Marine Ecological Research in Seashore and Seafloor Systems: Accomplishments and Future Directions

MARINE ECOLOGY PROGRESS SERIES I Published March 31 Mar Ecol Prog Ser

REVIEW

Marine ecological research in seashore and seafloor systems: accomplishments and future directions

James A. Esteslr*, Charles H. peterson2

'U.S. Geological Survey, Biological Resources Division, A-316 Earth and Marine Sciences Building, University of California, Santa Cruz, California 95064, USA 'Institute of Marine Sciences, University of North Carolina at Chapel Hill, Morehead City, North Carolina 28557, USA

ABSTRACT Research in seashore and seafloor communlt~eshas contributed mmensely to the conceptual growth of ecology Here we summarize some of the most Important findings and discuss needs and opportunities for future work Dispropoi t~onatelylarge numbers of the most influential contrlbutlons are derived from studies of rocky short 5 and coral reefs because aspects of these systems (accessibility) and of their most common species (sessile or weaklv motile, high density short generation tline) make them well suited to manipulative experiments Foremost among the research contributions froin seashore and seafloor systems are increased understanding of (1) competition and consumer-prey interactions, (2) trophic cascades and other Indirect specles ~nteractions (3) the evolution of defense and resistance in consumer-prey systems (4) the importance of propagule transport and recruitment vanat~onto adult populations (5) the impacts of physlcal d~sturbanceand (6) the generation and maintenance of specles diversity on ecological t~rnescales We acknowledge the importance of manipulative expenments in the growth of marine ecology but question whether a stnct adherence to this approach will best serve future needs Some of the most pressing needs for future knowledge are (1) documenting the complex influences of spatial and temporal scales on ecological processes, (2) identifying the role of large, mobile predators in manne ecosystems, (3) understanding factors hmitlng manne autotrophs, (4)integrating historical biology and neontology and (5) appreciating intersystem linkages Increased attention to conducting arrays of expenments, taking measurements and observations, and documenting change at larger scales of space and time will provlde lnsights that are unattainable by the commonly used methodological protocols Novel approaches, including (1) evaluating and managing human disturbance for the loint purpose of conservation and learning, (2) developing stronger ties between scientists worhlng in open-ocean and near-shore systems and (3) developing collaborative prolects among scientists In the academic governmental, and pnvate sectors are required to understand many of these processes

KEY WORDS: Coral reefs Ecological concepts . Kelp forests . Novel approaches - Rocky shores , Unconsolidated substrates

INTRODUCTION munities, and ecosystems. Marine and estuarine systems associated with the seafloor, especially on coastal The broad goal of ecological research is to under- hard substrata, have contributed substantially to this stand the structure and dynamics of populations, corn- agenda. Here we review important conceptual advances that are based on research in seashore and seafloor - systems, the system-level characteristics and research 'E-mail: jestesCncats ucsc edu approaches that have led to these contributions, the

O Inter-Research 2000 Resale of fullarticle not permitted Mar Ecol Prog Ser 195:281-289, 2000

resulting strengths and limitations of current know looked for them in these habitats. The suite of charac- ledge, and visions of what is both possible and neces- teristics of these hard-substrate systems in shallow sary to move the field toward interesting and useful water makes manipulative experiments both feasible new horizons. Our focus is on spatial patterns and tem- and profitable, an approach that has come to dominate poral dynamics of populations and communities, the ecological research in hard-substrate systems in recent processes that explain them, and the level of success decades (Dayton & Oliver 1980, Paine 1994, Rafaelli & that science can achieve in understanding and predict- Hawkins 1996).Experimental manipulation is far more ing those patterns and dynamics. This is not a com- limited in the deep sea, but the development of man- prehensive, in-depth review, but rather an overview, ned and unmanned research submersibles has created strongly influenced by our own experiences and per- new opportunity for exploring ecological dynamics in spectives. Despite our potentially non-representative these systems (e.g. Thistle & Levin 1998). viewpoints, however, the ideas expressed in this review A list of contributions from research in hard-sub- have been exposed to and modified by extensive input strate marine systems would be vast. One need only from dozens of our colleagues in the field of ocean peruse titles from the general ecological and marine ecology. specialty journals to see this. Several recurrent themes Marine ecological systems associated with the seafloor emerge from the profusion of research. A substantial occur from near the poles to the equator and from the proportion of papers addresses pair-wise interactions intertidal zone to the deepest ocean bottom; thus, they among species or guilds of species. Most of them focus are necessarily characterized by immense taxonomic on competition (Connell 1983) or consumer-prey inter- and physical/chemical variation. This variation can be actions (Schmitt 1987). Definitive evidence for the im- categorized in numerous ways. We divide it in the tradi- portance of both processes is provided by studies of tional fashion by substrate type-hard versus unconsol- numerous taxa in many areas of the world. A second idated (soft)-because this is a recurrent and reasonably theme concerns the indirect effects of apex consumers dichotomous distinction among marine benthlc systems, on lower trophic levels (Power et al. 1996). Indirect and the methods used and many of the processes inves- effects of apex predators typically play out in 1 of tigated segregate accordingly. Most work on population, 3 ways-via trophic cascades, in which top consumers community and ecosystem dynamics has come from facilitate autotrophs by limiting populations of mid- studies in nearshore and estuarine environments, and level consumers (Fretwell 1987, Carpenter & Kitchell our presentation is weighted accordingly. 1993); via preferential consumption of competitive do- minants, which frees limiting resources and enhances diversity among competitors (Paine 1966, Connell1978); STATE OF THE FIELD or via positive species interactions including, especially, provision of biogenic habitat by 'bioengineers' Hard-substrate systems (Jones et al. 1994). Studies built around the second of these processes provide important evidence for the Hard-substrate systems are common from the inter- Intermediate Disturbance Model of species diversity tidal zone to the deep sea, and notably include inter- (Connell 1978, Lubchenco 1978, Sousa 1979). A third tidal rocky headlands, boulders, and limestone benches theme to emerge from research on coastal marine sys- (Connell 1972, Sousa 1979, Underwood & Denley tems concerns the ecological and evolutionary roles of 1984), shallow subtidal rock walls (Witman 1987) and defense and resistance in consumer-prey interactions reefs (Connell et al. 1997), seamounts (Genin et al. (Hay & Fenical 1988). Although there is empirical evi- 1986, 1989, Keating et al. 1987), and hydrothermal dence of defense and resistance for a variety of trophic vents, where rocky crust is being actively formed levels, geographic regions, and modalities of defense, (Grassle 1986, Tunnicliffe 1991). Our focus is mainly the most well-developed findings concern the role of on shallow-water systems-rocky shores, coral reefs, secondary plant metabolites in plant-herbivore interac- and kelp forests. All 3 systems have been productive tions withtropicaYsubtropica1 reef systems. A final arenas for ecological research because they are com- theme of conceptual importance is 'supply-side ecol- paratively easy to access and observe; many of the key ogy'-the notion that dispersive life history stages organisms are abundant, sessile or weakly motile, and (usually spores and larvae) significantly influence the have short generation times; and some strong inter- population dynamics of adult stages in species with actions among species tend to characterize specific complex life cycles (Sale 1977, Doherty & Williams systems (Paine 1980, Menge et al. 1994). This is not 1988, Roughgarden et al. 1988, Underwood & Fair- to say that all species are strong interactors (most may weather 1989, Caley et al. 1996). Larval characteristics not be), but rather that at least some strong interactors and physical transport processes are also important in have been found virtually everywhere scientists have explaining the rapid colonization of habitat patches in Estes & Peterson: Mdr~neecologiccll r-esearch in seashore and sedfloor systems 283

dynamically open systems, such as newly created inveltebrates in many shallow habitats that lack such hydrothermal vents (Mullineaux et al. 1995). structural barrlers to foraging as aquatic vegetation or shell debrls (Peterson 1979, Oliver & Slattery 1985, Olafsson et a1 1994, but see Rafaelli & Hall 1992) Soft-substratesystems (3) Impoitant demonstrations of tri-trophic lnteract~ons have emerged from estuarine experiments, showing Unconsolidated sediments characterize the sea floor that fish, wading bird, dnd sholebird predation IS often over a large fraction of the global ocedn Habitats iange directed preferentially towards predatory crustaceans, from intertidal sandy beaches and protected estuaiine large predatory polychaetes, or small demelsdl fishes mudflats to deep-sea deposits Physicdl legime and thereby releasing populdtlon cont~olson thelr smaller water depth, whlch in turn lnfluerlce sediinent distur- ii~~c,rtebrdteprey (Kneib & Stiven 1982, Commlto & bance and grain size, play domindnt loles in establish- Ambrose 1985, Wilson 1986, Kneib 1988) (4)The strong ing community composition and character in marme interactions significant to soft-sedlment community soft sediments (Hall 1994) dynamics do not generally include lnterspeclfic coin- Study of the dynamics of soft-sediment populations petition, but lnstead involve e~therpledation and phys- and communities has an almost century-long history ical disturbance of the sediments 01 tlansfolmation of dating froin early Scandinavian pioneers Some of the the physical habitat by creatliig an emergent or seabed initial focus of this work addressed questions of the re- structural habitat (Nowell & Jumars 1984, Peterson lationships between benthlc invertebrate-prey resour- 1991, Hall 1994) (5)Food limitation IS generally impor- ces and demersal fishes in the North Sea (Blegvad tant to both main functional groups of basal consumers 1928) In the inid 20th century other Scandinavian ln soft sediments-deposit and suspension feeders marine ecologists made imp01tant advances in relating (Levinton & Lopez 1977, Peterson & Black 1987) Sea- ieproductive modes and larval life histolies to dispersal sonal food availability contiibutes on a laige scale to and recolonization dynamics of benthic invertebrates temporal dynamics by inducing pulses of reproductive (Thorson 1950, Segeistralc 1962) Modern rc,scdrch hds actlvity and settlement, but on local scdles it is growth stressed experimental approaches in evaluating the rate not abundance that responds most commoi~lyto roles of physical and biological disturbance in organiz- competition for food in this system (Wildlsh & Krist- ing soft-sediment systems (Woodin 1Y7b FImclren et a1 manson 19971 1986 Hall 1994) By integrating fluid dynamics and sediinentology with ecology, much progress has been made ln understanding recruitment dynamics of soft- DEVELOPMENT OF INNOVATION sediment invertebrates (Eckman 1983, Nowell & Jumais 1984, Butman 1987, Olafsson et a1 1994) Interdiscipll- Ecologists may differ gredtly in the11 pe~sonallists nary research also has characteiized the significant of the most Interesting conceptual developments in un- historical focus on habitat relationships in soft-bottom derstandlng the dynamlcs of benthic/demersal marine environments (Snelgrove & Butman 1994) ecosystems Regardless of one S perspective, it is easy Listing the major contributions of soft-sediment to embrace the view that marlne ecology has long been lnvestlgations to our general understanding of the and continues to be a productive area of scientific dynanilcs of natuial systems is necessailly idlosyn- iesearch, and thus that exteinal guidance, infiastruc- crdtic Nevertheless, many people would include the tural changes, and imposition of new visions iepresent folloxvlng facets (1)The study of soft-sediment benthic unnecessdry interference with a successful formula communit~esas a function of water depth has revealed Under this philosophy, an effective strategy for fund- the maintenance of extremely high species diveisity at ing agencies might be simply to let science proceed in great depths with diversity increasing with global the future as it has in the past, banking on the ex- aiea of habitat despite the low ldtes of energy provi- pectation that continued productivity by a renewable sion (Grassle 1989) Although the mechanisms res- resource of imaginative scientists will piovide the sub- ponsible fol these depth-related patterns are still In strate for intellectual growth th~ough~ndlxridual and question, this work has produced many conceptual collaborat~vecreativity and original syntheses of accu- contnbut~onsto theories of biodiversity maintenance mulating knowledge A critic of this philosophy, on (Rex et a1 1993, Pineda & Caswell 1998) Research on the other hand, could reasonably make the following evolution dnd maintenance of coral diversity has had argument while hlstory clearly indicates past suc- similarly large impacts on understanding biodiversity cesses (as briefly discussed above) and staying the (Connell 1978, Hughes 1989, Jackson 1991 Kailson & course promises even mole in the future, the very Cornell 1998) (2) Predation by crustaceans and fishes methods that have led to these successes and the con- has been shoivn to reduce density of soft-sediment ceptual themes that have emerged from them con- 284 Mar Ecol Prog Ser 195: 281-289,2000

dition our thinking, constrain our creativity, and inhibit (GIS) mapping and analysis and in satellite imagery our capacity for innovation. We believe that there is to investigate ecological processes on larger spatial truth in both perspectives, that these views are not scales than was possible heretofore. mutually exclusive, and that an effective agenda for Large, mobile predators. Understandably, ecologists research should thus contain elements of each philoso- have focused attention on those species they could phy Our major motivation for writing this paper is to most easily manipulate, i.e. small to moderately sized address issues that emerge under the latter view and organisms that do not wander widely and are abun- thereby encourage marine ecologists to consider hon- dant in small areas amenable to experimentation. This estly and thoughtfully how they may break through selectively excludes certain groups of species from constraints of vision that they may not even recognize study, thus providing a potentially biased picture of exist. What, then, would we like to know about sea- important patterns and processes in benthiddemersal shore and seafloor systems and what opportunities systems. Scientists have speculated about the ecologi- exist for facilitating the novel research needed to ob- cal ro1.e~of such highly mobile groups as marine mam- tain that knowledge? mals, birds, and large fishes, but have not known how to incorporate them adequately into compelling evalu- ations. This problem is exacerbated by the fact that Critical gaps in understanding prevailing standards of scientific rigor (which empha- size experimental manipulation, replication, and local This section identifies important issues that are still controls) that are often achievable in st.udies of rela- poorly understood. With each, we discuss opportuni- tively small-bodied, sessile or weakly mobile species ties for catalyzing novel and recent developments in (Paine 1994) are difficult or impossible to meet in technoiogy that offer hope of progress. addressing such questions for large, highly mobile Scale. This is an older issue (Dayton & Tegner 2984, components of the ecosystem. Furthermore, many Levin 1992), although it is as topical and elusive now as scientists who study mobile marine vertebrates as- ever before. Some of the questions pertaining to scale sume a strong bottom-up vicw of ecosystem dynamics, are: (1) Over which dimensions of space and time do the thereby creating a perspective of 'response to' rather most significant organizing processes operate? (2) Can than 'effect on' their environment as the domain of measurements to understand these processes be scaled inquiry. New approaches-ranging from technolo- accordingly, or must they be? and (3) What are the gical to conceptual to philosophical-are needed, f0.r patterns of generality and variation within and across research on these species. Natural history observa- processes and ecosvstems? These important questions tions, usually obtained opportunistically, often are a have led to considerable debate. Their relevance to source of significant ~nsightinto the ecological roles of ecology also transcends coastal and seafloor marine these elusive creatures. Recent advances in the devel- ecosystems. We see several opportunities for increased opment of instruments for tracking and measuring the understanding of questions of scale and, as in the past, behavior and phys~ologyof large, mobile marine ver- work on benthiddemersal marine systems could play a tebrates promise new insights into such questions as leading role. One such opportunity is the use of meta- where and how they forage (Gentry & Kooyman 1986, analyses to evaluate patterm across multiple studies Block et al. 1993, Davis et al. 1999). Further under- (Gurevitch & Hedges 1999). An emerging scientific standing of their roles in community organization and culture of ecological synthesis needs to be cultivated dynamics could be obtained in 4 ways: (1) excluding and supported. The rich informational base from past them from areas where they are otherwi.se abundant, research in benthiddemersal systems seems ripe for (2) protecting them in areas where they are otherwise such an approach, and recent examples are exciting rare or have become rare due to exploitation, (3) track- and encouraging (Menge et al. 1994, Caley et al. 1996). ing long-term changes in populations and communi- A second opportunity is conducting experimental stud- ties in response to intentional management actions, ies on varying spatial and temporal scales (Thrush et and (4) using historical data from archaeology or al. 1997a,b). This has always been possible, but is paleontology to infer relationships between commu- rarely done. Long-term data sets, sometimes even ut~l- nity structure and the presence-absence of large izing historical, archaeological or paleontological in- mobile predators. Using marine reserves for large- formation, have provided novel temporal perspectives scale experiments is a useful approach for studying on marine systems (Simenstad et al. 1978, White 1987, some species. Because of the dramatic impacts of fish- Allen & Smith 1988, Dayton 1989, Baumgartner et al. ing, especially on seafloor communities in the coastal 1992, Connell et al. 1997, Jackson 1997, Dayton et al zone (Dayton et al. 1995), the use of reserves as an 1999). A third opportunity comprises the potential use adaptive management experiment is especially pro- of new technology in Geographic Information System mising (Lauck et al. 19981. Estes & Peterson- Marme ecological resc,arch in seashore and seafloor systems 285

Limiting factors on autotrophs. Plants have long to understand organizational processes within each. commanded particular attention in ecological studies One notable exception is 'supply-side ecology' (Gaines because of their pre-eminence in controlling the flux of & Roughgarden 1987, Roughgarden et al. 1988),where- energy and nutrients and because of the~rimportance in the oceanic realm is recognized as a potential trans- as 'ecosysten~engineers' (sensu Jones et a1 1994) In port vector for the dispersive life-history stages of prov~ding or modifying structural habitat fol other otherwise sessile and weakly motile species. Presently, organisms Four factors are thought to limit marlne this is an area of active research in marine ecology. plant populations-physical disturbance, herbivoly, Similar interactions between the physical transport light, and nutr~entsWhile there 1s abundant ev~dence vectors such as internal waves and benthic organisms for each, a broad synthesis of thelr joint influence 1s and communities have been responsible for reinark- lacklng for 2 maln reasons f~rst,past stud~eshave able new discoveiies on subtidal rock walls (Witman et tended to focus on slngle fdctors, second, methodolog- al. 1993) and coral reef envii-onments (Leichter et al. ical differences among different investigators have 1996). Otherwise, the nature and importance of link- made geograph~cand taxonomic contrasts difficult to ages among various marine and even terrestrial eco- interpret Both problems are technically resolvable- systems are poorly known. Coastal benthiddeinersal the first by conducting multl-factor~alexperlinents and systems are especially interesting in this regard be- the second by establish~nga programmatic lnfrastruc- cause they are juxtaposed with the land on one side ture wherein s~milarapproaches are used to study and the open sea on the other, and in both cases sig- dllferent areas and d~fferentspecles nificant linkages between systems occur via physical Historical biology. Ecologists working on marlne (oceanic, atmospheric, riverine) and biological (mobile benthic/demersal systems seem to have taken an un- species) transport mechanisms (Polis et al. 1997, Paerl usually stiong ex~stential/neontological view of the et al. 1998). New opportunities for the study of such world, thus endeavoiing to undeistand the workings of processes are available with recent developments in maiine systems from the perspective of extant specles isotopic analyses, remote sensing, satellite imagery, characterlstlcs and community compos~t~onw~th rela- CIS technology, and instrumentation for tracking ani- tlvely l~ttlethought given to hlsto~ythat extends be- mals at sea. yond individual memory Iinportant new Insights can be obtalned when ecologists expand thelr time scales to Include evolutional y p1 ocesses and historical events OPPORTUNITIES AND CHALLENGES (Simenstad et a1 1978, Jackson 1991, Steinberg et a1 1995) This goal is best ach~evedby ecolog~sts101n1ng As 1s true for any successful endeavor, one challenge forces with b~ogeographers,h~stor~ans, archaeolog~sts faced by benthlc/demeisal ecologists 1s to shed the con- and paleontologists The knowledge of recent historl- stralnts of tradit~on-not absolutely, for the value of cal status of community compos~tlonand population small-scale nlanipulat~veexperiments has not and may abundance can help disciimlnate between climat~c never run ~tscourse, but sufflc~entlyto recognize other explanat~onsfor change such as climatic iegime sh~fts needs, to more freely explore opportunities, and perhaps

(Anderson C? P~att1999) and human explo~tat~onor even to rethlnk the standards of sc~ent~ficInference hab~tatmodificat~on (Martin 1973) In add~tionevalua- While admittedly something of a potpourri, we urge that t~onof longer histories of community composition pro- prograrnrnatlc ~nfrastructuresbe Implemented to em- vides Insight into the evolut~onary cond~t~onsand phasize or take advantage of the following Issues interactions that shaped the species that we study today Use of moleculai genetic techniques offers special promise in defining the geographical d~mens~ons Effects of human exploitation of populations and taxonom~c relationsh~ps among specles Thls molecular approach will also help define Human activities perturb natural ecosystems on the spatlal structure of explo~tedpopulat~ons whlch is scales than cannot be achieved for the purpose of certa~nto Improve management and clar~fyrelation- learning alone. For instance, there is little doubt that ship between the openness of populat~onsand diver- fisheries have dramatically affected fish stocks and sity maintenance especially crltlcal to understanding marine communities (Dayton et al. 1995, Botsford et al. the deep sea (Powers et a1 1990) More work at the 1997, Pauly et al. 1998).While most emphasis has been Interface of ecology and evolution promlses excitlng on simply documenting the effects of fishing on fishes, new d~scoveiies(Palumb~ 1992) the fact that so many coastal fish stocks have been Linkages among ecosystems. Most prlor research on depleted provides numerous opportunities for under- marlne benth~c/demersalsystems has proceeded by standing their ecological roles. Marine reserves, to the identifying or deflning specif~csystems and attempting extent that they protect fish stocks from depletion and 286 Mar Ecol Prog Ser 195: 281-289, 2000

enhance their recovery, also should be looked to as this approach to marine ecosystems are undefined important research opportunities (e.g. Alcala & Russ (Botsford et al. 1997). An example of the potential util- 1990, Lauck et al. 1998). ity of merging sclence and management IS the development of marine protected areas for the joint purpose of conserving exploited populations, assessing popula- Long-term, large spatial-scale studies tion-to-ecosystem-level impacts of fisheries, and deter- mining the roles of large predatory flshes in ben- The vast majority of even the best research on thiddemersal communities. While fishing is perhaps marine benthiddemersal systems has been done over the most well known agent of anthropogenic influence a period of just a few years at 1 or 2 sites. Benthlc on marine ecosystems, eutrophication is another pro- ecologists must expand their efforts to encompass cess that is dramatically transforming estuari.ne and longer and larger scales (Brown 1995). Some work of shallow coastal systems in some parts of the world this nature has been done (e.g. Connell et al. 1997), (Turner & Rabalais 1994, Nixon 1995, Paerl et al. 1998). mostly through the initiative of individual investigators Much research has been devoted to understanding the rather than as a consequence of programmatic infra- effects of nutrient loading on phytoplankton (without structures. The few data available are sufficient to yet adequate understanding of the dynamics of nui- demonstrate that these approaches produce important sance blooms). Yet the food-chain consequences of insights not otherwise attainable (see Brown & Heske nutrient loading, and how change in productivity and 1990 for a terrestri.a.1 example, Estes et al. 1998 for a composition of the microalgal assemblage alters the marine example). composi.tion, production, interactions and dynamics of consumers at higher trophic levels are unknown (Paerl et al. 1998). The use of environmental management on Population consequences the scales of watersheds for large-scale experiments, with resource managers working in conjuncti.on wlth Most experimental studies in marine benthiddemer- marlne ecologists, holds tremendous promise for an- sdl communities have emphasized mechanisms and swering important questions about system dynamics processes, but few have expanded these mechanisms and the sustainability of ecosystem services. and processes to demonstrate population-level effects. The main reason for this failure is that the research is not conducted for sufficiently long periods or/and over Biodiversity sufficiently large areas. Since species and populations are the essential currency of applied ecology and the Biodiversity has emerged as a powerful scientific grist of evolution, future research is needed to bridge and social allegory, largely because species and pop- this gap from the qualitative to the quantitative. Fur- ulation~ are being lost at alarmingly high rates thermore, innovations to our understanding of the gen- from many terrestrial systems (Soule & Sanjayan 1998). eration of population and even community dynamics The oceans are a paradox in this regard (Roberts & can come from studies relating individual behavioral Hawkins 1999). On the one hand, some of the strongest or physiological responses to environmental forcing: evidence for changes in biodiversity comes from the rarely do such studies make the connections between fossil record of marine species (Sepkoski et al. 1981), the individual and the population, despite a potential thus demonstrating that the sea is not invulnerable to for enhancing predictive capacity by uncovering the mass extinction. On the other ha.nd, while presently underlying mechanisms for population and community species are being lost at high rates from some terres- change (Bertness 1992, Wootton 1993, Micheli 1997). trial systems, few marine species are known to have become extinct during the 20th century (Carlton 1993). Reasons for this apparent discrepancy are intriguing Developing stronger working relationships between and warrant further evaluation by marine ecologists. scientists and managers Are recent extinctions of marine species in fact rare, or is it simply that the taxonomy of so many of these spe- Several of the challenges identified in this review are cies remains to be properly described? In addition, not easily addressed solely within the provi.nce of basic understanding the role of biodiversity looms as a major research. However, researchers working in, collabora- challen.ge. Given the apparent red.undancy of species tion with regulatory and management agencies could within functional groups in many marine benthid address some of them. There has been an appeal demersal systems, what significance does that diver- by many scientists for appIication of the principles of sity have to the dynamics and sustainable functioning ecosystem management; yet the protocols for applying of any givcn system? Answers to these questions are Estes & Peterson: Marine ecological r-esearch in seashore and seafloor systems 287

important for assessing environmental impacts, de- brates: the spatial scales of pattern explained by active signing relevant monitoring programs, and managing habitat selection and the emerging role of hydrodynami- the health of marine ecosystems. cal processes. Oceanogr Mar Biol Annu Rev 25:113-165 Caley MJ, Carr MH. Hixon MA, Hughes TP, Jones JP, Menge Research funding to study marine ecosystems is BA (1996) Recruitment and the local dynamics of open never sufficient to assess all component species, so the marine populations. Annu Rev Ecol Syst 27:477-500 degree to which species can be pooled by taxono- Carlton JT (1989) Man's role in changing the face of the mic/functional group without loss of important infor- ocean: biological invasions and implications for conserva- tlon of near-shore environments. Conserv Biol 3:265-273 mation about the state and dynamics of the system has Carlton JT (1993) Neoextinctions of marine invertebrates. Am critical implications to the conduct of science. Answers Zoo1 33:499-509 to this problem should also help shed light on why Carpenter SR, Kitchell JF (1993)The trophic cascade in lakes. some systems seem so readily invaded by exotics, and Cambndge University Press, Cambridge might help define and protect ecosystem integrity and Commito JA, Ambrose WG Jr (1985) Multiple trophic levels in soft-bottom communities. Mar Ecol Prog Ser 26:289-293 sustainability-perhaps the greatest challenge of the Connell JH (1972) Community interactions on rocky intertidal 21st century (Carlton 1989). shores. Annu Rev Ecol Syst 3:169-192 Connell JH (1978) Diversity in tropical rain forests and coral reefs. Science 199:1302-1310 Acknowledgements. An earlier version of this paper was writ- Connell JH (1983) On the prevalence and relative importance ten as a backqround document for the OEUVRE (Ocean Ecol- of interspecific competition: evidence from field experi- ogy: understanding and Vision for Research) workshop, con- ments. Am Nat 122:661-696 vened by the U.S. National Science Foundation's Division of Connell JH, Hughes TP, Wallace CC (1997) A 30-year study of Ocean Sciences in March 1998 at Keystone. Colorado. We coral abundance, recruitment, and disturbance at several thank M. E. Hay and P. A. Jumars for inviting us to participate scales in space and time. Ecol Monogr 6?:461-488 in the workshop and for comments on an earlier version of the Davis RW. Fuiman LA, Williams TM, Collier SO, Hagey WP, review. Partial support was provided by NSF Grant OCE 97- Kanatous SB. Kohin S, Horning S (1999) Hunting behavior 12809 [to C.H.P). We appreciate the substantial input from of a marine mammal beneath the Antarctic fast-ice. countless numbers of our colleagues at the workshop and Science 283:993-996 afterwards. The paper itself was improved by comments from Dayton PK (1989) lnterdecadal variation in an Antarctic P. K. Dayton and 2 anonymous referees S. L Reese helped sponge and its predators from oceanographic climate prepare for publication. shifts. Science 245:1484-1486 Dayton PK, Oliver JS (1980) An evaluation of experimental analyses of population and con~munitypatterns in benthic LITERATURE CITED marine environments. In: Tenore KR, Coull BC (eds) Manne benthic dynamics. University of South Carolina Alcala AC, Russ GR (1990) A direct test for the effects of pro- Press. Colun~bia,p 93-120 tective management on abundance and yield of tropical Dayton PK, Tegner MJ (1984) The importance of scale in marine resources. J Cons Int Explor Mer 46.40-47 community ecology: a kelp forest example with terrestnal Allen MJ, Smith GB (1988) Atlas and zoogeography of com- analogs. In: Price PW, Slobodchikoff CN, Gaud WS (eds) mon fishes in the Bering Sea and Northeastern Pacific. A new ecology: novel approaches to interactive systems. NOAA Natl Mar Fish Serv Tech Rep US Dep Commerce Wiley, New York, p 457-481 66:l-148 Dayton PK, Thrush SF, Agardy MT (1995) Environmental Anderson PJ, Piatt JF (1999) Community reorganization in the effects of marine fishing. Aquat Conserv Mar Freshw Gulf of Alaska following ocean climate regime shift. Mar Ecosystems 5:205-232 Ecol Prog Ser 189:117-123 Dayton PK, Tegner MJ, Edwards PB, Riser KL (1999) Tem- Baumgartner TR, Soutar A, Ferreira-Bartrina V (1992) Recon- poral and spatial scales of kelp demography: the role of struction of the history of Pacific sardine and northern oceanographic climate. Ecol Monogr 69:219-250 anchovy populations over the past two millenia from sedi- Doherty PJ, Williams D (1988) The replenishment of coral ments of the Santa Barbara basin, California. Rep Calif reef fish populations. Oceanogr h4ar Biol Annu Rev 26: Coop Ocean Fish Invest (CalCOFI) 33:24-41 487-551 Bertness MD (1992) The ecology of New England salt marsh Eckman JE (1983) Hydrodynamic processes affecting benthic plant communities. Am Sci 80:260-268 recruitment. Limnol Oceanogr 28:241-257 Blegvad H (1928) Quantitative investigations of bottom inver- Elmgren R, Ankar S, Marteleur B, Ejdung G (1986) Adult tebrates in the Limfjord 1910-1927 with special reference interference with postlarvae in soft sediments: the Ponto- to the plaice food. Rep Dan Biol Stn 34:33-52 poreia-Macoma example. Ecology 67:827-836 Block BA, Finnerty JR. Stewart AFR. Kidd J (1993) Evolution Estes JA, Tinker MT, Williams TM, Doak DF (1998) Killer of endothermy in fish: mapping physiological traits on a whale predation on sea otters linking oceanic and near- molecular phylogeny. Science 260:210-214 shore ecosystems. Science 282:473-476 Botsford LW, Castilla JC, Peterson CH (1997) The mana- Fretwell SD (1987) Food chain dynamics: the central theory of gement of fisheries and marine ecosystems. Science 277: ecology? Oikos 50:291-301 509-514 Gaines SD, Roughgarden J (1987) Fish in offshore kelp forests Brown JH (1995) Macroecology. University of Chicago Press, affect recruitment to intertidal barnacle populations. Chicago Scince 235:479-481 Brown JH. Heske EJ (1990) Control of a desert-grassland tran- Genin A, Dayton PK, Lonsdale PF, Spiess FN (1986) Corals on sition by a keystone rodent gulld. Science 250:1705-1707 seamount peaks provide evidence of current acceleration Butman CA (1987) Larval settlement of soft-sed~mentinverte- over deep-sea topography. Nature 322:59-61 288 Mar Ecol Prog Ser 195: 281-289, 2000

Genin A, Noble M, Lonsdale PF (1989) Tidal currents and Olafsson EB, Peterson CH, Ambrose WG Jr (1994) Does re- anticyclonic motions on two North Pacific seamounts. cruitment limitation structure populations and cornmuni- Deep-Sea Res [Part A) 36:1803-1825 ties of macro-invertebrates in marine soft sediments. the Gentry RL,Kooyman GL (1986) Fur seals: maternal strategies relative significance of pre- and post-settl.ement proces- on land and at sea. Princeton University Press, Princeton ses. Oceanogr Mar Biol Annu Rev 32:65-109 Grassle JF (1986) The ecology of deep-sea hydrothermal vent Oliver JS, Slattery PN (1985) Effects of crustacean predators communities. Adv Mar Biol23:301-362 on species composition and population structure of soft- Grassle JF (1989) Species diversity in deep-sea communities. bodied infauna from McMurdo Sound, Antarctica. Ophe- Trends Ecol Evol4.12-l5 lia 24:155-175 Gurevitch J, Hedges LV (1999) Statistical issues in ecological Paerl HW, Pinckney JL, Fear JM, Peierls BL (1998) Ecosystem meta-analyses. Ecology 80:1142-1149 responses to internal and watershed organic matter load- Hall SJ (1994) Physical disturbance and marine benthic ing: consequences for hypoxia in the eutrophying Neuse communities: life in unconsolidated sediments. Oceanogr River Estuary, North Carolina, USA. Mar Ecol Prog Ser Mar Biol Annu Rev 32:179-240 166:17-25 Hay ME, Fenical W (1988) Marine plant-herbivore interac- Paine RT (1966) Food web complexity and species diversity. tlons: the ecology of chemical defense. Annu Rev Ecol Syst Am Nat 100:65-75 19:lll-145 Paine RT (1980) Food webs: linkage, interaction strength and Hughes TP (1989) Community structure and diversity of coral community infrastructure. J Anim Ecol 49:667-685 reefs: the role of history. Ecology 70:275-279 Paine RT (1994) Marine rocky shores and community ecol- Jackson JBC (1991) Adaptation and diversity of coral reefs. ogy: an experimentalist's perspective Excellence Ecol 4: BloScience 41:4?5-482 1-152 Jackson JBC (1997) Reefs since Columbus. Coral Reefs Palumbi SR (1992) Marine speciation on a small planet. 16(Suppl):23-32 Trends Ecol Evol ?:l 14-1 18 Jones CG, Lawton JH, Shachak M (1994) Organisms as Pauly D, Christensen V, Dalsgaard J. Froese R, Torres F Jr ecosystem engineers. Oikos 69~373-386 (1998) Fishing down marine food webs. Science 279: Karlson RH, Cornell HV (1998) Scale-dependent variation in 860-863 local vs. regional effects on coral species richness. Ecol Peterson CH (1979) Predation, competitive exclus~on,and Monogr 68:259%274 diversity in the soft-sediment benthic communities of estu- Keating BH, Fryer P, Batiza R, Boehlert GW (1987) Sea- aries and lagoons. In: Livingston RJ (ed) Ecological pro- mounts, islands, and atolls. Geophys Monogr 43:l-405 cesses in coastal and marine systems. Plenum Press. New Kneib RT (1988)Testing for indirect effects of predation in an York, p 233-264 Intertidal soft-bottom commumty. Ecology 69.1795-1805 Peterson CH (1991) Intertidal zonatlon of marine inverte- Kneib RT, Stiven AE (1982) Benthlc invertebrate responses to brates in sand and mud. Am Sci 79:236-249 size and density manipulations of the common mummi- Peterson CH, Black R (1987) Resource depletion by active chog, Fundulus heteroclitis, in an intertidal salt marsh. suspension feeders on tidal flats: influence of local density Ecology 63:1518-1532 and tidal elevation. Limnol Oceanogr 32:143-166 Lauck T, Clark CS, Mangel M, Munro GR (1998) Implement- Pineda J, CasweU H (1998) Bathymetric species-diversity pat- ing the precautionary principle in fisheries management terns and boundary constraints on vertical range dlstribu- through marine reserves. Ecol Appl 8:S72-S78 tion. Deep-Sea Res (11) 45:83-101 Leichter JJ, Wing SR, Miller SL, Denny MW (1996) Pulsed Polis GA, Anderson WB, Holt RD (1997) Toward an integra- delivery of subthermocline water to Conch Reef (Florida tion of landscape and food web ecology: the dynamics of Keys) by internal tidal bores. Limnol Oceanogr 41: spatially subsidized food webs. Annu Rev Ecol Syst 28: 1490-1501 289-316 Levln SA (1992) The problem of pattern and scale in ecology Power ME, Tilrnan D, Estes JA, Menge BA, Bond WJ, Mills Ecology 73: 1943- 1967 LS, Daily G, Cashlla JC, Lubchenco J, Paine RT (1996) Levinton JS, Lopez GR (1977) A model of renewable food Challenges in the quest for keystones. BioScience 46: resources and limitation of deposit-feeding benthic popu- 609-620 lation~.Oecologia 31: 177-190 Powers DA. AUendorf FW, Chen TT (1990) Application of Lubchenco J (1978) Plant species diversity in a marine inter- molecular techniques to the study of marine recruitment tidal community Importance of herbivore food preference problems. In: Sherman K, Alexander LM, Gold BD (eds) and algal competitive abilities. Am Nat 112:23-39 Large marine ecosystems. Patterns, processes and yields. Martin PS (1973) The discovery of America. Science 179: American Association for the Advancement of Science, 969-974 Washington, p 104-121 Menge BA, Barlow EL, Blanchette CA, Navarrete SA, Rafaelli D, Hall SJ (1992) Compartments and predation in an Yamada SB (1994) The keystone species concept: varia- estuarine food web. J Anim Ecol61.551-560 t~onin interaction strength in a rocky intertidal habitat. Raffaeli D, Hawkins S (1996) Intertidal ecology. Chapman & Ecol Monogr 64:249-286 Hall, London Micheli F (1997) Effects of predator foraging behavior on Rex MA. Stuart CT, Hessler RR, Allen JA, Sanders HL, Wilson patterns of prey mortality in marine soft bottoms. Ecol GDF (1993) Global-scale latitudinal patterns of species Monogr 633203-224 diversity in the deep-sea benthos. Nature 365:636-639 Mul11neau.x LS, Wlebe PH, Baker ET (1995) Larvae of benthic Roberts CM, Hawkins JP (1999) Extinction risk in the sea. invertebrates in hydrothermal vent plumes over Juan de Trends Ecol Evol 14:241-245 Fuca Ridge. Mar Biol 122:585-596 Roughgarden J, Gaines S, Possingham H (1988) Recruitment Nixon SW (1995) Coastal marine eutrophication: a definition, dynamics in complex life cycles. Science 241:1460-1466 social causes, and future concerns. Ophelia 41:199-219 Sale P (1977) Maintenance of high diversity in coral reef fish Nowell ARM, Jumars PA (1984) Flow environments of aquatic communities. Am Nat 11 1:337-359 benthos. Annu Rev Ecol Syst 15:303-328 Schmitt RJ (1987) Indirect interactions between prey: appar- Estes & Peterson. Marine ecological research in seashore and seafloor systems 289

ent competition, predator aggregation, and habitat segre- to complex ecological systems: where to next? J Exp Mar gation. Ecology 68:188?-1897 Biol Eco1216:243-254 Segerstrdle SG (1962) Investigations on Baltic populations of Tunnicliffe V (1991) The biology of hydrothermal vents: ecol- the bivalve Macoma balthica (L.).Part 11. What are the rea- ogy and evolution. Oceanogr Mar Biol Annu Rev 29: sons for the periodic failure of recruitment and the scarcity 319-407 of Macorna in the deeper waters of the inner Baltic? Com- Turner RE, Rabalais NN (1994) Coastal eutrophication near mentat Biol Soc Sci Fenn 24:l-26 the Mississippi River delta. Nature 368:619-621 Sepkoski JJ Jr, Bambach RK, Raup DM, Valentine JW (1981) Underwood AJ, Denley EJ (1984) Paradigms, explanations, Phanerozoic marine diversity and the fossil record. Nature and generalizations in models for the structure of inter- 293:435-437 tidal communities on rocky shores. In: Strong DR, Sinl- Simenstad CA, Estes JA, Kenyon KW (1978) Aleuts, sea berloff D, Abele LG, Thistle AB (eds) Ecological com- otters, and alternate stable-state communities. Science munities: conceptual issues and the evidence. Princeton 200:403-411 University Press, Princeton, p 151-180 Snelgrove PVR, Butman CA (1994) Animal-sediment relation- Underwood AJ, Fairweather PG (1989) Supply-side ecology ships revisited: cause versus effect. Oceanogr Mar Biol and benthic marine assemblages. Trends Ecol Evol4:16-20 Annu Rev 32:lll-178 White BN (1987) Oceanic anoxic events and allopatric specia- Soule ME, Sanjayan MA (1998) Conservation targets: do they tion in the deep sea. Biol Oceanogr 5:243-259 help? Science 27932060-2061 Wlldish D, Kristmanson D (1997) Benthic suspension feeders Sousa WP (1979) Experimental investigations of disturbance and flow. Cambridge University Press, Cambridge and ecological succession in a rocky intertidal algal com- W~lsonWH Jr (1986) The importance of predatory infauna in munity. Ecol Monogr 493227-254 marine soft-sediment communities. Mar Ecol Prog Ser 32 Steinberg PD, Estes JA, Winter FC (1995) Evolutionary conse- 35-40 quences of food chain length in kelp forest communities. Witman JD (1987) Subtidal coexistence: storms, grazing, mutu- Proc Natl Acad Sci USA 92:8145-8148 alism and the zonation of kelps and mussels. Ecol Monogr Thistle D, Levin L (1998) The effect of experimentally in- 5?:167-187 creased near-bottom flow on metazoan meiofauna at a Witman JD, Leichter JJ, Genovese SJ, Brooks DA (1993) deep-sea site, with comparison data on macrofauna. Deep- Pulsed phytoplankton supply to the rocky subtidal zone: Sea Res (1) 45525-638 influence of internal waves. Proc Natl Acad Sci USA 90: Thorson G (1950) Reproductive and larval ecology of marine 1686-1690 bottom invertebrates. Biol Rev 25:l-45 Woodin SA (1976) Adult-larval interactions in dense infaunal Thrush SF and others (1997a) The sandflat habitat: scaling assemblages: patterns of abundance. J Mar Res 34:25-41 from experiments to conclusions. J Exp Mar Biol Ecol216: Wootton TJ (1993) Indirect effects and habitat use in an inter- 1-9 tidal community: interaction chains and interaction modi- Thrush SF and others (1997b) Scaling-up from experiments fications. Am Nat 14 1:? 1-89

Editorial responsibility: Kenneth Sherrnan (Contributing Submitted: February 10, 1999; Accepted: October 26, 1999 Editor), Narragansett, Rhode Island, USA Proofs received from author(s): March l?, 2000