*Present address: Dept. of Biology, Dalhousie University, Halifax,Nova Scotia, B3H 4J1 Canada

Coral Reefs (1997) 16, Suppl.: S77—S91

Coral reef ecosystems:how much greater is the whole than the sum of the parts?

B. G. Hatcher*

Pelagic and Reef Fishes Resource Assessment Unit, CARICOM Fisheries Resource Assessment and Management Program,Tyrell Street, Kingstown, Saint Vincent and the Grenadines, West IndiesE-mail: hatcher@caribsurf.com

Accepted: 31 January 1997

Abstract. The ecosystem concept has been applied tocoral reefs since the time of Charles Darwin, perhapsbecause of the apparent integrity of the biotic-abioticnexus. The modern model of the ecosystem as a hierarchywith emergent properties is exemplified in reefs as massivestructures formed by small colonial organisms, the self-similarity of these structures across large spatial scales,and the uniformity of function by diverse biological com-munities. Emergent properties arise through the integra-tion of processes up the levels of organization and largerspatial and temporal scales encompassed by a whole reef.The organic response of reef morphology to hydro-dynamic forcing, the constancy and conservatism of or-ganic production across a broad range of environments,and the global persistence of reefs in the face of massiveevolutionary change in species diversity are interpreted asemergent properties. Coral reefs, of course, function by thesame basic laws as other ecosystems, but there is cause toview them as an end member of a continuum because oftheir structural complexity and high internal cycling.Well-defined boundary conditions mean that highly inte-grative measures of ecosystem process based on physicaland biogeochemical models (e.g. community metabolism)have provided the main applications of systems ecology toquestions of coral reef function. Organism-populationapproaches are being reconciled with form-functionalmodels to yield new insights to ecosystem processes andinteractions among reefs and adjacent systems. The formand metabolism of reef production are strongly affectedby phase shifts in benthic community structure, and mostreef systems are more open to trans-boundary fluxes andexternal forcing than the early models suggest. The at-tractive paradigm of the reef as a self-sufficient ecosystemis dying slowly as research focus shifts from atolls tomore open fringing and bank barrier reefs, and organicinputs to system production are measured. Coral reefscontribute little in a net sense to global ecosystem pro-cesses, but on an areal basis their exports of organic

products are significant. Holistic models and measures ofecosystem processes incorporate the unusual whole-partrelationship of reefs and are practically essential to an-swering the key questions facing coral reef science in thenext millennium.

Introduction

The aim of this study is to explore the role of the ecosys-tem concept (Tansley 1935; Odum 1953) in our under-standing of coral reefs. Ecosystem processes maintainingbiological diversity and controlling the flux of materialshave been well studied because they can be examinedacross a broad range of spatial-temporal scales in allecosystems. Coral reefs (like lakes, e.g., Schindler 1990)have received particular attention from ecologists work-ing at the ecosystem level because of the apparent distinct-ness of their boundaries. Here I focus on the relevance,usefulness and recent application of ecosystem conceptsand measurements to coral reef research.

Three elementary questions emerge from the somewhatcryptic query posed in the title:

1. What are ecosystem processes in coral reefs?2. Why (and how) do we study them?3. Has ecosystem research advanced coral reef science?

The answers cannot be stated succinctly, but the state-ments following summarize the relevant themes for dis-cussion:

1. Ecosystem processes are those which link the physicalenvironment to the interacting assemblage of organ-isms. Common examples include biological produc-tion, biogeochemical cycling and the evolution andmaintenance of biological diversity (Table 1). As such,ecosystem processes transcend abiotic-biotic distinc-tions, levels of biological organization, and spatial-tem-poral scales of observation. Their study is as muchabout boundaries, scales and rate constants as aboutany particular physical, biological or geologicalentity or phenomenon. Ecosystem research focuses on

universal processes, which are fundamentally no differ-ent in coral reef systems than in any other.

2. We study ecosystem processes to improve understand-ing, prediction and control by quantifying emergentparameters across hierarchies of organization and spa-tial-temporal scales. Certain measurement techniquesand currencies (e.g., carbon flux) are particularly suit-able for such integration in reef ecosystems, and novelmodels and tools (e.g., dissipation structures, feedbackanalysis) have been developed to deal with the com-plex, non-parametric data they generate.

3. Ecosystem research identifies the variables of state (e.g.,net vertical accretion rate) and sets the boundary con-ditions (e.g., maximum sea level rise with which reefscan keep up) that can assess the status of reefs andpredict their responses to environmental change. Wehope that the measurement of ecosystem processes willproduce scale and case-independent results, and thatmodels based on them will usefully simplify the com-plexity of reefs while still explaining or predicting ac-tual observations. Optimistically, ecosystem scienceaims to do for ecology what Newtonian physics did formechanics. The morphoedaphic index (Schlesinger andReiger 1982) or the fundamental biological diversitynumber (Hubbell 1997) are good examples.

Coral reef ecosystems: boundary conditions

‘‘2 to some degree, an ecosystem is in the eye of thebeholder.’’

—B. Babbitt, Secretary, ºS Department of the Interior

Coral reefs are outstanding examples of marine ecosys-tems. Reefs embody the mixture of the minute and grand,ephemeral and permanent, simple and complex that weassociate with the natural systems of this planet. ‘‘Ecosys-tem’’ is one of those wonderful words that communicatesa fuzzy concept of near-universal consensus, but meansvery different things to different people when it comes tospecifics. While few would agree exactly on the compo-nents, processes, scales and boundary conditions that de-fine a reef ecosystem, many use the phrase glibly in theirintercourse with scientists and others. Yet it is the specificsof ecosystem structure and function that concern scientists.

The demands of society for prediction and control ofanthropogenic change in the earth’s ecosystems have for-ced ‘‘ecosystem management’’ to the top of the environ-mental, resource management, and even political agendas(Christensen et al. 1996). Many have felt the effects on thereview, funding and application of ecosystem research.The proceedings of the eight Coral Reef Symposia and therecent International Coral Reef Initiative (Crosby et al.1995) nicely plot the emergence of ecosystem approachesto the research and management in coral reefs. But what isan ‘‘ecosystem approach’’ ? Surely before one undertakesecosystem management, there must be a clear and practi-cal definition of the ecosystem. Many investigators havetried to do this for coral reefs (e.g., Fosberg 1961; Preob-razhensky 1977; Fagerstrom 1987; Kinsey 1991).

Perhaps many would agree on some general definitionof a coral reef: a marine limestone structure built by

calcium-carbonate secreting organisms which, with its as-sociated water volumes supports a diverse community ofpredominantly tropical affinities, at a higher density ofbiomass than the surrounding ocean. This definitionincludes the abiotic and biotic aspects, but lacks anyspecification of scale or integration (i.e. connectivity, self-organization, homeorhesis), which are usually associatedwith the ecosystem concept. For example no one definesa solitary coral polyp as a coral reef. Yet it has many of theattributes associated with coral reef ecosystems: roundedshape, distinct boundaries on its surrounding environ-ment, symbiotic life style, high animal to plant biomassratio, calcium carbonate precipitation, P/R ratio of aboutone. It is even arranged with a nutrition-gathering peri-phery around a digestive centre: but it’s not a reef. Simi-larly, a lump of coral rock on a lagoon sand sheet (i.e.,a ‘‘bommie’’) is not a coral reef. Nor is the algal flat on anatoll rim: these are parts of a coral reef. A fringing reef ona Caribbean island coast is, however, considered to bea coral reef ecosystem, as is an atoll in the Maldives. TheGreat Barrier Reef is not a coral reef (it is a coral reefprovince containing thousands of reefs), but it is generallyreferred to as a coral reef ecosystem (which includes thevast inter-reef areas of water and sediment).

It appears that our definition of coral reefs has more todo with the boundaries and scales than with the compo-nents and functions of the ecosystem. All of these exam-ples can be studied as coral reef ecosystems (sensu stricto),even as they are not all coral reefs. It is more thansemantics that the ecosystem can be defined at more thanone level of organization and across a rather large rangeof spatial and temporal scales: it reflects the hierarchicalnature of ecosystems (Webster 1979; Miller 1991). Thus, itis not so much a level or scale that we use to define a reefecosystem as the nature of the boundary with anotherlevel or scale. Most often it is a Cartesian boundary (e.g.,the transition from reef slope to open ocean). Interestingly,it can be a temporal transition (e.g., between Cretaceousand Tertiary reefs). Problems arise, however, when thecomponents of ecosystems (e.g. fish populations) do notcorrespond to the Cartesian boundaries. One way aroundthis is to use functional attributes (processes) to define theboundary conditions (e.g., the mixing line of lagoonal andoceanic water masses, or the 1% isopleth of coral larvaldensity). That these process-derived boundaries often maponto Cartesian boundaries reflects the interaction be-tween physical structure and biotic function that charac-terizes coral reef ecosystems (e.g., topographically control-led water residence time determines the relative import-ance of biological processes of nitrogen transformation indifferent reef habitats, Hatcher 1985). From this functionalviewpoint, in the simplest sense, an ecosystem is defined asone in which the internal processes dominate over thetrans-boundary processes. This is intuitively obvious forsystems like coral reefs or lakes, which have a relativelyhigh degree of enclosure or isolation from the largersystems in which they are embedded. The view of coralreefs as relatively closed systems, within the boundaries ofwhich accurate budgets of biotic and abiotic materialsmay be derived, has profoundly influenced coral reef ecol-ogy, starting with the first application of systems ecology(e.g. Sargent and Austin 1949; Odum and Odum 1955).

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Table 1. Major ecosystem processes of coral reefs are listed with the relevant levels of biological organization. The types and spatial andtemporal scales of measurements commonly made of these process are shown (ranked in decreasing scale), along with some references toexamples

Process Measurements Scales Examples

Accretion Vertical growth, margin ex- Barrier reef—reef Davies and Hopley 1983(ecosystem, community) pansion, infilling and erosion matrix, 105—year Kan et al. 1995

Biological Net export and accumulation Atoll—reef zone Smith 1988, Crossland et al.production (P

NEW) day—year 1991

(community) Photosynthetic rates, Lagoon—colony Adey and Steneck 1985community metabolism (E) week—hour Gattuso et al. 1993

(population) Population growth, Reef province—reef Munro 1977, Alcala andemigration and harvest rates zone, decade—day Gomez 1985

Organic Community respiration (R) Lagoon—colony Atkinson and Grigg 1984decomposition week—hour Hansen et al. 1987.(community) Rates of herbivory and Reef zone—matrix Hatcher 1981, Riddle et al.

detritivory month—day 1990Microbial and anaerobic Reef zone—matrix Hopkinson et al. 1987metabolism day—hour Sorokin 1995

Biogeochemical cycling, C, N and P pools and fluxes, Ocean basin—reef Smith et al. 1981export and hydrodynamics and matrix Andrews and Muller 1983accumulation kinematics year—hour Bilger and Atkinson 1995(community) Net export and accumulation Atoll—reef zone Smith 1988, Crossland et al

(PNEW

), sedimentation rates year—day 1991Net calcification (G) Lagoon—bommie Smith and Harrison 1977

hour—week Gattuso et al. 1995

Maintenance of Speciation, extinction, Global ocean—reef McGhee 1988, Sepkoskibiodiversity geographic radiation, zone 1991, Jackson 1992(biosphere, adaptation and response to 106—102 years Pandolfi 1996.ecosystem) climate change(community, Community succession, Reef province—reef Connell 1978, Griggpopulation) response and recovery from zone 1983, Rogers 1992

disturbance 103 y—month Tanner et al. 1996(population) Dispersion, settlement and Reef province—reef Doherty 1987, Black et

recruitment of reef organisms bommie al. 1991, Fisk and Harriotdecade—day 1990

(population, Competition, predation, Reef—colony Buss and Jackson 1979organism) parasitism and symbiosis decade—colony Wilkinson 1987

Ecosystem processes and models

‘‘Ecological systems become closed when transfer ratesamong adjacent systems approach zero or when differ-ences in process rates between adjacent elements are solarge that the dynamics of the elements are effectivelydecoupled from one another.’’

—J.A. ¼iens (1989)

Twenty-five years ago, when systems ecology was stilla young discipline, Howard Odum (1971 p. 10) publishedhis ‘‘macroscope’’ view of the science: its message remainsbroadly relevant. As research moves from the descriptiveto the predictive stage, we approach ‘‘How?’’ and ‘‘Why?’’questions by making simplifying assumptions and con-structing, testing and refining models based on these. Thekey of course is the simplifying assumption (Odum’s ‘‘de-tail eliminator’’). Ecological systems (especially coral reefs)are of such complexity that theoretical development al-ways involves abstraction to another level of organizationwith fewer components or simpler dynamics, for which itis possible to collect data and which is easier to model(Wiegert 1988). If the abstraction is down the hierarchy oforganization (e.g., modelling crown-of-thorns starfish out-breaks from laboratory measures of fecundity and larvalsurvival) we call it ‘‘reductionism’’. If detail is eliminated

by measuring processes higher in the hierarchy (e.g., mod-elling COT outbreaks from sediment-climate relation-ships) we call it ‘‘holism’’ or ‘‘ecosystem science’’. (The twoapproaches are not irreconcilable, e.g., Pahl-Wostl 1993).Some of the most common ecosystem processes identifiedin holistic models of coral reefs are listed in Table 1.

The simplifications are invariably embodied in a model,which is used to explain, to predict, possibly to control theecosystem of interest (Reichelt et al. 1983; Jorgensen 1994).Samples from the range of reef models include a captivereef in a mesocosm (e.g., Adey and Loveland 1991), a hugeconvection cell (Rougerie and Waulthy 1993), a balancedbiogeochemical budget (e.g., Smith 1988), a hierarchy ofcritical units (e.g., Bradbury 1977), or a big wheel ofrecycling materials with some small, but important andhard to measure, spokes radiating off (Hatcher 1996). Allstrive to capture the essential properties and processes ofreefs. All explicitly or implicitly define system boundarieswithin certain spatial and temporal scales. Where theydiffer is in whether the reef system is viewed as essentiallyclosed or open and the degree of complexity they incor-porate (Table 2).

Models of coral reef ecosystems are evolving from con-ceptually and methodologically simple, closed systemstowards a view of reefs as open, complex systems whichare more difficult to deal with but undoubtedly more

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Table 2. Models of coral reef ecosystems are classified into three basic types. Some analogs, the distinguishing characteristics, commonly usedmethods and examples of each type are listed

Model type Characteristics Methods Examples

Closed Strong boundary Biogeochemical budgets Sargent and Austin 1949(Analogous to a conditions, internalA for hydrologic control Kinsey 1983, Smith 1988coral, chemostat, external fluxes, self- volumes Gattuso et al. 1995oasis) sufficient, steady-state, Trophodynamic Polovina 1984, Opitz 1995

retentive-conservative biomass budgets

Open Trans-boundary fluxes Biogeochemical flux Dahl et al. 1974, Smith et al.(Analogous to a large, strong external budgets 1981, Eakin 1996sponge, biofilter, forcing, variable source- Analytical and numerical Black et al. 1991, Rougerieriver) sink relationships, physical hydrodynamic models and Waulthy 1993, Bilger and

transport processes dominate and simulations Atkinson, 1995

Complex Thermodynamically open, Energy flow Odum 1983(Analogous to a energy and information Pattern and network Reichelt et al. 1981dissipative struc- dissipated rapidly, fractal, analysis Johnson et al. 1993ture, information self-regulating, cybernetic Transition matrix Tanner et al. 1996network, city) analysis

realistic (Table 2). The reality, of course, is continuum ofclosure in both the structural and functional attributes. Inthe more closed models, reefs are self-sufficient oases ofhigh biomass in the ocean desert (Odum and Odum 1955).The reef ecosystem is analogous to an organism or a re-action chamber, with tight boundaries and dominantinternal dynamics of recycling and self-seeding. Organi-zationally the system has high internal connectivity, isself-regulating, and has high persistence stability. Materialand information are conserved, and transfers across sys-tem boundaries are small proportions of the total flux,most of which is internal. This model derives from earlythinking of systems ecology, trophodynamics, island bio-geography and biological accommodation, and from a fo-cus on isolated atolls as study sites. Compared to manyother marine ecosystems (e.g., estuaries, kelp forests) reefsare relatively isolated and self-contained. Closed modelshave useful applications (both to population and bio-geochemical studies of clearly delimited reefs), but fail tocapture important ecosystem processes that connect reefsto the surrounding environment (e.g., export of harvest-able production).

More open models portray reefs as sources and sinksembedded in a larger matrix of adjacent ecosystems(which may include other reefs). Analogous to big biofil-ters (Sorokin 1995), they strip plankton and nutrientsfrom the advective stream, transforming them and ac-cumulating or exporting the resultant materials and or-ganisms. The system is driven by external forcing but hasthe capacity to attenuate oscillations. Connectivity withadjacent systems is high, and the reef can be a net importeror exporter of different materials, depending on the com-munity structure and the physical environment in which itis embedded. Open models demand measures of boundaryprocesses which are often methodologically difficult (e.g.,larval dispersion, detrital loss) but are more amenable tothe elucidation of causal relationships between forcingprocesses and system parameters (e.g., tidal currents andbioparticle retention in a lagoon).

Thermodynamic models, long employed in the analysisof physical-chemical systems, are explicitly parameterized

in terms of degree of closure. They have the potential toavoid the artificial dichotomy imposed by the need tobalance budgets or define source or sink. In these modelsa coral reef is analogous to a city, with considerablestructure and strongly hierarchical organization. Theyfunction within wide constraints to dissipate variableinputs of energy and information, but are subject toprecipitous change of state near the limits of constrainton the faster processes (O’Neill et al. 1986; Pahl-Wostl1993). Despite the obvious advantages of these abstrac-tions, extensions of thermodynamic theory to complexsystems, based on the thinking of Prigogine and Allen(1982) and others have been little used in reef systems todate.

The Odums, of course, used energy flow as the basis forthe first models of reef ecosystems (Odum and Odum1955; Odum 1971), and the basic nomenclature of inputs-outputs, production-consumption, pools and fluxes, dissi-pation and control remain the dominant language ofsystems ecology (Odum 1983). Here ecosystem compo-nents are defined in terms of pools between which energyor materials flow and are grouped according to theirmode (source or sink) and scaled according to their sizeand turnover rates. Energy, carbon and nutrient-basedflux budgets have a long history of application to coralreefs (e.g., Johannes et al. 1972; Dahl et al. 1974), butnutrient currencies have received particular attention be-cause nutrient supply is often assumed to limit some keyprocess like nitrogen fixation or primary production(Smith 1984; Atkinson 1988).

Other approaches use functional groupings of orga-nisms as the system components and tropic or competitiveinteractions as the interconnecting processes (e.g., the top-down model of Polovina 1984). While there are clearlydifferences in the components and currencies used, themethods are not mutually exclusive and are often com-bined in ecosystem models such as the hybrid modelscurrently being used by Pauly and Christensen (1995) toestimate the level of primary production required to sup-port coral reef fisheries (for future reference, their numberis 8.3% of reef net primary production).

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Fig. 1. Spatial and temporal scales ofcoral reef ecosystem components andprocesses. The nested habitats of reefsare shown as bands on the spatial axis.Components of the biologicalhierarchy of organization occupyoverlapping domains in the time-space plot. Oceanographic, climaticand geological processes are locatedaccording to the temporal-spatialextent of their discrete or continuous(arrow) distributions. The upperboundary of reef ecosystems(incorporating both biotic and abioticcomponents and processes) is shownto extend to ten of kilometers andabout 10 000 y

Simplifying by moving up a hierarchy (holism) inva-riably assumes a degree of functional redundancy withinlevels of organization and groups ecosystem componentsat those levels into single components at a higher level.For example, the functional groupings of free-living ben-thic algae used in models of reef benthic communitystructure and function (e.g., Littler et al. 1983; Steneck1988) is a simplifying assumption that has served uswell. Similarly, DeMartini et al. (1996) compared reef fishdensities on two Hawaiian reefs sampled more than adecade apart. They were unable to detect any changein species populations, which were highly variable, butwhen fish were classified in functional groups, the powerof the tests was sufficient to detect large declines inabundance. In complex ecosystems like coral reefs,functional classification of components at higher levelsof biological organization is a well-proven tool for dis-cerning the roles of ecological processes (e.g., Done et al.1996).

Whatever the detail eliminator we choose, whatever ourmodel of the ecosystem, the goal remains the ‘‘principletechnique of scientific enquiry: by changing the scale ofdescription, we will move from unpredictable, unrepeat-able individual cases to collections of cases whose beha-vior is regular enough to allow generalizations to bemade’’ (Levin 1992). The recognition that the variability inocean phytoplankton communities is best predicted byspectral analysis of mixed layer dynamics (e.g., Platt andDenman 1975; Mackas et al. 1985) is perhaps the mostpowerful unifying concept in marine ecology currentlyavailable. In the reef context, a most elegant (if less gen-eral) example is the tuning of spur and groove topographyto the ocean swell regime. Almost fifty years ago Munkand Sargent (1948) showed how a dimensionless wavenumber predicted the length and frequency of these com-plex reef formations.

Forced to supply criteria for distinguishing studies ofecosystem processes (Table 1), I point first to questionsposed at the higher levels of organizational hierarchies

(whether biological or physical-process). Then I followLevin (1992) in saying that studies of ecosystem processes‘‘2 first ask how much variation can be explained byvariation in the physical environment, and then look toautonomous biological factors to account for the bal-ance.’’ Physical processes have been demonstrated to de-fine and control a wide range of reef processes (Hatcheret al. 1987; Hamner and Wolanski 1988) and providean avenue to analysis of ecological phenomena whichspan broad ranges of area and time (e.g., Bradbury andYoung 1981; Andrews and Muller 1983; Sebens and Joh-nson 1991; Black et al. 1995; see also papers in Hughes1993).

Spatial-temporal scaling

‘‘The only things that can be universal, in a sense, arescaling things.’’

—M. Feigenbaum (1979)

Several things happen as we move up nested hierarchies:space-time scales increase, rate constants get slower, en-vironmental variables which perturb systems get incorpo-rated (Table 1; Fig. 1). Constraints on system behaviormay change from within to between levels in a hierarchy,or between hierarchies (Simon 1973; Webster 1979). Forexample, stochastic environmental processes may controlhighly variable reef fish density in guilds or patchreefs, but biotic interactions may operate to hold abund-ances constant at the level of the community (Planes et al.1993).

Coral reef ecosystems as we conceptualize them extendto the tens of kilometers in length scales and to tens ofthousands of years along the time dimension (Fig. 1).Above these we have reef provinces and cycles of reefdestruction and regrowth. Biological levels of organiza-tion group within, but also extend beyond, ecosystemboundaries. A population may exist wholly within the

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Fig. 2. The closure continuum applied to reef ecosystems. Schemat-ics of three characteristic reef morphologies (bank barrier, fringingand atoll) are located along a gradient of increasing degree of closureof the processes that control ecosystem processes and the exchangeof organisms, energy, nutrients and information with adjacent eco-systems. The juxtaposition of net autotrophic and heterotrophiczones is depicted by distinct bands and patches. Characteristic pat-terns of water flow over and around reefs are shown with arrows.The relative significance of retention and recycling of organic mater-ial is reflected in the size of the dashed ellipse. As reefs become less

hydrodynamically open and more isolated from external nutrientsources, long water residence times and self-supporting communities(e.g., symbioses) favor the recycling of organics within the reef andinhibit exchanges with the surrounding ocean. Correspondingly, therelative potential of nutrient limitation changes, the excess and newproductivity decreases (causing a decrease in the f-ratio), and the rateat which the system dissipates energy and information is reduced.No reef systems are completely closed, and most fall towards themore open end of the continuum

limits of a reef or extend well outside of it. While they maybe nested in an organizational sense, the biological levelsdo not nest fully in space-time, but rather overlap tovarying degrees. Habitats, on the other hand, form a fullynested set along the spatial continuum. Patch reefs occurwithin reef zones and consist of reef matrix, which in turndefines interstitial spaces.

Physical processes may be local, relatively constantphenomena occurring over a large temporal range (e.g.,submarine groundwater discharge); they may be periodicor sporadic phenomena, spanning a large range of distan-ces (e.g., waves, storms: the causes of physical disturbance);or they may be scale spanning phenomena which extendcontinuously through the dimensions (e.g., eddy-diffu-sion). In these, larger is slower, in a linear relationship(e.g., the exchange turnover of water in reef lagoons de-creases with their volume).

A key message from scaling exercises (Hatcher et al.1987; Fig. 1) is that ecosystem processes can be definedand measured at many scales (not just that of the wholereef), depending on the question being addressed and theobserver’s perception (Table 1). One geochemist’s tidalpool is another’s lagoon; one physicist’s turbulence is thenext’s bulk flow, one mathematician’s chaos is another’sequilibrium, one ecologist’s ecosystem is another’s environ-ment. Different patterns emerge at different scales of obser-vation. Our ability to predict ecological phenomena de-pends on whether (and how) processes change within their

domains of scale (i.e., they may be scale-dependent, such asthose controlling reef fish community structure: Galzin1987; or they may be scale-invariant such as those control-ling the morphology of fish prey: Aronson, 1994), and onthe form of the non-linearities at the transitions betweendomains (Allen 1985; Holling 1992; Knowlton 1992).

A more subtle message of scaling analyses is that biolo-gical hierarchies do not separate as clearly or progressi-vely in time-space as physical-process hierarchies (O’Neillet al. 1986). One useful scheme recognizes the pervasiveinfluence of the degree of system closure (in the popula-tion, hydrodynamic and thermodynamic senses) on eco-system processes involving the flux of organisms andmaterials and its apparent relationship to reef morpho-logy (Fig. 2) due to the dominant role of water exchangein controlling such fluxes (e.g., Smith 1984; Hamner andWolanski 1988; Black et al. 1990).

Spatial-temporal scaling is not an easy concept to graspand apply to coral reefs. Some workers are grappling withthe science of scale using dimensional and spectral analy-sis, geostatistics, the mathematics of fractals and othercross-disciplinary tools (e.g., see collections of papers inGiller et al. 1994; Patten and Jorgensen 1995), but therehave been few thorough applications to coral reef systems.Reef scientists working at any level of organization needparticularly to recognize the space-time scaling of ecologi-cal processes because of the rather large range of scalesencompassed by reefs (Fig. 1).

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Table 3. Emergent properties of coral reef ecosystems are classified into three modes by which they arise from ecosystem hierarchies. Theessential characteristics are listed along with examples of processes exhibiting that mode

Mode of emergence Characteristics Example process References

Additive Processes sum linearly up Photosynthetic Kinsey 1983, Atkinson andlevels of hierarchy production Grigg 1984

Integrative Processes incorporate Reef growth (vertical Davies and Hopley 1983up hierarchy accretion) Miller 1991

Differential Processes differ across Phase-shifts in benthic Done 1992, Knowlton 1992levels and interact non- community dominance Aronson 1994linearly up hierarchy

Emergent properties of coral reef ecosystems

‘‘In such (scaling) analysis, natural scales and frequencieswill emerge, in which rests the essential nature of thesystem’s dynamics.’’

—Holling (1992)

One reason to study ecosystem process in reefs is thattheory predicts certain emergent properties from complex,highly organized systems (e.g., Patten and Odum 1981;Prigogine and Allen 1982), and coral reefs can provideuseful tests of such predictions. Few have done this ex-plicitly (e.g., Bradbury 1977; Reichelt et al. 1981; Miller1991), but virtually all scientists make use of emergentproperties to characterize coral reef structure and function(e.g. net community metabolism to quantify the trophicstatus of reefs, Kinsey 1983; diversity indices to quantifysuccession and evolution, Sepkoski 1992). The need formeasurable parameters of complex systems is by far themore common reason to search for emergent properties ofcoral reefs (Table 1).

Let it be accepted that ecosystem processes are thosethat operate at the scales of ecosystems (even if logisticconstraints require us to measure them at smaller scales),and transcend the boundaries among levels of organiza-tion as they map onto space-time. Thus, for example,locomotion is not an ecosystem process because its mag-nitude, sign and scales are species-specific and cannot bemeaningfully integrated for an entire community or habi-tat. Migration to off-reef feeding or breeding sites is anecosystem process because it represents a loss of materialfrom the ecosystem, regardless of whether it is quantifiedfor a single species or an entire community. Because they‘‘scale up’’, ecosystem processes can be seen to emergefrom the system to provide some degree of generality.

I recognize three types of emergence of ecosystem prop-erties (Table 3). Firstly, they may be the summation of theresults of ongoing, small-scale process over larger andlonger scales. Photosynthetic production occurs only atthe level of the chloroplast-cell system, but can be ex-pressed sensibly at all levels up to the biosphere. I call thissimplest form ‘‘additive emergence’’: the process is re-stricted to one level of biological organization, but theform of the resulting product differs among levels, andmagnitude increases additively with time and spatial scale.Speciation can act in a similar way (although it is notusually referred to as an ‘‘ecosystem process’’). The causa-tive mechanisms (mutation and selection) operate at the

level of the organism (or lower, —the gene), but are mani-fest at population, community and global levels. Aronson(1994) provides some marine examples of additive emerg-ence from evolutionary biology.

Emergent properties can also result from the upscaleintegration of faster, smaller processes into slower, largerprocesses which have some different properties and can-not be fully predicted from the sum of the componentprocesses (this is the hierarchical model, Webster 1979;O’Neill et al. 1986). For example, reef accretion occurswithin the coral-microalgal symbiosis as the CaCO

3skele-

ton is laid down, within the matrix as corals and othercalcifiers produce, trap and bind carbonate frameworkand sediments, within the lagoon as it fills in with theseproducts and within the entire reef ecosystem as it growsand infills in excess of loss processes such as dissolutionand off-reef sedimentation. Reef growth is the result of thecomplex interaction of many different, smaller scale pro-cesses. We can think of this as ‘‘integration emergence’’:many small-scale processes interact (sometimes non-lin-early) to produce the greater whole, which operates atlarger, longer scales (Holling 1992).

Thirdly, ecological emergence occurs as the manifesta-tion of exchanges among levels of organization or acrossboundaries of ecosystems. In contrast to primary produc-tion, for example, the consumption of organic matter isa richly variable process (whether the mechanism is detri-tivory, herbivory or predation) that occurs at, but differsprofoundly among, several levels of organization in reefecosystems. For example, grazing fish exhibit a remark-able range of adaptations to reef plant characteristics anddistribution, but they all convert plant tissue into gas,detritus and fish flesh. Subsequent transfers of organicmaterial up to top predators (including man) or intomicrobial communities of the sediment are constrained bythe net result of the grazers’ various modes of plant con-sumption. We could call this ‘‘difference emergence’’: thewhole is defined by its balance of exchange with otherlevels in the system’s hierarchy. (This is the trophic dy-namic property: Lindeman 1942; Polovina 1984).

All three types of emergent properties have many exam-ples in coral reef ecosystems, but the themes of similarityof pattern across scales (scale-independence, Aronson1994: fractal geometry, Bradbury et al. 1984) and simplifi-cation up levels of organization persist. Ecosystem scienceattempts to capitalize on these effects by focusingmeasurement and analyses at the higher levels of organi-zation. In doing so, it is both constrained and empowered

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to include the physical and geochemical processes whichoften dominate system dynamics at the larger and longerscales (Fig. 1).

Looking for emergent properties in ecosystem processesrequires empirical observations. As higher levels oforganization generally encompass larger and longerscales, ecosystem science is faced with some difficultmeasurement challenges. One either measures a process atmanageable scales and then sums up-scale, hoping theprocess is scale-invariant (additive emergence, Table 3), orone measures a variate which hopefully integrates therelevant processes at the scale of interest (integrative ordifference emergence). The small-scale complexity (i.e.‘‘fine grain’’, Wiens 1989) of coral reefs hinders the firstapproach, while their physiography and hydrodynamicsgreatly aid integrative measurements of ecosystem pro-cesses.

Consider the example of primary productivity in reefecosystems (Hatcher 1990, 1996). Photosynthesis and res-piration can be measured at the level of the individualplant, the patch reef or the sediment community by en-closing them and sampling the controlled water volume todetect change in oxygen or carbon dioxide. The diel inte-gral of the processes at the level of the plant is net photo-synthetic productivity, while at the level of the enclosedcommunity it is net community production (animal aswell as plant respiration is included). At higher levels (andlarger scales) of habitat integration the latter measurebecomes the ecosystem parameter ‘‘E’’ (excess production:Kinsey 1983). It can be measured by following waterflowing across a reef flat, or sampling the retained water inan entire lagoon. It can also be approximated by measur-ing the net flux of nutrients essential to community meta-bolism in or out of control volumes, as long as the ratio ofnutrient to carbon or energy in the materials producedare known. In the old and elegant methods (Sargentand Austin 1949) the water mass integrates the processacross time and space, allowing single, integratedmeasures of the metabolic performance of entire commu-nities up to the scales of a lagoon-reef ecosystem (Smith1988). The underlying processes of photosynthesis andrespiration are the same from polyp to reef, but themagnitude of the net production term differs amongthem because more and different components contributeto the integrated signal at larger scales. It should bepossible to calculate E for a lagoon by area-weightedaverages of net community production for all the systemsnested within it. The fact that such estimates never matchthose of the integrated process reflects not just the com-pounding of measurement error but the fact that themeasurement time scales appropriate for a coral colonyare far shorter than those for a lagoon (i.e., there isa measurement scale mismatch: Smith and Kinsey 1988).Ecological research is rife with such mismatches, it iscertainly not a problem unique to reefs (Wiens 1989; Levin1992).

Simplistically, ecosystem processes are the emergentproperties of ecosystems. While not unique in nature, theholistic integrity that arises from the complexity of physi-cal and organic interactions makes coral reef ecosystemsparticularly significant to the scientists who study theirprocesses.

Population versus systems approaches

‘‘One of the greatest barriers to the development of inter-faces between population biology and ecosystems scienceis the perceived mismatch, especially as regards evolutio-nary processes 2 . There is considerable overlap betweenthe spatial and temporal scales of interest to the popula-tion biologist and the ecosystem scientist.’’

—S.A. ¸evin (1992)

Understandable and appropriate differences of opinionarise on the issues of which models, methods and spatial-temporal scales of observation sets are best suited toanswering a given question about coral reef dynamics.This is not a trivial issue, since it has to do with the goalsof science, processes of abstraction, model development,and the determination of boundary conditions. Some ofthe questions commonly addressed by reef scientistsclearly define these issues. For example, the questionasked by Kan et al. (1995) whether the growth of a fringingreef at high latitude could keep up with sea level riseduring the Holocene clearly establishes the model as netvertical accretion rate versus local sea level rise andspecifies the space-time scales and methods of measure-ment. One would not think of answering this question bymeasuring coral colony expansion, bioerosion and sedi-mentation rates on the present reef slope. The net ac-cretion variate, as measured from dated strata in verticalcores, is the time space integral of all these processeswhich is scaled to the sea level curves.

Most of the questions we ask about reefs cannot be sounambiguously assigned to ecosystem levels and scales.For example, the question of how storm waves alter thestructure of coral reef communities asked by Massel andDone (1993) has been approached at levels of organizationfrom the individual coral colony to entire reef tracts, atscales of meters to miles, and minutes to millennia. Notsurprisingly, no two studies provide the same answer:undetectable to massive effects have been measured at alllevels and scales. Physical disturbance is a strongly scale-dependent process, such that the pattern of ecologicaleffect measured is a function of the scale of observation(Wiens 1989; Aronson 1994; Christensen et al. 1996).There is yet to emerge a fundamental parameter for quanti-fying and predicting storm effects on reef communities (seepapers in Hughes 1993). In this case, the scale of theobservation set defines the effect of the process, and it is anecosystem process only when expressed at the ecosystem(entire reef) scales.

Though we may make different simplifying assump-tions, apply different models, or measure with differenttools when studying coral reef structure or function, wecan all agree that the starting point is to identify the timeand spatial scales of the system of interest and the pro-cesses being measured (Hatcher et al. 1987). Only then,can the environment, degree of enclosure (Fig. 2) and typeof constraints (i.e. the boundary conditions) of a problembe set (e.g., Platt et al. 1984). Reef ecologists increasinglydesign their sampling or experiments to span a range ofscales (Andrews and Muller 1983; Doherty 1987; Rogers1992). For example Galzin (1987) measured reef fishdistribution at spatial scales of meters to hundreds of

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kilometers to demonstrate that variability decreased withincreasing scale.

I have so far skirted the issue of differences betweenpopulation-based and energy or mass-based approachesto the study of reef ecosystem processes. Mixing examplesof models for coral species and chemical species purposelycounters the conventional view that ecosystem processesare defined and measured only in terms of materials fluxes.It is time to discard this misconception, as communityecology has made major contributions to our understand-ing of ecosystem processes (e.g., O’Neill et al. 1986; Pahl-Wostl 1993; Christensen et al. 1996).

The two schools of ecology have produced differentviews of ecosystem processes. One holds the ecosystemconcept as a fuzzy idea: useful perhaps for purposes ofdescription but not as a model for prediction and controlin systems of such taxonomic diversity and functionalcomplexity as reefs. To meet those objectives, we mustfurther develop quantitative models of the biotic compo-nents of ecosystems and their interactions: the organism,its species populations, and the communities they form. Itis on these components that the bulk of ecological re-search has been conducted and to which the best-testedtheorems apply (e.g., Connell 1978; Sale 1991). Determi-nistic or stochastic models of these systems, developed atthe scales of the underlying mechanisms may be sufficientto predict the trajectory of a coral reef ecosystem throughtime-space. What is required now are better methods tocombine and extend these measurements and models upto the levels of organization and scales at which we definecoral reefs. One recent application uses simplified rules ofinteractions between components in transition matrixmodels to predict the structure of benthic communities atwhole-habitat, decade scales which characterize manyforms of disturbance in reef ecosystems (Tanner et al. 1995).

A population-based approach is not inconsistent withthe ‘‘macroscope’’. Indeed, ‘‘macroecology’’ continues todevelop as a legitimate branch of the field (e.g., Brown1995), which empirically relates statistical patterns of di-versity, distribution and abundance to abiotic factors.

The other view sees an ecosystem as a machine thatprocesses material. The emergent properties which arisefrom interactions between the components demand quan-tification of processes in different modes and scales thanthose defined by the biotic components alone. To predictthe behavior of a complex system like a coral reef mayrequire the measurement and modelling of a small numberof high-order variables which integrate component beha-vior and capture the essential functions of the entire sys-tem (Simon 1973; Field et al. 1989). Energy, chemical orinformation currencies are usually used in these models: inpart because good physical-chemical theory and engineer-ing models are available; in part because they integrateand are measurable at the larger, longer scales of ecosys-tems. Recent applications use network analysis of carbonfluxes to predict significant change in the trophic structureand function of reef communities in response to shiftsfrom micro to macro-algal dominance (e.g., Johnson et al.1995), or use whole-reef scale biogeochemical budgetsto quantify the small contribution of reef metabolismto global climate change (e.g., Smith and Buddemeier1992).

There is much to be learned about coral reefs fromdeveloping and exploring the contrasts between popula-tion-community and mass-balance approaches to thestudy of ecosystems. Certainly there is no shortage ofrelevant literature (e.g., Jones and Lawton 1994; Pattenand Jorgensen 1995) but few good examples from reefresearch. In assessing ecosystem processes it is a mistaketo focus only on the physical and biogeochemical ap-proaches of systems ecology, because the abundance andbehavior of species populations can have profound effectson material fluxes and budgets (e.g., Smith et al. 1981showed how the presence of a single species of algaestrongly affected a reef ecosystem’s response to change insewage input). Reef ecologists, like those who seek emer-gent properties in other clearly-bounded ecosystems(e.g., lakes: Edmondson and Lehman 1981; Schlesingerand Reiger 1982), are not yet in a position to identifya single approach as ‘‘right’’: again, it depends on thequestion posed and the scale of the phenomenon underinvestigation.

The alternative approaches are effectively reconciled inthe ‘‘dual hierarchies’’ of O’Neill et al. (1986 p. 198), whichrecognize their differences but also their similarities. Thetraditional hierarchy of organization is split into a set ofbiotic levels and a set of functional levels, but the essen-tials of hierarchy theory (Webster 1979) are thought toapply to both (Pohl-Wostl 1993). It is necessary to con-sider both approaches, even when focusing on one. Someare working to understand how the details of lower levelsinform processes at higher levels, others are working topredict system behavior with as few details as possible.The models, methods, time and space scales of our obser-vation sets are appropriately diverse. It is a tribute to thematurity of coral reef science that this dichotomy is be-coming a non-issue: I think we all recognize hierarchicalorganization and the cruciality of scaling in reef ecosys-tems. Regardless of the hierarchy and scales in which wechoose to work, the behavior of that system may notnecessarily predict the behavior of others nested within orwithout. Reef ecosystems (no matter how defined) are morethan the sum of their nested parts (sub-systems). We are all,in some sense, striving to discover how much more: in thissense at least, we are all studying ecosystem processes.

Current contributions of ecosystem research to coral reefscience

The existence of such a large, multidisciplinary scientificsociety as the ISCRS, focusing for a week on a single, raretype of seabed reflects the pervasive and compelling con-cept of the coral reef as an ecosystem, and demands therecognition of processes operating at the levels and scalesof entire reefs. Management based on single species popu-lation models has been demonstrated to be impractical inthe socioecological context of tropical reef ecosystems,while (largely untried) management based on higher levelsof organization (i.e., habitat, ecosystem) is increasinglyperceived as the only hope of conserving coral reefs (e.g.,Bohnsack and Ault 1996; Christensen et al. 1996).

There is a set of questions facing coral reef sciencewhich either explicitly or implicitly forces us to consider

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processes at the higher levels and larger-longer scales ofecosystems. They are the questions that now, and prob-ably in the near future at least, will continue to set priori-ties for research:

1. In face of anthropogenic environmental change, willcoral reefs continue to exist in form and function asthey did during the pre-industrial Holocene?

2. What are the forms and magnitudes of organic andinorganic products and services man can remove fromcoral reefs on an ecologically sustainable basis?

3. In what ways and to what extent do coral reefs interactwith adjacent, non-reef ecosystems?

Scarcely a piece of reef research cannot be embedded inat least one of these questions, no matter the hierarchy,level or scale of the process it seeks to investigate. Ecosys-tem models and measurements of ecosystem processes areessential to all three.

The first question is essentially the topic of the SCOREWorking Group 104 — Coral reef responses to globalchange (Buddemeier 1995). Key ecosystem approacheshere are the application of geological models of reef per-formance during the Pleistocene and Holocene to predictchange under various greenhouse scenarios. Smith andBuddemeier (1992) convincingly use ecosystem pro-cess measurements and analytical tools to scale reef metabo-lism to carbon flux over a broad range of cases, demon-strating that normal reef metabolism usually results insmall net efflux of CO

2to the atmosphere. There is, of

course, significant variation in the rate, but whetherthe net flux is positive or negative, the role of reefs inexacerbating or ameliorating atmospheric CO

2concen-

tration will always be minuscule on human time scales(Buddemeier, 1996), although possibly significant atgeological scales (Opdyke and Walker 1992).

Another aspect of the system response to environmentalchange question concerns shifts between alternate stablestates for reef benthos: micro or macroalgal dominated(Hatcher 1984; Done 1992; Knowlton 1992). Models in-corporating biotic forcing and non-linear interactionswithin and among system levels, which can be extended towhole reef and decadal scales, are needed here (e.g., May1977; Field et al. 1989; Holling 1992). This is a tall orderthat should foster new applications of ecosystem analysisto reefs.

The second and third questions of harvestable exportsand transfers to and from adjacent ecosystems are moretractable, given current understanding of reef ecosystemprocesses and the models, tools and measurements at ourdisposal. The advantage is that reasonable answers tothese questions can be made based primarily on esta-blished physical and chemical principles, and rather crudeassumptions about the biology. The essential model isa biogeochemical budget in which the total fluxes ofinorganic and organic matter are huge, but the net fluxesare so small that measurement becomes problematic, evenwith good, system level techniques (Smith 1988; Smith andKinsey 1988). For example, excess production (E) by mostreef ecosystems studied to date is only about 3% of theirgross photosynthetic production, and the absolute magni-tude of E approximates the same low value per unit areaas the oligotrophic ocean (Crossland et al. 1991). Yet this

is the amount of organic material available to supportboth sustained reef growth and export to man and adja-cent ecosystems. Whether the excess production of reefs inmesotrophic oceans is correspondingly higher remains anoutstanding question because so few system-levelmeasurements have been made of such reefs. Averagedestimates of excess production from the handful of whole-reef measures available suggest that only about 15% ofE accumulates in reef structure and that 10% at most isharvested by man (Crossland et al. 1991). The remaining75% of E is assumed to be exported from the reef system.Recent measurements by Erez (1990) based on near-reefconcentration gradients suggest that this number is of theright order for Red Sea fringing reefs.

The magnitude of the proportion of E harvested andavailable for harvest by man from reefs is a key issue thatclearly requires ecosystem-level models and the measure-ment of ecosystem processes. Expressed on an areal basis,the value derived from measures of community metabo-lism (Crossland et al. 1991) corresponds to about onetwentieth of the primary production Pauly and Christen-sen (1995) estimated was required to sustain existing fishcatches from reefs, based on the ECOPATH (top-down)model. The discrepancy between these estimates does notnecessarily result only from error compounding introphodynamic models (e.g., Grigg et al. 1984 obtainedrather close agreement on estimates of net system produ-ctivity using ECOPATH and community metabolismmeasures). It suggests that the average reef (or at least thetypes that man fishes most intensely, such as fringing reefsaround densely-populated coasts) has a higher E thanmost reefs measured to date, or that more of the E remainsin these systems in a form suitable to support harvestablesecondary production.

The question of variability amongst reef systems used tocalibrate and verify these models is a crucial one. The bulkof the data come from about sixty measurements of reefflat metabolism at sea level (Kinsey 1983, 1991). They givethe tight modal results that have led to the sweepinggeneralization that entire reef systems (and, by areal scal-ing, the global reef signal) have P/R ratios only slightlygreater than one, corresponding to values of E only slight-ly greater than zero (Smith 1988; Crossland et al. 1991;Gattuso et al. 1995). The outliers are interesting in thatthey are either reefs which have not yet reached sea level(the high E reefs, e.g., Adey and Steneck 1985) or whichreceive substantial inputs of organic material (the negativeE reefs, Kinsey 1983). Such reefs are abundant throughoutthe world as bank barrier and fringing types, which aregenerally closer to human development than emergentbarriers and atolls. It follows that a more representativemodel of coral reefs’ capacities to sustainably export or-ganics (and perhaps a reconciliation of the discrepanciesbetween reductionistic and holistic measurements of eco-system processes) will now be better served by studies ofsubmerged, near shore, and nutrient enriched reefs thanby more sampling of reef flats at sea level in the oligo-trophic ocean. Measuring community metabolism in suchsystems (which are often very open hydrodynamically andbiogeochemically) poses serious methodological prob-lems, but they are not insurmountable (e.g., Smith andHarrison 1977; Rogers 1979; Adey and Steneck 1985).

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Fig. 3. The concept of new production (PN%8

) applied to the coralreef ecosystem. A schematic diagram splits the primary productionof organic material (P

T05!-), resulting from the processes of photosyn-

thesis (P) and nutrient assimilation, into a component (PN%8

) thatdraws on allochthonous nutrients and a complementary one (P

R%'%/)

that uses nutrients remineralized from organic material already inthe system. The analogous terms formalizing community metabol-ism (excess production and respiration by the entire community) areshown in brackets. For simplicity the components and processes ofsecondary production based on P

T05!-are not shown, and the or-

ganic pool includes both living and detrital organic material. Netinputs of nutrients to the reef (most of the total input is simplyadvected through) are depicted from the atmosphere (as dinitrogen),and from the ocean as both dissolved inorganic nitrogen and phos-phorus and particulate organic material containing these nutrients,which are delivered to the reef hydrodynamically. The main path-ways of nutrients in simplified marine systems for which P

N%8has

been estimated are shown with bold arrows: the uptake by plants ofnew DIN delivered by vertical mixing, the uptake of ‘‘old’’ DINremineralized from organic production within the system, and theloss of organic materials from the system due to the sinking oforganic particles. In reef systems atmospheric and advective inputsof nutrients (including gaseous and organic forms respectively) takeon a greater significance, resulting in other nutrient pathways(dashed arrows). The uptake by plants of nutrients derived from thecapture, metabolism and subsequent remineralization of ‘‘new’’ par-ticulate organic material (N

POM) is a potentially significant contribu-

tion to PN%8

of reefs, which is not reflected in estimates of net systemproduction based on community metabolism (i.e., E is less thanPN%8

by an amount equivalent to the respiration of the NPOM

).Export of system-produced organics greatly exceeds the loss tosedimentation in reef systems, and in dynamic equilibrium advectivelosses and harvests will approximate P

N%8but may be under-

estimated by E

New production in reef ecosystems

‘‘The concept of new production provides a conceptualbasis for the relationship between nutrient supply andecosystem function, and how these relate to the earth’sbiogeochemical cycles.’’

—¹. Platt, P. Jauhari and S. Sathyendranath (1992)

One of the most informative ecosystem measures resultsfrom the partitioning of organic production into a main-tenance term and a net term. Derived originally fromenergy budgets for individual organisms (another exampleof the scale-independence of some ecosystem models), theparameterization recognizes that the component of pro-duction not consumed within an ecosystem is available foraccumulation or export. Obviously this bears directly onthe questions of nutrient supplies to, and organic exportsfrom, reefs.

The key concept here is that of ‘‘new production’’(P

NEW), as originally defined in nitrogen currency for the

photic zone of the pelagic ecosystem by Dugdale andGoering (1967). It is the component of primary produc-tion which is derived from allochthonous nutrient inputs.They used the net nitrogen flux in a dynamic equilibriumbox model of the mixed layer to partition the primary

production into new and recycled components (Fig. 3).The convenient nitrogen dynamics of the photic zonemean that new production is well-estimated by the flux ofnitrate into the system (mainly through vertical mixing),while the remineralization of organic matter within thesystem is the main source of ammonium. Thus, am-monium assimilation estimates the recycled production:that component of primary production derived fromautochthonous nutrients. The two types of production areobviously complementary and additive to yield the totalnet primary production in the system. The assumed pro-portionality of nitrogen flux to new organic productionmeans that the magnitude and type of system productioncan be inferred simply by measuring and budgeting thetwo inorganic nitrogen species in a controlled volume ofseawater (be it a bottle or an upwelling zone).

Subsequent work has developed the concept of newproduction into a powerful generality by using the dimen-sionless ratio ‘‘f ’’ (i.e., the ratio of P

NEWto total primary

production) to effectively classify the degree of closure andtrophic status of pelagic production systems in differentparts of the ocean (despite significant discrepancies be-tween the theoretical and operation definitions of theterms, e.g., Platt et al. 1992). The concept is directly rele-vant to the questions of limitation, accumulation and

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export that characterize the study of ecosystem processesin coral reefs. The measurement and calculation ofPNEW

(and the f-ratio) for coral reefs, however, is muchmore difficult than for the pelagic ecosystem because ofthe variety and magnitude of nutrient supplies to supportprimary production (Fig. 3). The reef is fixed relative tothe water mass, so advective processes such as topo-graphic upwelling, boundary-layer mixing and wavepumping deliver large amounts of nutrient in both dis-solved and particulate form (Atkinson 1988; Hamner andWolanski 1988). Dinitrogen fixation (atmospheric input)is also a significant contributor of allochthonous nitrogento support new production in reef systems, and losses tothe atmosphere (denitrification) are also likely to be sub-stantial in some reef habitats (D’Elia and Wiebe 1990).The complexity of the nitrogen cycle in reefs means thatsimple nitrate and ammonium fluxes cannot be used topartition new and recycled production, but estimates ofPNEW

based on budgets of phosphorus should be possible(Smith 1984, 1988).

The source of inorganic nutrients to support PNEW

inatolls has been postulated to be the deep ocean waterupwelled through the reef matrix by thermal convection(Rougerie et al. 1992). An impressive body of biogeo-chemical research demonstrates the existence of geoendo-thermal upwelling, but the significance of its contributionto P

NEWis difficult to assess because of the operational

problems in distinguishing the new nutrient supply fromthe rapid regeneration of nutrients from organic matter inthe coral reef matrix (Tribble et al. 1994).

The fact that much of the advective flux of nutrients toreefs is in the form of particulates further complicates theestimation of P

NEW. Some of the material is captured by

the reef as plankton (i.e., by the ‘‘wall of mouths’’, Hamnerand Wolanski 1988) and subsequently metabolized. In-puts of nutrients in organic form must first be re-mineralized before they can support new production(Fig. 3), but they represent a potentially large (and untilrecently, overlooked) supply of allochthonous nutrients toreefs (Kinsey 1991). Of course, great quantities of organicmaterial are also advected out of reef systems as detritus,so the net result of particulate exports minus importsprovides another means of estimating P

NEW(assuming the

system’s organic pool is in steady state). Estimating themagnitude of particulate fluxes at whole-reef scales isdifficult, but measures by Erez (1990) and Ayukai (1995)demonstrate that the nutrient inputs in the form of parti-culates captured by the reef can be of the same order as thenet system production!

In defining PNEW

for reefs it is tempting to equate it withexcess production (Kinsey’s ‘‘E’’: 1983). Although the indi-ces are conceptually similar, the operational definitionsand methodological constraints differ. Excess productionis derived from community metabolism measurementsthat balance total system photosynthetic production withthe respiration of all reef organisms. The remainder (E)underestimates P

NEWfor reef ecosystems because parti-

culate organic inputs must first be respired before thenutrients they contain can be used to support new produc-tion. Reef systems in which organic nutrient inputs elevatePNEW

will have a correspondingly higher community respi-ration, thereby depressing E. Thus may explain in part

why E has been found to be so constant across a ratherlarge range of reef ecosystems (Kinsey 1991), despite largediscrepancies in measures of yield (export production).

The bottom line is that PNEW

of reefs differs from, and ispotentially greater than, E by some variable, but possiblylarge amount. The implication is that the proportion ofproduction available for harvest or export to adjacentecosystems based on measurements of community meta-bolism may be underestimated for some reef systems. Thediscrepancy will be most pronounced in more open reefsystems (Fig. 2) receiving significant particulate inputsand supporting high macroalgal biomass (i.e., those mostlikely to be subject to anthropogenic influence). These arethe types of reefs for which we have the fewest measures ofecosystem processes and for which the demand for man-agement science is greatest.

Indices of ecosystem function like E and PNEW

captureemergent properties of entire communities (e.g., theirtrophic status or degree of internal and external coupling)and can be used to assess their responses to variation inthe environment (e.g., as the f-ratio predicts planktoncommunity performance in oligotrophic and eutrophicareas of the ocean, Platt et al. 1992). Large-scale (geo-graphic) differences in ecological processes in reef ecosys-tems also appear to be closely related to variations in thenutrient supply regime (Hallock and Schlager 1986; Birke-land 1996). Models that predict the response of reef pro-duction processes to local and global increases in nutrientsupply are the most urgent requirement of ecosystemscience.

The question of nutrient limitation of reef productivityis of particular interest from both a theoretical and man-agement perspective (Atkinson 1988). In contrast to muchof the ocean, the assumption of nutrient limitation of netprimary productivity is questionable in reef systems. Ex-perimental work at scales of small portions of reef habitat(e.g., Kinsey and Davies 1979; Bilger and Atkinson 1995),up to entire reef lagoons (e.g., Grigg et al. 1984; Smith1988) suggest that the nutrient supply rate exceedsthat required to support the observed net productivityof reef ecosystems (even though restrictions on uptakemay limit gross production rates). If nutrients donot regulate primary production on reefs, however, itchallenges the current formalization of new production(Platt et al. 1992).

Finally, because the major pool and pathway of exportfrom reef systems is detrital organic material (Alongi 1988;Sorokin 1995), measurements of magnitude, form and fateof detritus in coral reef ecosystems provide indices of thetrophic status and processes controlling export produc-tion. For example, reefs that export large quantities ofmacroalgal detritus (e.g., Killar and Norris 1988) exhibitan imbalance of primary production and grazer consump-tion compared to other reefs (e.g., Crossland and Barnes1983) that may indicate progress towards a benthic com-munity phase shift long before it is measurable as anincrease in macroalgal biomass. Although decompositionprocesses are more diverse and difficult to measure thanproduction processes, their study is becoming a growthindustry (e.g., Ducklow 1990; Riddle et al. 1990; Sorokin1995) with major benefits for our understanding of thefunction of coral reef ecosystems.

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Synthesis and closure

‘‘The likelihood that measurements made at a particularscale will reveal something about ecological mechanismsis a function of the openness of the system’’

—J.A. ¼iens (1989)

In trying to synthesize this discussion of reef ecosystemprocesses, I return to the concept of the closure continuum(Fig. 2). For many of the questions discussed here, theappropriate models and methods are largely determinedby the position of the ecosystem on this continuum. In reefecosystems the degree of hydrodynamic closure is theprimary determinant of that position, thereby affectinga broad range of ecosystem processes from nutrient up-take to competitive dominance of certain corals. Reefecosystems range from very open linear bank barrier reefsfar from shore, which have not yet reached sea level,through fringing reefs with nearshore lagoons, to emer-gent atolls with enclosed lagoons and multiple patch reefsystems. With increasing hydrodynamic, thermodynamicand organizational closure, the physical and biologicalprocesses that enhance larval retention, nutrient recyclingand homeorhesis increase, and the connections with ad-jacent systems and production available for growth andexport decrease.

To answer the key questions facing coral reef science inthe next millennium, I believe that we should attempt bothpopulation-community and materials-flux measurementsacross a range of spatial-temporal scales in the more opentypes of reef systems. Comparisons of ecosystem processesamong reefs far apart on the closure continuum will im-prove our models and contribute to the quest for someunified body of theory.

Acknowledgements. Thanks to Richard Aronson, AnnamarieHatcher and Donald Kinsey for stimulating discussions, and toNancy Knowlton, Steve Smith and Bill Wiebe for helpful reviewswhich significantly improved the manuscript. I acknowledge themany reef scientists whose work educated and inspired me but wasunable to cite herein. A. Hatcher’s help drafting the figures is muchappreciated. Support was provided through the Canadian Inter-national Development Agency and the organizers of the EighthInternational Coral Reef Symposium, for which I am grateful.

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