TP Crowe Stress in Rocky Intertidal Comm

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<ul><li><p>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</p><p>Impacts of anthropogenic stress on rocky intertidal communities</p><p>T.P. Crowe1;, R.C. Thompson1, S. Bray2 &amp; S.J. Hawkins1;21Biodiversity and Ecology Division, School of Biological Sciences, University of Southampton,Bassett Crescent East, Southampton SO16 7PX, U.K.2Centre for Environmental Sciences, University of Southampton, Highfield, Southampton SO17 1BJ, U.K.</p><p>Key words: anthropogenic stress, community, harvesting, human impact, introduced species, pollution,rocky shore, siltation, trampling</p><p>Abstract</p><p>Rocky shores provide a harsh environment for marine organisms and we briefly discuss natural sources of variationin community structure before considering anthropogenic impacts in detail. We review impacts caused by (a) acutedisturbances: 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. Commu-nity level effects are emphasised throughout and illustrative examples are drawn from field-based case studies.Particular attention is given to the lessons learned from oil spills and the effect of chronic pollution by tributyltinon dogwhelks, the impacts of which ranged from the biochemical to community levels of organisation. Impactsare placed in a global and historical perspective and the potential for the recovery of shores under appropriatemanagement is discussed. Finally we consider the relative merits of the multivariate and univariate approaches tostudying impacted communities and suggest priorities for future research.</p><p>1. Introduction</p><p>Rocky shores occur throughout the coastlines of theworlds oceans. They are the most extensive littoralhabitat on eroding wave-exposed coasts and are alsoa major habitat on more sheltered coastlines, such asfjords and rias. This already extensive natural habitatis further increased by the plethora of artificial hardstructures such as breakwaters, jetties, docks, groynes,dykes, sea walls which essentially function as artificialrocky shores.</p><p>Sheltered bays, fjords and rias are widely usedas harbours which range in size from small fishingports or marinas up to major industrial ports. Artificialshores generally occur in densely populated and oftenindustrialised regions, while even in remote places,rocky shores can be impacted by a variety of activitiesranging from subsistence collection of food throughto mining waste and occasional catastrophic oil spills.</p><p>* Corresponding author: Phone: 023 80594386; Fax: 02380594269; E-mail:</p><p>Thus many rocky shores are subjected to a variety ofstresses caused by human activities. These anthropo-genic stresses are superimposed on the stress causedby natural environmental factors such as emersion inair due to the tides and wave action (see Raffaelli &amp;Hawkins, 1996 for review).</p><p>In this review we start by briefly considering termsand definitions. We then outline natural stressors thatinfluence rocky shore communities and the problemof separating their effects from those of anthropo-genic stresses. We then consider acute and chronicanthropogenic stresses and review research into theirimpact on rocky shore communities. Special atten-tion is focussed on the acute impact of oil spillsand the chronic pollution caused by tributyltin inantifouling paints. We emphasise the need to inte-grate from individual responses up to the communitylevel. The discussion provides a global and historicalperspective. We consider the scales and relative impor-tance of different impacts and examine the potentialfor recovery of rocky shore communities. Finally</p></li><li><p>274</p><p>we highlight gaps in our knowledge and point outpriorities for future work.</p><p>We concentrate on the intertidal zone of rockyshores; coral reefs and subtidal habitats are outsidethe scope of this review but are occasionally discussed,particularly in relation to processes that have receivedlittle attention on rocky shores. Many of the ideas andexamples in this paper draw on publications in variousconference proceedings (e.g. Hawkins &amp; Southward,1992; Hawkins et al., 1994; Hawkins, 1999a, b)and we have taken the opportunity to integrate andsynthesise these into this review.</p><p>2. Terminology</p><p>A variety of terms has emerged to describeenvironmental disturbances and their effects. Theenvironment is contaminated by input of man-madesubstances, but pollution is only said to occur whenthe contaminant actually has an effect on a biolog-ical variable (Clark et al., 1997). Similarly stress is,broadly speaking, the response of a biological entity(individual, population, community, etc.) to a disturb-ance (or stressor). Hence anthropogenic stress is theresponse of a biological entity to an anthropogenicdisturbance. Stresses at one level of organisation (e.g.individual, population) may also have impacts on otherlevels, for example causing alterations in communitystructure. These terms are difficult to define preciselyand have been used in many different ways (see Parkeret al. (1999) for a detailed review). Inputs, disturb-ances or other sources of stress are generally describedas being either chronic or acute. A chronic disturb-ance operates at a low level over a long period, whilean acute disturbance is a discrete, usually large event.These terms are roughly analogous to the terms pressand pulse which are used to describe environmentaldisturbances of long and short duration respectively(Bender et al., 1984). This latter terminology wasrecently refined by Glasby and Underwood (1996).Their classification distinguishes between the durationof the disturbance and the duration of the response ofthe target organisms or community (the impact). Theyrecognised that, for example, a disturbance of eithershort duration (pulse) or long duration (press) couldcause either no response, have a short term impact orcause a long term change in a population. Careful useof clearly defined terminology will aid well-designedresearch into human impacts on rocky shores. Few ofthe studies reviewed below were designed to discrim-</p><p>inate among these alternatives, however, and impactswill be discussed by reference to the acute and chronicdisturbances that caused them.</p><p>3. Separating natural and anthropogenic stress</p><p>Rocky shore organisms are subject to two majornatural gradients of physical stress (see Raffaelli &amp;Hawkins, 1996 for review). First there is the verticalgradient of increasing stress with increasing exposureto air higher on the shore, due to the alternation ofthe tides. This gradient is essentially unidirectionalfor most marine organisms and is present on bothmicrotidal (e.g. </p></li><li><p>275</p><p>which are equally effective in avoiding short pulses ofpollutant as spells of low salinity or emersion. Manyorganisms have well developed sensory mechanismsto detect and hence respond to stressors (e.g. Akberali&amp; Davenport, 1982) and can also detect and respondto pollutants such as heavy metals (e.g. Redpath &amp;Davenport, 1988). Many intertidal algae are equallyresilient and are able to tolerate considerable uptakeof heavy metals (Barreiro et al., 1993; Castilla, 1996)and withstand oil spills and dispersant application.Thus it is sometimes difficult to detect the effectsof anthropogenic stress at the level of the individualorganism.</p><p>Impacts are more often investigated at a popula-tion or community level. Populations and communitiesexhibit considerable variability in space and timeunder the influence of many physical and biologicalfactors (e.g. Hartnoll &amp; Hawkins, 1985; Underwood,1985; Foster et al., 1988). On rocky shores, dramaticnatural fluctuations can be caused by factors suchas extremes in temperature (Crisp, 1964), red tides(Southgate et al., 1984) and variations in recruitmentsuccess (e.g. Bowman &amp; Lewis, 1977; Caffey, 1985;Gaines et al., 1985; Underwood &amp; Fairweather, 1989).Against such a background of variation, it is oftenextremely difficult to detect reliably the additionaleffects of human activities.</p><p>The difficulties in detecting the comparativelyminor effects of low-level chronic stress at thecommunity level on rocky shores have been appre-ciated for some time (Lewis, 1976, 1977; Hawkins&amp; Hartnoll, 1983; Hiscock, 1985). In most cases,for community level effects to be expressed anddetected, the disturbance must either come from apoint source (e.g. a large effluent) or a catastrophicevent (e.g. an oil spill or the aftermath of a redtide). Recently the need for properly designed impactassessments has been emphasised (Underwood, 1992,1994). Such designs involve repeated sampling andcomparison with multiple control or reference sitesenabling natural spatial and temporal variation tobe objectively separated from putative impacts (seeUnderwood, 1992, 1994).</p><p>The majority of work on rocky shore communitieshas tended to concentrate on selected prominentspecies or functional groups analysed in a univariatemanner. Multivariate analysis of whole communities,which is common in research on soft sediment biota(e.g. Gray et al., 1990; Agard et al., 1993; Somer-field et al., 1995), has not been so widely used (butsee Hockey &amp; Bosman, 1986; Fuji &amp; Nomura, 1990;</p><p>Lasiak &amp; Field, 1995; Underwood &amp; Skilleter, 1996;Coates, 1998; Lasiak, 1998, 1999). The large amountof experimental community ecology that has beendone on rocky shores, however (Connell, 1972; Paine,1977, 1994; Underwood et al., 1983, Hawkins etal., 1992), often allows good interpretation of likelyimpacts on particular species and, in some cases,communities.</p><p>4. Acute anthropogenic disturbances</p><p>4.1. Oil spills</p><p>The best-recorded community level impacts ofanthropogenic stress are from oil spills. These havebeen well documented on rocky shores (Clark et al.,1997). Details of selected major spills are summarizedin Table 1. Most of these spills led to oil beingwashed onto rocky shores, but the major spill in theArabian/Persian Gulf during the Iraq/Kuwait warimpacted mainly depositing shorelines, althoughsome rocky areas were affected (Watt et al., 1993;Jones et al., 1998). Where oil became stranded on lowenergy depositing shores or mangroves, recovery wasgenerally slower than on more wave exposed rockyshores.</p><p>Table 1. Selected major oil spills (modified from Hawkins &amp;Southward, 1992)</p><p>Ship or installation Date Oil spilt Oil beached(tons) (tons)</p><p>Persian Gulf Jan 91 &gt;1million ?Ixtoc 1 3 Jun 79 500 000 12 000Amoco Cadiz 16 Mar 78 233 000 80 000TTorrey Canyon 18 Mar 67 100 000 35 000Braer 5 Jan 93 85 000 ?Sea Empress 21 Feb 96 72 000 515 000Khark 5 19 Dec 89 70 000 ?Metula 9 Aug 74 51 000 42 000Exxon Valdez 24 Mar 89 38 000 4 500Urquiola 2 May 76 30 000 25 000Aragon 30 Dec 89 25 000 ?</p><p>Some costly early mistakes were made in cleaningup oil spills which often led to more damage beingdone during clean-up than caused by the oil itself (seeFoster, et al., 1990 for review). For example, as aresult of the Torrey Canyon oil spill in Cornwall, the</p></li><li><p>276</p><p>major damage was not caused by the 10 000 tons ofoil which came ashore, but by excessive treatmentwith over 14 000 tons of first generation dispersants.These were later shown to be very toxic to marinelife (Corner et al., 1968). The dispersants killed thegrazer Patella vulgata, and, to a lesser extent, otherherbivores such as Monodonta lineata and Littorinaspp. This reduction led to dense growth of ephemeralgreen algae followed by an equally dense growth offucoids. This proliferation occurred on many of theexposed and moderately exposed shores of south-westCornwall (see Smith, 1968; Southward &amp; Southward,1978; Hawkins et al., 1983; Hawkins &amp; South-ward, 1992; Hawkins et al., 1994 for further details).Similar, but more localised, flushes of ephemeral algaeand fucoids were shown after the Braer (Newey &amp;Seed, 1995) and Sea Empress spills (Moore, 1998).Some dogwhelks survived the Torrey Canyon spilland were able to reproduce locally under the shelterof the fucoid canopy (Bryan, 1969). Barnacles wereonly affected in areas that were cleaned repeatedly.Over the next few years, however, they succumbedto smothering by algae and predation from the nowdense populations of dogwhelks. Of greatest signifi-cance was the highly favourable environment for thesettlement and early survival of Patella vulgata createdby the fucoids. Patella depressa remained scarce in thearea until the mid 1980s (see Southward &amp; Southward,1978; Hawkins &amp; Southward, 1992).</p><p>We now have over 20 yrs of observations on therecovery of the shores affected by the Torrey Canyonspill. We also have a good background knowledge ofspatial and temporal variation of these systems to putthe results into context (see Southward &amp; Southward,1978; Hawkins et al., 1992a). Recovery of key speciesto previously observed normal levels of spatial andtemporal variation was judged to have occurred within1015 yrs. This recovery was through a series ofdamped oscillations (Southward &amp; Southward, 1978;Hawkins et al., 1983; Hawkins &amp; Southward, 1992)and a similar pattern is starting to emerge since themore recent Exxon Valdez spill (Paine et al., 1996).Disruption of the community to such a vast extentresulted primarily from the widespread killing ofPatella. These limpets can be considered a keystonespecies on moderately exposed and exposed shoresthroughout the northeast Atlantic because of theimportance of their grazing (see Hawkins et al., 1992for review; Mills et al., 1993; Power et al., 1996;Raffaelli &amp; Hawkins, 1996; Hurlbert, 1997 for recentcritiques of the keystone concept).</p><p>Since the Torrey Canyon spill there has been muchwork on the impacts of other spills both large (e.g.Myers et al., 1980; Conan, 1982; Shaw, 1992; DeVogelaere &amp; Foster, 1994; van Tamelen, 1997; Joneset al., 1998) and small (e.g. Bowman, 1978; Popleet al., 1990; Lopes et al., 1997; Smith &amp; Simpson,1998). Over the years various overviews and reviewshave been written (e.g. Southward, 1982; Lewis,1982; Hawkins &amp; Southward, 1992; Suchanek, 1993)which summarize a diverse and often grey literature.Paine et al. (1996) and Petersen (in press) both ablysummarize the explosion of literature following theExxon Valdez spill.</p><p>Oil spills have variable effects on the biota. Somespecies can be remarkably tolerant of oiling (e.g.barnacles, Southward &amp; Southward, 1978; mussels,Newey &amp; Seed, 1995), although generalization isdifficult as the degree of mortality of a particulargroup of animals varies among locations and with oiltype. For example, Smith (1968) and Southward andSouthward (1978) showed oil tolerance in barnacles insouth-west England to Kuwait oil following the TorreyCanyon spill whilst Newey and Seed (1995) demon-strated a decrease in cover due to Gullfaks Norwegiancrude oil following the Braer spill. Newly settled spathave also been shown to be much more resilient thanadults (Bonsdorff &amp; Nelson, 1981). Other specieshave been impacted more by clean-up operations....</p></li></ul>