in the death of the female (Gibbs & Bryan, 1987). At environmental concentrations of 12 ng Sn 11 some females become sterilised. When environmental levels reach 4 ng Sn l1 most females in the population are unable to breed (Gibbs et al., 1988). At highly contaminated sites juvenile Nucella may become sterile before ever being able to breed (Gibbs & Bryan, 1987). As a consequence of the direct development of Nucella and the relative immobility of adults, there is a scarcity of juveniles at affected sites. The structure of the population is thereby altered (Bryan et al., 1986), subsequently becoming dominated by adult males before it disappears altogether (Spence et al., 1990a).

Nucella was effectively exterminated from many localized areas in its European range (Norway to Portugal) from the late 1970s to the mid-late 1980s (Gibbs et al., 1991a), most notably on shores adjacent to harbours or marinas where TBT levels have extended above the critical 2 ng SN l1 . This situation has been especially severe on the south coast of England (Gibbs et al., 1991c) where virtually all dogwhelk populations have been affected to some degree (Bryan & Gibbs, 1991). In the UK, a ban was imposed in 1987 on the use of organotin paints on boats less than 25 m in length and on equipment used in mariculture (Duff, 1987). The process of recovery has been slow, however, as imposex itself is irreversible. In French waters, the use of antifouling paints was restricted in 1982 (Alzieu, 1986). Seven years later, levels of TBT in Brittany were still sufcient to cause a high level of imposex

282

Figure 2. Summary diagram of the known effects of TBT on dogwhelks (Nucella lapillus) at a hierarchy of levels of organisation. From Hawkins et al., 1994.

in Nucella populations (Gibbs et al., 1991a). In some areas, recovery was thought likely to be inhibited by the continued legal use of TBT on ships larger than 25 m (Davies & Bailey 1991) and by the fact that TBT stored in sediments continues to be leached into the water column (Langston et al., 1990). Nevertheless, abundance of dogwhelks is now increasing on the coasts of Britain, Norway and France, and there is some debate about the wisdom of a total ban in case alternative antifouling treatments prove to be even more harmful (Pearce, 1999; Evans et al., 1998, 2000a). Since the initial visible stages of imposex in Nucella develop at levels of TBT as low as 0.5 ng Sn l1 , imposex can be used as a sensitive bioindicator of TBT pollution (Gibbs et al., 1987). In addition to their clear responses to TBT and world-wide distribution, their accessibility, commonness and ease of identication makes these gastropods ideal bioindicators for contamination studies (Bryan et al., 1985; Bryan, 1984

but see Evans et al., 2000b). Consequently they are now used to provide a world-wide indicator of TBT pollution (Bright & Ellis, 1990; Ellis & Pattisina, 1990; Spence et al., 1990b; Smith & McVeagh, 1991). Whelks have been shown to be important predators in rocky shore communities world-wide (Connell, 1961, 1970; Dayton, 1971; Underwood, 1978; Fairweather et al., 1984; Fairweather, 1987, 1988a, b). Despite speculation (Spence et al., 1990a; Bryan & Gibbs, 1991; Hughes & Burrows, 1993) no studies have so far shown a clear community effect as a consequence of TBT-induced dogwhelk decline. Recently, experiments on moderately exposed shores on the Isle of Man were used to determine the likely consequences of their decline. On such shores, a natural cycle exists in which barnacle-dominated assemblages alternate with fucoid-dominated assemblages (summarised in Hawkins & Jones, 1992). The alternation between these assemblages is mediated by the grazing of limpets, which is

283 inhibited by the presence of barnacles. Algae that settle among barnacles are thus able to escape grazing and form mature clumps. Experimental reductions in the density of dogwhelks increased the abundance of barnacles relative to control plots, thus modifying the initiation and persistence of algal clumps and signicantly altering the community structure and dynamics of these shores (Proud, 1994; Hawkins et al., 1994). 5.5. Thermal pollution Thermal efuent has been a factor in the marine environment for a number of years and is largely associated with cooling water out-falls from power stations and large industrial facilities. Studies of rocky substrata exposed to thermal pollution are, however, scarce (reviewed by Langford, 1990). Some work has been done on thermally impacted algae. For example, Vadas et al. (1978) showed that Fucus vesiculosis declined rapidly and Ascophyllum nodosum was also detrimentally affected by thermal extremes and rapid diurnal uctuations caused by a cooling water outfall in Maine. They pointed out, however, that although this gave an insight into the response of individual organisms, the response of the community as a whole remained largely unknown. In some cases exotic species colonise hard substrata where a cooling water out-fall is present. For example, in a thermally affected dock in Swansea (UK), communities of introduced barnacles Balanus amphitrite and Elminius modestus showed enhanced breeding (Naylor, 1965a, b; reviewed by Langford, 1990). The indigenous species, Balanus crenatus, did not breed in the heated water (>20 C), but B. amphitrite did and consequently replaced B. crenatus. The only study to date which has identied community-wide effects was done at Wylfa Nuclear Power Station by Bamber (1991), who found decreasing diversity in the communities associated with Laminaria holdfasts with increasing proximity to the cooling water out-fall. Interpretation is hampered, however, by the fact that no information was given on actual temperatures or on the presence of biocides in the cooling water. This is a point highlighted by Vadas (1979): There are numerous problems confounding nearly all eld studies [in this area]. Often thermal plumes produce or induce indirect effects, most commonly increased turbidity and sedimentation in discharge areas [reducing photosynthetically available light and adversely affecting lter feeders]. Also toxicity from chlorination to reduce fouling or from heavy metals eroded from cooling pipes may occur. Therefore separating the community effects of thermal discharge from other factors associated with the outfall is problematic. The effects of thermal discharge at the community level requires further investigation. Whether thermal efuents can have a permanent impact on communities on rocky substrata is unknown. In the case of the Swansea Docks, however, when the thermal discharge was removed, the exotic species declined and indigenous species were restored (Naylor, 1965a, b). 5.6. Collecting and gathering Man has utilised intertidal organisms as a source of food since prehistoric times (for review see Siegfried et al., 1994; Grifths & Branch, 1997; Castilla, 1999). These plants and animals still provide a major resource for human populations in coastal regions of America, Africa (see Siegfried, 1994), Asia (Akimichi, 1995), Australasia (Underwood, 1993a) and some oceanic islands (e.g. Azores, Santos et al., 1995). Mans exploitation of the intertidal is facultative and, unlike most other intertidal predators, it is not directly inuenced by density dependent predator-prey relationships, nor by the physical factors (such as storms, desiccation stresses) which regulate the abundance of prey species (Dye et al., 1994a). Intertidal organisms are especially vulnerable since they are either sessile or their movement during low tide (the principal time for collection) is conned to refuges such as pools, crevices or habitats beneath boulders. With the exception of chemo-defence, via toxins, most of the antipredator defences used by these organisms are ineffective against man (Hockey, 1994). Consequently, there is considerable concern that certain species are being over-exploited and marine habitats are being damaged (Newton et al., 1993; Grifths & Branch, 1997). A variety of organisms is collected (over 30 spp. in each of South Africa and South America see Siegfried et al., 1994). Mussels, limpets, abalone, whelks, winkles, octopus, crabs, lobsters, barnacles, echinoderms, ascidians, and algae are collected for human consumption, as animal feed or as shing bait (Kingsford et al., 1991; Keough et al., 1993; Underwood, 1993a; Addessi, 1994; Siegfried, 1994). Numerous species of invertebrates, especially molluscs, are also collected for their ornamental value as marine curios (Wells, 1980; Newton et al., 1993). More recently

284 there has also been substantial increase in the collection of live sh and invertebrates for aquaria (Addessi, 1994). Substantial quantities of algae are collected from intertidal and subtidal habitats, e.g. over 180 000 t per annum in Chile and 30 000 t per annum in South Africa (Siegfried et al., 1994), for production of agar, alginates, carrageenans, and to a lesser extent as a food source, or as a fertiliser (Santelices & Grifths, 1994; Vasquez, 1995). Species with low dispersal are particularly vulnerable to overexploitation, as are isolated populations such as those on oceanic islands (see Webber et al., 1998). Harvesting can be divided into subsistence or recreational gathering and commercial collection. Subsistence gathering has taken place, for the most part in a sustainable manner, for at least 100 000 yrs (Siegfried et al., 1994; Kyle et al., 1997). However, this type of collection is having a greater impact with increasing use of non traditional equipment to facilitate harvesting, transport and storage snorkels, SCUBA, outboard motors, freezers etc. (Underwood, 1993a; Santos et al., 1995). Recreational collectors typically gather invertebrates to use as shing bait, as ornamental souvenirs, or for consumption (Underwood, 1993a) and while the take per person may be quite small (e.g. 3 to 4 crabs per person per day), cumulative effects can be considerable (Kingsford et al., 1991; Underwood, 1993a). Commercial harvesting is a more intensive form of exploitation and provides a substantial source of export income in some countries (e.g. US $200 million for Chile during 1980, Siegfried et al., 1994). It is more systematic and potentially more threatening than subsistence gathering since a few species are repeatedly targeted. Some studies have shown little effect of collection, indicating that resources are being removed in a sustainable manner (Kyle et al., 1997). However, in most cases target species are considerably less abundant, and are of smaller average size and biomass in areas where they are exploited than in comparable areas where collection is minimal (Hockey & Bosman, 1986; Castilla & Bustamante, 1989; Keough et al., 1993; Underwood, 1993a). Apart from direct effects on the particular target species, collection is also likely to have indirect effects on organisms which are not exploited, and hence the assemblage as a whole (Figure 3). This is especially true when the target species has a keystone role in structuring the community (Dye, 1992; Underwood, 1993a; Branch & Moreno, 1994; Grifths & Branch, 1997; Lasiak, 1998, 1999; but see Sharpe and Keough (1998) for an example of minimal indirect effects). Removal of grazers such as limpets or urchins, for example, has been shown to result in proliferation of micro and then macroalgae on the shore (Hawkins & Hartnoll, 1983; Branch & Moreno, 1994; Dye et al., 1994b; Lindberg et al., 1998). Conversely, removal of macroalgae leads to loss of habitat for small invertebrates which live amongst the algae, and will also create space which may become colonised by larger invertebrates, and opportunistic algae (Santelices & Grifths, 1994; Vasquez, 1995). Over-exploitation of large vertebrate predators, such as sea otters, which feed in the intertidal at high tide has also lead to extensive changes in community structure on some shores (Estes & Palmisano, 1974; see Estes & Duggins, 1995). Collection can also have indirect effects on predators, which rely on commercially collected organisms as a food resource. For example, over-exploitation of limpets is believed to have contributed to extinction of the Canarian black oystercatcher which feeds on these molluscs (Hockey, 1987). A range of management strategies is available to help reduce and regulate collection (for reviews see Underwood, 1993a; Dye et al., 1994a; Odendaal et al., 1994; Grifths & Branch, 1997). There are numerous examples where reductions in the amount of collection has led to an increase in the abundance of particular target species within protected areas (e.g. Castilla & Duran, 1985; Oliva & Castilla, 1986). Increases in the abundance of adults may also enhance local recruitment of juveniles (Prince et al., 1988; Davis, 1995), however evidence of enhanced recruitment to neighbouring areas is less apparent (see Castilla & Bustamante, 1989; McClanahan & Kaunda Arara, 1996). It is difcult to develop management strategies which will be generally applicable because of the variety and complexity of ecosystems. These problems are further complicated by temporal and spatial variability in recruitment to target populations (Hockey, 1994; Harris et al., 1998). Management strategies should therefore consider both the population and the community level of resolution (Keough & Quinn, 1991; Dye et al., 1994a; Grifths & Branch, 1997; Keough & Quinn, 1998). However, collecting and interpreting multi-species data in order to make predictions at the community level is difcult and may tend to obscure trends for individual species (Keough & Quinn, 1991). The complexity of resource management is illustrated by an example from marine reserves in Chile. Here a large predatory gastropod (Concholepas

285

Figure 3. (A and B) MDS ordinations based on Bray-Curtis indices of similarity derived from root-root transformed mean macrofaunal abundance and biomass estimates respectively (circles, ovals and squares represent study sites in the southern, central and northern region of Transkei respectively; open and shaded areas represent exploited and non-exploited sites respectively. Letters/number combinations (e.g. M1, M2, etc.) refer to specic localities see Lasiak (1999) for details. Reproduced with permission.

concholepas) is one of the main species collected commercially from the intertidal zone (25 000 t in 1980). Creating a reserve to exclude harvesters from the shore led directly to a dramatic increase in the abundance of C. concholepas and two species of limpet which had also been exploited previously. This was followed by a reduction in the abundance of mussels, one of C. conchelepas main prey items, and an increase in the abundance of algae. This was a transient state as grazing by limpets substantially reduced the abundance of algae, creating space which was subsequently colonised by barnacles. Hence reducing collection lead to varied and to some extent unpredictable changes in community structure and vertical distribution of these organisms (Duran & Castilla, 1989; Branch & Moreno, 1994). Both types of community (exploited and unexploited) are common along the whole coast of Chile and it is evident that human exploitation is affecting the shoreline at a landscape scale of resolution (Paine, 1994). Some management strategies may actually be counter-productive. For example, introducing a sizerestriction to prohibit removal of smaller individuals from the population may lead to a relative increase in the collection of larger more fecund individuals. For many marine invertebrates the greatest natural

mortality is on small individuals, with larger individuals escaping predation and making a major contribution to reproductive output (Underwood, 1993a). This can be especially important in protandrous species such as limpets. Hence a more appropriate strategy may be to have both lower and upper size limits. Lower limits would be set to allow most individuals to breed once or twice before harvest while upper limits would protect larger particularly fecund individuals and females in protandrous species. Mariculture may help reduce exploitation of natural populations. For example, in South Africa 75% of the mussel shery is now supplied from articially reared populations (Siegfried et al., 1994). Many marine algae have also been successfully cultivated (for review see Vasquez, 1995). There are, however, considerable environmental problems associated with intensive rearing in mariculture (for review see Ocean Studies Board, 1995). 5.7. Trampling and habitat degradation Habitat degradation as a result of either collecting organisms from the shore or by trampling on the shore, perhaps to gain access to the sea for swimming or SCUBA diving, is a major problem (Liddle & Kay,

286 1987; Hawkins & Roberts, 1992). There is a direct causal relationship between this type of human activity and damage to intertidal habitats. Damage from recreational visitors is more intensive during weekends and holiday periods (Kingsford et al., 1991; Vanherwerden & Grifths, 1991) and decreases with distance from the nearest point of easy access (Addessi, 1994; Pombo & Escofet, 1996). Experimental studies in temperate regions have shown that the abundance of barnacles, mussels and macroalgae may be directly reduced as a result of trampling with indirect changes (both increases and decreases) in the abundance of other species (Brosnan & Crumrine, 1994; Fletcher & Frid, 1996; Keough & Quinn, 1998). This may be accompanied by an increase in the amount of bare space and subsequent colonisation by opportunistic species (Povey & Keough, 1991; Fletcher & Frid, 1996). In the tropics, trampling on the reef at causes direct damage to both branched and massive corals (Liddle & Kay, 1987). Apart from physical damage to marine organisms, human presence may frighten away predators, such as oystercatchers which feed on the shore while the tide is out. This may have indirect effects on the abundance of prey species which are usually eaten by these birds (Lindberg et al., 1998). Somewhat ironically, marine reserves frequently become a focus for visitors to the seashore and there is concern that the recreational carrying capacity of shores in some reserves may be exceeded, leading to habitat degradation. If the reserve is large enough this problem can be reduced by restricting public access to a selected area, such as that adjacent to the car park (Fletcher & Frid, 1996). Ideally, measures to reduce habitat degradation should be considered in parallel with those aimed at reducing collection in the intertidal. This can be achieved as part of an integrated Coastal Zone Management plan where a range of strategies offering differing levels of protection are applied along a coastline with a view to maximising the total utility of the zone. Additional measures such as elevated boardwalks, fences, and visitor education may also be effective in reducing the amount of damage caused by each individual visitor (Carlson & Godfrey, 1989; Fletcher & Frid, 1996). However, recovery after the trampling disturbance is removed may be both variable and slow. Experimental studies on temperate shores have shown that some algal and barnacle cover returned after one year (Povey & Keough, 1991), while larger invertebrates such as mussels had not completely recovered ten years after trampling ceased (Dye, 1992; Brosnan & Crumrine, 1994). A nal consideration should also be given to the potential damage from scientic activity. Rocky shores provide a very tractable system and a great deal of research has been done on them. Some of the most studied shores are now riddled with remnants of previous research (drill holes, plastic screw anchors, screws, settlement tiles etc., pers. obs.). These activities tend to be very localised and the effects if any (we are not aware of any published work assessing this aspect) are likely to be minor (but see Bruton and Stobbs (1991) for evidence of overcollection by marine scientists). However, if scientists hope to credibly promote conservation strategies they must adopt a responsible attitude to ensure minimal damage (see Hawins (1999) for further discussion). 5.8. Siltation Rocky shore communities may potentially be impacted by increased sediment loading in the water column. This can result from urbanization of coastlines and watersheds in their hinterlands leading to suspended material being transported by rivers or run off into the coastal zone. It is also a problem in areas adjacent to intensive irrigated agriculture or where overgrazing has led to soil erosion. To date there has been considerable attention given to the impacts of increased silt load on coral reefs (e.g. McClanahan & Obura, 1997; Ochoa Lopez et al., 1998; Wesseling et al., 1999). In contrast this is a neglected area in rocky shore ecology, although some work, particularly in shallow subtidal habitats, has suggested that increases in sedimentation can lead to alterations in assemblages, including proliferation of algal turfs (Thom & Widdowson, 1978; Seapy & Littler, 1982; Airoldi et al., 1995, 1996; Airoldi & Cinelli, 1997; Airoldi, 1998; Airoldi & Virgilio, 1998). 5.9. Introduced species Intertidal communities are also subject to stress from species that have been introduced accidentally or intentionally by man. Most accidental introductions are transported as fouling on the undersides of ships, or in ships ballast water (for reviews see Lewis, 1964; Raffaelli & Hawkins, 1996). Elminius modestus became established in Europe following introduction by shipping during the Second World War (Lewis, 1964 for review). Although widespread in occurrence,

287 its impact on local barnacle assemblages is primarily restricted to estuaries and bays where it can become the dominant barnacle. On more exposed coastlines, it has stabilised at a lower level and appears to coexist with the native barnacles (Southward, 1991). Alternatively, species may be introduced as, or with, organisms which are transplanted for aquaculture. For example, the edible periwinkle (Littorina littorea) was introduced, probably accidentally, to the east coast of America in the middle of the 19th century where it had a major impact on rocky shore communities, and in some locations displaced the native mud snail (Ilynassa obsoleta) (Carlton, 1982, 1989). Other examples include introduction to Europe of the slipper limpet and oyster drill from America and the marine alga Sargassum muticum from Japan (Carlton, 1989; Critchley et al., 1990; Southward, 1991; Raffaelli & Hawkins, 1996). The range of Sargassum is increasing dramatically and has been shown to have modied macroalgal assemblages in northern Spain and the Pacic coast of North America (Walker & Kendrick, 1998). In many cases these introductions have not so far been found to have dramatic inuences on marine communities. However, the potential for major and probably permanent impact remains, especially if pathogens are transferred with introduced species and nd new hosts which lack natural resistance, as has occurred with Salmonids transferred for aquaculture and stock enhancement (for review see Jonsson & Flemin, 1993). of coastline, although the Gulf spills extended to 100s of kilometres. Clearly some stretches of rocky coastline have been chronically impacted for hundreds of years. For example, food collection in S. Africa and parts of the Mediterranean dates back into pre-history (Siegfried, 1994). In more developed countries this impact has probably lessened since medieval times. Industrial and domestic pollution is primarily a product of the last 300 yrs or so. Its impact is restricted to urbanized coastlines, especially embayed areas. The duration of these impacts in most instances is 100 yrs at most. In developing countries industrialization and population growth is accelerating the process (Morton, 1990; Da Silva et al., 1997; Liu & Morton, 1998). In countries which are losing their traditional heavy industries, reversal of degradation is occurring. Treatment of waste and tighter environmental regulations speed this process. Many coastal ecosystems are recovering, albeit slowly, and rocky shores in these areas are no exception (e.g. the Mersey and Liverpool Bay region, Hawkins et al. 1999a, b). Ironically, collection of mussels is prevented in many places by public health concerns due to sewage contamination. Thus in some instances pollution may actually lessen community level disruption. Disposable income, leisure time and availability of personal transport have all increased dramatically over the last 50 yrs. In some ways, the decline of subsistence gathering of food and fertilizer from the shore has been mirrored by an increase in recreationally-related impacts in the more developed world (Fletcher & Frid, 1996) and in areas of the third world which are being developed for tourism (Hawkins & Roberts, 1992). Paradoxically these impacts can be particularly heavy in reserve areas where public access is encouraged to promote awareness of conservation issues (Fletcher & Frid, 1996; Section 5.7). Table 3 is a tentative attempt to rank the importance of various anthropogenic disturbances and their impacts at the population or community level on rocky shores. We suggest that collection of food or other resources (e.g. algae for fertilizers, pharmaceuticals) in less developed countries probably has a greater impact on shores over very large scales (Section 5.6). Red tides whether natural or prompted by eutrophication, can have similar broadscale effects, but are periodic and acute (Section 4.2). Of the more chronic pollutants, TBT clearly has a marked effect on a limited suite of species (oysters and stenoglossan gastropods) at the individual or population level but

6. Overview 6.1. Scale and relative importance of impacts It is clear that rocky shores are subject to a variety of impacts on a range of spatial and temporal scales. On a global scale, there can be few pristine shores, even in the most remote regions. Most impacts are localized, associated either with point sources or urban areas with a diversity of diffuse inputs of contaminants and elevated recreational or food collection activities. On a broader scale, intensive use of the shore for food collection can cause impacts at a regional level over 100s to 1000s of kilometres (e.g. in Chile, reviewed by Paine, 1994). Eutrophication can also act on a broad scale (e.g. in the Baltic, Bonsdorff et al., 1997). Acute impacts are generally localized and most oil spills rarely cover more than a few 10s of kilometres

288 community level effects are not widely documented (Section 5.4). Potentially one of the most serious impacts on shores, because it is essentially irreversible is the introduction of alien species. These can markedly change community processes and ecosystem function (Section 5.9). 6.2. Recovery Assessment of the relative severity of stresses must consider the ability of shore communities to recover once disturbances cease. As for impacts, recovery is impossible to assess without reference to natural spatial and temporal variation (Underwood, 1989). The degree of natural variability differs among shores. On northern European shores, for example, sheltered areas are generally dominated by a community dominated by algae which is stable through time. Moderately exposed shores, on the other hand, have been shown to exhibit both small and larger scale uctuations in the relative cover of seaweeds or barnacles (Hawkins et al., 1992; Burrows & Hawkins, 1998 for reviews), making it more difcult to assess recovery. Designing sampling programmes to assess impacts and recovery requires careful consideration of such natural levels of variation (Underwood, 1993b, 1994). Our review suggests that rocky shores do not generally suffer persistent residual damage after an input has been stopped. Pollutants rapidly disperse and there are few sinks for pollutants, other than the biota themselves and possibly sediment trapped by algal turfs or animal matrices. Exceptions include baking of oil to form asphalt-like pavements high on the shore, which can persist for several years (Jones et al., 1998). Diesel oil has also been found trapped in kelp holdfasts up to 7 yrs after a spill on a sub-Antarctic island (Smith & Simpson, 1998). Peterson (in press) has suggested that oil spills are more of a press than a pulse disturbance. Most shore communities get back to some approximation of their original state(s) within 5 yrs or so after minor impacts. This process can be more prolonged after severe impacts; for example shores badly impacted by dispersants following the Torrey Canyon spill probably took 1015 yrs to recover. Recovery after physical impacts, such as food collection or trampling, can also usually occur rapidly once the disturbance stops. Unlike seagrass beds or coral reefs, rocky shores do not generally have major slow-growing biogenic structures, and can usually regenerate quite quickly. This depends on the species involved, however. Some species of algae and barnacles returned to experimental plots one year after trampling had ceased (Povey & Keough, 1991), whereas mussels had not completely recovered ten years after trampling ceased (Dye, 1992; Brosnan & Crumrine, 1994). Ascophyllum nodosum canopies can also take a very long time to recover following disturbance (Jenkins et al., 1999). Rapid recovery is aided by the open nature of rocky shores with recruitment via larval or algal propagules from remote unimpacted sources (Hawkins et al., 1999a). Whilst this is true for most species, slower recovery has been noted in animals with direct development (high shore littorinids following the Gulf oil spill, Watt et al., 1993; dogwhelks following TBT pollution, Gibbs et al., 1991a). Although rafting can occur, input from remote sources is much slower. With these species, a case could be made for reintroduction (see Hawkins et al., 1999a) but care must be taken that the correct genotype is re-introduced as these animals have considerable variability generated by local selection. 6.3. Approach In contrast to research on soft sediment communities, which often involves the use of multivariate techniques to consider the assemblage as a whole (e.g. Gray et al., 1990, Agard et al., 1993; Somereld et al., 1995), most of the papers reviewed here discuss responses of individual species or functional groups (e.g. dogwhelks, Gibbs et al., 1991; limpets, Tablado et al., 1994), indicator communities (e.g. kelp holdfasts, Bamber, 1991) or shifts in dominant suites of species (e.g. assemblage dominated by mussels to one dominated by coralline algae, Dye et al., 1994). If summaries of the entire community are discussed, it is usually in terms of diversity (e.g. Littler & Murray, 1975; Bamber, 1991). This ows from the classical approach to the study of rocky shores, based on experimental manipulation of one or more conspicuous species or functional groups with a view to unravelling the roles of individual species in community processes (e.g. Connell, 1961, 1972, 1974; Paine, 1974, 1977). This largely univariate approach has the advantage that it can characterise detailed responses of the selected dominant species, and it retains the focus on direct links between the disturbance and the response. Although the selected fauna/ora may be the most noticeable or tractable, however, they may not always be the most responsive to any given impact. Responses

289
Table 3. Tentative summary of relative impacts of different sources of stress on rocky shore communitites. To enable comparison among the different sources of stress, each has been given a score from 1 to 5 points, based on the literature reviewed
Source of stress Extent of impact [local/rare () broadscale/ common ( )] Developing world Developed world ? ? ?
?

Severity of impact [minor (, sublethal) severe ( , mass mortality of most species)]

#

Time to recovery [short (, 1-2 yr) long ( , 1015 yr) permanent ( )] spp. dependent # spp. dependent spp. dependent spp. dependent

Amount of eld research done

Toxic algal blooms Oil acute Oil chronic Nutrient pollution Heavy metals Antifouling paints Thermal pollution Harvesting Trampling (recreational) Introduced species

? not known; only example available: copper mine tailings (Castilla, 1996); # for dogwhelk populations.

of meiofauna on rocky shores, for example, have received very little attention (Gibbons & Grifths, 1986) and may in some cases be more sensitive at a community level than the macrofauna (Warwick, 1993). It may be informative to compare the responses of different sections of the community, or individual indicator species with responses of the community as a whole (see Somereld et al., 1995). This would serve as ground-truthing for existing approaches against the broader, multivariate background, and improve our capacity for early detection of impacts. 6.4. Way forward Predicting the likely impacts of disturbances depends on an understanding of the natural dynamics of the community (Suchanek, 1994). Although we have considerable knowledge of community-level processes that operate on exposed rocky shores (e.g. Underwood et al., 1983; Hawkins et al., 1992), particularly at certain well-studied locations, we have little understanding of communities on sheltered or estuarine rocky shores and articial substrata. These habitats are among those most likely to be impacted by human activities due to their proximity to urban areas and because contaminants are more concentrated in sheltered coastal waters than on exposed coasts. Research on such habitats should therefore be an urgent priority and models of community processes in other rocky habitats should be further rened and their spatial and temporal generality assessed (see Underwood & Denley, 1984; Foster et al., 1990; Underwood & Petraitis, 1993).

Research into anthropogenic impacts is needed at the basic level of identifying patterns of impact by comparing communities at putatively impacted rocky shores with those at unimpacted controls. Responses to many sources of stress, e.g. heavy metals, thermal pollution, have simply not been assessed in eld-based studies or at a community level (see Sections 5.3, 5.5). Experimental research to understand the mechanisms involved in impacts is also scarce, even for such highprole events as oil-spills (see Section 4.1). We should aim to be better prepared to extract more thorough, high-quality information from acute events, e.g. oil spills (Section 4.1). Wherever different management techniques are applied, the opportunity should be taken to determine how effective they have been, to compare different approaches and rene them for future application adaptive management (Walters, 1986, 1993). For example, comparisons of different methods for dispersing oil can help reduce the damage done during future clean-up operations (e.g. Watt et al., 1993). There is a particular need for long term studies. Long term effects of chronic sources of stress are particularly hard to distinguish from natural changes (Section 3; GESAMP, 1990). Carefully designed monitoring programs are required to identify such impacts and should also be accompanied by experimental research to enable identication of causative links (GESAMP, 1990). Recovery after acute events may also take several years and can only be studied properly over long periods of time (e.g. Torrey Canyon spill, Hawkins & Southward, 1992). Apparent shortterm recovery may simply be part of continued period

290 of increased variability or temporary convergence of populations or communities at impacted and control sites (Underwood, 1989). Such studies should include proper controls to enable analysis using Beyond BACI (Before After Control Impact) techniques (see Underwood, 1992, 1994). 6.5. Conclusions It is clear that the communities of chronically impacted shores can continue to function, albeit in a different state. On such shores, a proliferation of ephemeral, opportunistic species tends to occur and different communities converge towards a common altered (degraded) state. Although easily damaged, rocky shore communities are, on the whole, quite resilient and are able to recover if sources of stress are removed (see Grimm and Wissel (1997) for detailed denition of resilience and related terms). Communities on most impacted shores recover within 1015 yrs. This is due largely to the fact that the majority of species have a planktonic larval phase and can recruit to recovering areas from nearby populations. Thus, as long as some healthy populations persist, for example in marine reserves, management to allow recovery of impacted shores has a reasonable chance of being effective. The biggest problem in identifying anthropogenic impacts on rocky shore communities is the considerable spatial and temporal variation of the communities. This also means that recovery can be difcult to dene and measure. The ease of nondestructive sampling and relatively easy access does, however, allow the research required to describe spatial and temporal variation, understand its causes and to predict and identify community level responses to anthropogenic stress. and more recently by EU grant MAS3-CT95-0012 (EUROROCK).

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Acknowledgements The authors would like to thank Enid Scapaticci for text processing SJHs early scribblings, Sarah Anderson for chasing up references, Nick Smith for drawing the gures, an anonymous referee for valuable comments and Martin Attrill for his patience and input. TPC was funded by NERC Fellowship GR5/98/7/MS, RCT by Leverhulme Grant F180AO and SB by the Faculty of Science, University of Southampton. SJH has been funded by NERC for many studies relevant to this paper over the years

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