nutrient enrichment on coral reefs: is it a major cause of ...people.uncw.edu/szmanta/pdfs/szmant...

743Q 2002 Estuarine Research Federation

Estuaries Vol. 25, No. 4b, p. 743–766 August 2002

Nutrient Enrichment on Coral Reefs: Is It a Major Cause of Coral

Reef Decline?

ALINA M. SZMANT*

Department of Biological Science and Center for Marine Science, University of North Carolina atWilmington, 5600 Marvin K. Moss Lane, Wilmington, North Carolina 28409

ABSTRACT: Coral reefs are degrading worldwide at an alarming rate. Nutrient over-enrichment is considered a majorcause of this decline because degraded coral reefs generally exhibit a shift from high coral cover (low algal cover) tolow coral cover with an accompanying high cover and biomass of fleshy algae. Support for such claims is equivocal atbest. Critical examination of both experimental laboratory and field studies of nutrient effects on corals and coral reefs,including the Elevated Nutrient on Coral Reefs Experiment (ENCORE) enrichment experiment conducted on the GreatBarrier Reef, does not support the idea that the levels of nutrient enrichment documented at anthropogenically-enrichedsites can affect the physiology of corals in a harmful way, or for most cases, be the sole or major cause of shifts in coral-algal abundance. Factors other than nutrient enrichment can be significant causes of coral death and affect algal cover,and include decreased abundance of grazing fishes by fishing, and of grazing sea urchins to disease; grazing preferencesof remaining grazers; temperature stress that kills coral (i.e., coral bleaching) and creates more open substrate for algalcolonization; sedimentation stress that can weaken adult corals and prevent coral recruitment; coral diseases that maybe secondary to coral bleaching; and outbreaks of coral predators and sea urchins that may be secondary effects ofoverfishing. Any factor that leads to coral death or reduces levels of herbivory will leave more substrate open for algalcolonization or make the effects of even low-level enrichment more severe. Factors that contribute to an imbalancebetween production and consumption will result in community structure changes similar to those expected from over-enrichment. Over-enrichment can be and has been the cause of localized coral reef degradation, but the case forwidespread effects is not substantiated.

IntroductionCoral reefs worldwide, and in particular in the

Caribbean and southern Florida, are experiencinga recent period of decline. There has been a majorloss of coral cover and diversity (Hoegh-Guldberg1999; Wilkinson 2000) coupled in many areas withan increase in algal biomass and shift in algal com-munity structure (McCook 1999). Coral reef algalcommunities are very productive (Hatcher 1988,1990) but heavily grazed by herbivorous fishes andechinoids, and are made up mostly of low biomassred crustose coralline algae (CCA), mixed assem-blages of short turfs, and calcified articulate forms(Steneck and Dethier 1994; Carpenter 1997; Hix-on 1997). Fleshy corticated forms are usually lim-ited to the back reef and refuges from herbivores.With minor exceptions reef-building corals domi-nate the substrate on healthy accreting reefs andalgal biomass is low. On degraded reefs, algal bio-mass increases as the dead coral substrate and CCAbecome overgrown by thick turfs that trap sedi-ment, and a variety of fleshy foliose and corticatedfoliose macrophytes become abundant. Because al-gae, like other plants, can respond to increased

* Tele: 910/962-2362; fax 910/962-2410; e-mail: [email protected].

nutrient availability with increased growth poten-tial, any such shift in community structure fromcoral-CCA-short turf to fleshy macrophyte-tall turfis commonly attributed to anthropogenic nutrientinputs (e.g., Johannes 1975; Pastorok and Bilyard1985; Bell 1992; Bell and Elimetri 1995; Lapointe1997).

Community structure of coral and algal compo-nents is determined by more than just the growthpotential of the algae. Sedimentation stress, stormdamage, thermal stress, over-harvesting of grazersand predators, physical damage from ship ground-ings, coral mining, and destructive fishing practic-es are just a sample of important natural and an-thropogenic stresses that are presently affectingcommunity structure and reef health and contrib-uting to present day coral reef decline ( Johannes1970; Hatcher et al. 1989; Glynn 1993; Dubinskyand Stambler 1996; McCook 1999). The questionto be addressed here is how much coral reef de-cline is being caused by nutrient over-enrichmentitself as opposed to the numerous other factorsknown to be currently affecting coral reefs (Fig.1).

I evaluate reports based on the supporting evi-dence for nutrient enrichment and the other fac-tors that could simultaneously affect coral reefs.

744 A. M. Szmant

Fig. 1. Diagrammatic representation of the many anthro-pogenic and natural stressors known to be affecting coral reefhealth and community structure.

Fig. 2. Diagrammatic representations of two conceptualmodels relating nutrient levels to coral reef community struc-ture. A) Relative dominance model proposed by Littler and Lit-tler (1984). B) Eutrophication gradient model proposed by Bir-keland (1988).

Coral reefs prone to nutrient effects are usuallyexposed to other anthropogenic stressors that canmake a reef more susceptible to nutrient effects orcause symptoms similar to those expected from nu-trification. In this paper, nutrients refer to inor-ganic and organic forms of the elements nitrogen(N) and phosphorus (P). This includes nitrate, am-monium, and soluble reactive phosphate assimilat-ed by plants, as well as dissolved organic forms ofunknown composition (dissolved organic N, dis-solved organic P), that can be remineralized to theinorganic forms available to plants. In many areashuman activities have increased the flux of nutri-ents into coastal waters (5 nutrification, as op-posed to eutrophication, a term describing a morecomplex process involving organic production andaccumulation and the nutritional status of a com-munity; Nixon 1995), which alters the growth en-vironment of coastal marine plant communities,and often leads to changes in community and eco-system structure of the affected systems.

This paper is not a comprehensive review of cor-al reef decline, nor of all the facets of reef ecologyinvolved in decline. The subject matter of nutrifi-cation is complex and hotly debated with regardto its effects on coral reefs, so any attempt to crit-ically address this question will draw on a broadrange of often contradictory studies. With coralreefs presently declining at a rapid rate, it is im-portant to understand the complexity of these in-teractions, and to place the role of nutrients inperspective.

Nutrients as Determinants of Coral ReefCommunity Structure

Conceptual models are often used to summarizethe broad role of nutrients in structuring coral

reefs and are invoked by those advocating the roleof nutrification in coral reef decline. Littler andLittler (1984) proposed a relative dominance mod-el for four photosynthetic functional groups thatcompete for reef substrate (corals, turfs, corallinealgae, and macrophytes). In this model nutrients(bottom-up) and herbivory-physical disturbance(top-down) factors interact to determine commu-nity structure. Corals and turfs dominate underlow nutrient conditions depending on whetherherbivory levels are high or low, respectively. Dom-inance shifts towards fleshy macroalgae with in-creased nutrients and decreased herbivory (Fig.2a). One shortcoming of this model is that thereis an extensive literature showing CCA and short(highly grazed) turfs to be important componentsof pristine (low nutrient, high herbivory) coralreefs (Hatcher 1988, 1990). Predictions based onthis model may lead to incorrect inferences aboutcauses of community change (i.e., high CCA cover

Nutrient Effects on Coral Reefs 745

and low coral cover could be interpreted to indi-cate nutrification).

Birkeland (1987) proposed another scheme inwhich at low nutrient fluxes and oligotrophic con-ditions, corals and reef-building algae co-exist witha limited number of non-reef building algae andfilter feeders. The dominance of the latter twogroups increases along an eutrophication gradientwith filter feeders alone dominating under themost eutrophic conditions (Fig. 2b). Nutrient sup-ply (a factor of both concentration and advectiveflow; Atkinson 1988) is an implicit part of his oli-gotrophic to eutrophic gradient. The role of her-bivory in modulating shifts in community structuretowards more eutrophic components with in-creased nutrient fluxes was recognized but notmade an explicit part of the model.

Steneck and Dethier (1994) proposed a thirdmodel with similarities to the Littler and Littlermodel. They divide the algal community into sevenfunctional forms (corals are not one of the forms)that differ in size, canopy height, longevity, andbiomass-specific productivity. The relative abun-dance of the seven functional forms is determinedby interactions between life-history characteristics,productivity potential and growth dynamics (whichintegrates their responses to nutrients, light, waterflow, and other physical-chemical environmentalcharacteristics), and the disturbance potential(which includes herbivory pressure).

Both the Littler and Littler and Birkeland mod-els would predict that increasing nutrient fluxwould cause a loss of corals due to competitionwith algae, but their predictions differ otherwise.In the Littler and Littler model, fleshy algae wouldonly dominate if herbivory also decreases, and cor-alline algae would prevail if herbivory remainshigh. In the Birkeland model, non-reef buildingalgae would dominate over the corals and reef-building algal species (presumably fleshy algae be-come dominant over calcifying forms). The Ste-neck and Dethier model predicts that larger fleshyalgal forms could dominate with reduced distur-bance or herbivory even if there is no change inproductivity potential and nutrient supply. Thismodel does not make explicit predictions aboutthe shift in coral and algal dominance, but if coralsare grouped with the coralline functional groups,it would predict that fleshy algae would outcom-pete corals as nutrients increased or herbivory de-creased.

Ignoring the differences between models, allthree can be used to predict increased fleshy algaldominance with nutrient enrichment. This intui-tive relationship between enrichment and in-creased algal growth is the primary factor behindthe propensity to blame coral reef degradation on

nutrient over-enrichment. As McCook (1999) as-serted, this notion assumes that reef algae are nor-mally growing under nutrient-limited conditionsand that enrichment stimulates their growth. Theevidence for this basic assumption is poor andbased on three a priori assumptions. Coral reefsonly occur under extremely low nutrient condi-tions (Bell 1992; Bell and Elimetri 1995; Lapointe1997). This assumption is based on early studies ofa few mid-oceanic atolls such as Eniwetak whereambient nutrient concentrations are low (Odumand Odum 1955; Johannes et al. 1972). It does nottake into consideration a variety of recognizedsources of nutrients to even remote reefs, such asvarious forms of upwelling, endo-upwelling, highadvective flow, N fixation, bird guano, and atmo-spheric deposition. Nor does it consider that mostreefs occur on island or continental shelves wheresome level of natural terrigenous inputs are to beexpected (Sander 1981; Andrews and Gentien1982; Smith 1983; Atkinson 1988; D’Elia 1988;D’Elia and Wiebe 1990; Lee et al. 1992, 1994;Rougerie and Wauthy 1993; Smith and Johnson1995; Leichter et al. 1996). The high-latitude Hout-man Abrolhos reef complex maintained vigorousreef growth throughout the Holocene in spite ofnaturally elevated nutrient conditions (Crosslandet al. 1984; Collins et al. 1993). A second assump-tion is that algae on coral reefs are nutrient limit-ed, evidence for which is sparse and contradictory(McCook 1999). Algae differ greatly in their re-sponse to nutrient supply. Nutrients may stimulategrowth of some algae while that of others exhibitno change (Larned 1998; Schaffelke and Klump1998; Schaffelke 1999; Stimson and Larned 2000;Thacker et al. 2001; Smith et al. 2001). A thirdassumption is that under normal circumstances al-gae are competitively dominant over corals, whichhas been recently challenged (McCook et al.2001).

Evidence for Sensitivity of Coral Reefs toNutrient Enrichment

Coral reefs are found wherever, over geologicaltime scales, the combination of physical, chemical,and biological conditions favor the accretion of cal-cium carbonate secretions (limestone) in reef-building and calcareous algae dominated commu-nities. Decreasing temperatures and herbivorypressure, the trend of increasing nutrient avail-ability, and possibly decreasing aragonite satura-tion state with increasing latitude limit coral reefsto the tropics and subtropics (Wells 1957; Johanneset al. 1983; Miller 1998; Kleypas et al. 1999). Ele-vated nutrients can supposedly tip the competitivebalance in favor of macroalgae, especially if her-bivore densities are low. McCook et al. (2001)

746 A. M. Szmant

TABLE 1. Nutrient concentrations at selected reef sites. Examples of ambient levels at naturally or anthropogenically elevated sitesas well as major reef regions. For Canton, the values are from near the pass where coral cover was the highest. For older KaneoheBay data, values are lowest and highest for the five regions studied, plus the weighted bay mean. For the Great Barrier Reef (GBR),the Furnas et al. (1995) report includes a large number of data, and I selected means and SE for one representative lagoon stationfrom their Cairns section. Values for nutrients are in mM, and for chlorophyll a (chl a) are in mg l21. nd 5 not detectable.

Station Type NO3 1 NO2 NH4 PO4 Chl a

Canton Lagoon, upwelling area; Smith and Jokiel 1978 2.5 1.5 0.6 —Kaneohe Bay pre-sewage diversion; Smith et al. 1981 0.33 to 0.91

bay x̄ 5 0.410.57 to 2.28bay x̄ 5 0.67

0.28 to 0.88bay x̄ 5 0.33

0.68 to 4.67bay x̄ 5 1.13

Kaneohe Bay post-sewage diversion; Smith et al. 1981 0.27 to 0.66bay x̄ 5 0.37

0.38 to 0.57bay x̄ 5 0.43

0.09 to 0.18bay x̄ 5 0.11

0.55 to 1.33bay x̄ 5 0.78

Kaneohe Bay, central bay 1998; Stimson et al. 2001 0.17 (0.39) 0.21 (0.20) 0.08 (0.03) —Mamala Bay, Baseline, bottom 1993–1994; Grigg 1995 0.04 (0.02) 0.05 (0.02) 0.13 (0.01) 0.17 (0.06)Mamala Bay, High Wave, bottom 1993–1994; Grigg 1995 0.72 (0.02) 0.10 (0.06) 0.08 (0.01) 0.17 (0.06)Mamala Bay, Rain Event, bottom 1993/1994; Grigg 1995 0.11 (0.13) 0.11 (0.04) 0.12 (0.02) 0.27 (0.20)

GBR, One Tree Reef; Hatcher and Hatcher 1981offshorereef slopelagoonreef crest

0.31 (0.03)0.31 (0.12)0.95 (0.06)1.54 (0.16)

nd0.76 (0.24)2.86 (0.21)5.52 (0.62)

GBR, mid-lagoon Station 11; Furnas et al. 1995 0.05 (0.01) 0.46 (0.13) 0.08 (0.01) 0.35 (0.05)

Houtman Abrolhos Islands, Australia, Easter Group;Crossland et al. 1984front reef flatback reef flatlagoon

1.020.960.93

0.210.280.32

0.220.240.29

Brazil, developed; Costa et al. 2000WetDry

8.035.75

4.8110.69

1.420.35

—

Brazil, less developed; Costa et al. 2000WetDry

1.680.41

3.590.86

0.180.13

—

questioned the premise that corals are competi-tively inferior to algae, noting that many studiesdemonstrate the opposite (e.g., De Ruyter vanSteveninck et al. 1988; McCook 2001). Elevated nu-trients may also affect physiological interactions be-tween corals and their zooxanthellae by stimulat-ing the cell division rates of the intracellular sym-bionts (see below). Elevated nutrients are also as-sociated with higher levels of water columnproductivity and abundance of filter feeders andbioeroders (Birkeland 1977, 1987; reviewed byGlynn 1997). High rates of bioerosion will reducerates of carbonate accretion and limit reef building(Hallock 1988). Tropical shallow platforms char-acterized by naturally nutrient-rich conditions dueto high rates of upwelling or river discharge aregenerally devoid of coral reefs (Wells 1957; Hallockand Schlager 1986), but more moderate rates ofupwelling allow for moderate to extensive reefbuilding (Glynn 1977, 1993; Smith and Jokiel1978; Andrews and Gentien 1982; Smith 1983).High islands surrounded by fringing and barrierreefs usually have breaks in their reefs where riversdischarge into their coastal zones, giving evidencethat over reef-building time scales, inputs of ter-

restrial materials such as freshwater, nutrients, andsediments limit coral reef growth.

This broad general inverse relationship betweennaturally occurring, chronically elevated nutrientconditions and coral reef formation is the stron-gest evidence for a negative effect of high nutrientfluxes on coral reefs, and has given rise to the viewthat coral reefs are particularly susceptible to an-thropogenic nutrient enrichment. The potentialcontributions of low temperature in upwelling sit-uations and sediment-laden freshwater dischargeto lower coral cover and growth rates confound asimple distribution-based interpretation of nutri-ent effects on coral reef health. There is very lim-ited quantitative information on what constituteshigh or low nutrient levels (concentrations or flux-es) that either limit coral reef formation or lead totheir decline. From the scant data available it isapparent that coral reefs have formed under abroad range of natural nutrient regimes (Table 1),but there are few nutrient data for most reef areasto form a more complete view of this range (Cross-land 1983; D’Elia 1988; Sorokin 1990; Szmant andForrester 1996).

Anthropogenic nutrient enrichment is more


Fig. 3. Conceptual representation of processes by which nu-trients enter coastal systems and are recycled and accumulatein sediments mediated by primary producers, detritus forma-tion, and herbivores.

likely to affect coral reefs closer to shore, withinlagoons or embayments (limited circulation andflushing), and reefs associated with larger landmasses (high island and continental reefs), espe-cially near significant human populations. Mid-ocean atolls and offshore barrier reefs, which areexposed to high ocean energy and much flushing,would not be expected to be as easily affected. Be-cause the distribution of degraded reefs more orless fits this expectation (Wilkinson 1998), it is log-ical to suspect that local anthropogenic activitiesincluding nutrient enrichment are causing reef de-cline. Loss of coral often co-occurs with increasedalgal cover and biomass (Tomascik and Sander1987; Wittenburg and Hunte 1992), especially offleshy macroalgae that can overgrow corals, lead-ing some to conclude that nutrient enrichment isthe cause of the algal increases and that the algaethemselves are directly responsible for the loss ofcoral. One example of a natural nutrient enrich-ment event that demonstrated such a cause-effectrelationship was the sudden algal bloom caused byan unusual upwelling event in the Gulf of Eilat fol-lowing the eruption of Mount Pinatubo in 1992(Genin et al. 1995). Thick algal mats formed overthe coral reef benthos except at a few locationswhere grazer abundance was noticed to be high.About 20% to 30% of the corals were smotheredand killed by the algal mats that were clearlycaused by upwelled nutrients, supporting the com-mon tenet. Most published investigations that at-tribute high algal cover to nutrient enrichment donot include algal cover or nutrient time series, orexperimental work demonstrating that the higheralgal biomass was the cause of a decrease in coralcover.

The impact of eutrophication on coral reefs wasdramatically brought to the world’s attention inthe late 1960s and 1970s when the water columnof southern Kaneohe Bay, Hawaii, turned greenwith phytoplankton, its sediments turned anoxic,and its coral reefs were overgrown by the bubblealga, Dictyosphaeria cavernosa (summarized by Laws1992). Attribution of the algal blooms to two majorsewage outfalls was straight forward. After the sew-age discharge was redirected to an ocean outfall,noticeable reef recovery was achieved within a de-cade. The phytoplankton blooms subsided withina few years, but it took longer for D. cavernosa toretreat because it was capable of drawing nutrientsfrom the sediments over which it grew (rather thanthe water column; Larned and Stimson 1996), andthe sediments had become enriched during theperiod of discharge within the bay (Fig. 3; Smithet al. 1981; Laws 1992). Largely because of Kane-ohe Bay, nutrient enrichment and water quality de-cline are evoked as the primary cause for de-

creased coral cover at other locations that is ac-companied with increases in algal abundance.

Water quality degradation can be broader thanjust nutrification and also includes organic carbonenrichment, as well as metals and organic pollut-ants from numerous types of point and nonpointsources, including agricultural and storm water dis-charges. Many areas with increased nutrient inputsalso have increased sediment and pollutant loadsentering the coastal zone from agricultural activi-ties. Corals, as well as typical reef algae, are sensi-tive to sedimentation, especially by organic-rich,silt-sized sediments ( Johannes 1970; Rogers 1990;Dubinsky and Stambler 1996; Fabricius and De’ath2001). It may be difficult to distinguish betweenthe effects of just nutrients and those caused bysediments rich in nutrients and organics.

Other Causes of Coral Reef DegradationAny factor that kills coral, such as storms, bleach-

ing, disease, and predation, opens up substrate foralgal colonization and can lead to gradual and po-tentially permanent coral reef degradation if coralsare not able to recruit or grow back (e.g., Ostran-der et al. 2000). Bleaching is caused by periods ofabnormally warm seawater temperatures and/orexcess ultraviolet radiation. It has caused loss ofcoral cover on the order of 15% to 90% in theIndo-Pacific and Caribbean during the extremelywarm years of 1997 and 1998 (Hoegh-Guldberg1999; Wilkinson 2000). The increased incidence ofcoral diseases noted over the past decade may berelated to corals being physiologically debilitatedby repeated bleaching events (Harvell et al. 1999).Partial mortality is a common consequence of cor-al bleaching and disease, exposing coral skeletonsto colonization by algae. Algal colonization successmay be increased due to reduced herbivory result-ing from overfishing (Ostrander et al. 2000). Theincreased algal cover leads to a greater susceptibil-

748 A. M. Szmant

Fig. 4. Relationship between biomass of grazing fishes andalgal cover on 19 reefs from seven geographic locations in theCaribbean (from Williams and Polunin 2001).

ity of the remaining part of the coral colony toalgal overgrowth. A major shift in communitystructure can then occur without any change innutrient conditions even though it may appearsimilar to what we would expect from a nutrient-induced effect.

Overfishing, by reducing grazing pressure, canaffect the ability of reefs to recover from distur-bance and lead to degradation. Fishing is a majorhuman activity on coral reefs, and reefs worldwideare overfished, especially those close to human set-tlements (Roberts 1995; Wilkinson 2000; Jacksonet al. 2001). The potential for overfishing to causecoral reef degradation is not generally recognized,but it is as serious a threat to coral reefs as that ofwater quality degradation (Szmant 1997). Loss oflarge predators and herbivores can result in tro-phic shifts because of decreased predation on reeforganisms such as algae, sea urchins, and coralli-vores (McClanahan and Shafir 1990; McClanahan1995; Roberts 1995). Williams and Polunin (2001)report an inverse relationship between herbivorousfish biomass and macroalgal cover over a broadrange of Caribbean reefs (Fig. 4). Reefs with high-er fish biomass were within no-fishing reserveswhere regulations were enforced. Reefs with morefish and less algae have greater potential to recoverfrom storm impacts (Done 1992, 1999; Roberts1995; Bythell et al. 2000). Algal blooms are com-mon after major storms but usually dissipate soonthereafter. Coral cover is re-established by success-ful re-attachment of coral fragments or by coralsexual recruitment (Highsmith 1982; Harrison andWallace 1990; Hughes et al. 1992). If grazers arereduced in abundance, the initial algal bloom can

be followed by a succession of more enduring algaltypes, and coral cover is not re-established. Such asuccessional sequence has been described as an al-ternative stable state of coral reef systems: an algal-dominated reef (Hatcher 1984; Hatcher et al.1989).

Outbreaks of coral diseases and corallivores haveboth killed much coral exposing dead skeletons toalgal colonization. Increases in algal cover on Pa-cific reefs followed outbreaks of the corallivorousseastar, Acanthaster plancii, beginning in the 1960s,and more recently, of the corallivorous snails Dru-pella spp. (Done 1999). Diseases have also contrib-uted to reef degradation indirectly by killing offcoral reef organisms that are ecologically impor-tant (Harvell et al. 1999). In the Caribbean, a dis-ease epidemic in 1983 killed 95% of the sea ur-chin, Diadema antillarum (Lessios 1988), which wasthe major invertebrate herbivore controlling algalpopulations on reefs, especially where herbivorousfishes were overfished (Hay 1984). Within weeks,increases in algal cover followed the die-off, occur-ring before declines in coral cover were docu-mented (e.g., Carpenter 1986; Lessios 1988;Hughes 1994; Steneck and Dethier 1994; Hugheset al. 1999).

It is widely accepted that climate change-relatedcauses of coral reef decline have been extensiveduring the past two decades, and especially duringthe past three years (Hoegh-Guldberg 1999; Wil-kinson 2000). Coral bleaching has affected evenpristine reefs in remote areas where eutrophica-tion is unlikely and overfishing less severe, but nosingle stress factor discussed is working alone. Thechallenge for scientists and environmental man-agers is to have sufficient understanding of localsystems and the ability to discern among the po-tential causes of decline. The effects of local waterquality degradation and overfishing can exacer-bate global warming and bleaching. While much isknown about the generalities of coral reef func-tion, our understanding of major ecosystem pro-cesses and their interactions is rudimentary, and itmay be difficult to pin-point the cause of a givenreef’s decline.

Experimental Evidence for Nutrient Effects onCoral Reefs

Nutrients can affect coral reef health throughdirect physiological effects on the corals, such asreduced growth or reproduction rates, or in-creased susceptibility to bleaching or disease mor-tality, mainly via effects on the coral-zooxanthellaesymbiosis; indirect effects on coral reef communitystructure via stimulating growth of reef algae orpromoting dominance by nutriphilic algae gener-ally uncommon on coral reefs; and reducing car-


bonate accretion by promoting increased abun-dance of filter feeders, which are responsible forbioerosion (this topic will not be discussed furtherbecause a cause-and-effect relationship betweenrates of bioerosion and coral physiology or shiftsin coral and algal dominance has not been dem-onstrated). Experimental evidence for effects ofnutrients on the physiology and ecology of reefcorals or coral reefs can be derived from eitherlaboratory or field experimental work, or fromstudies of field systems exposed to either natural-or anthropogenically-elevated nutrient conditions.

PHYSIOLOGICAL EFFECTS

Laboratory

Most of the evidence for direct effect of nutri-ents on coral physiology is from laboratory studiesin which corals were exposed to elevated nutrientconcentrations in aquaria for periods of a fewweeks to months. A limitation of such studies hasbeen the high nutrient concentrations used in or-der to obtain effects during short experimental pe-riods: e.g., 20 to 200 mM nitrate (Taylor 1978); 10to 50 mM ammonium (Hoegh-Guldberg and Smith1989; Jokiel et al. 1994); 10 mM phosphate (Du-binsky et al. 1990). Such concentrations are ordersof magnitude higher than the highest levels mea-sured on polluted coral reefs (Table 1), and it isdifficult to extrapolate from them to effects atmuch lower elevated concentrations. Most of theseexperiments were designed to examine the hy-pothesis that zooxanthellae in hospite are nutrientlimited. Their results must be interpreted cautious-ly when deducing negative effects of nutrients,since the experiments themselves were not de-signed for that purpose. The most common effectsreported in enrichment experiments with ammo-nium were increases in zooxanthellae density andzooxanthellae chlorophyll content, often accom-panied by elevated rates of photosynthesis. Theseresponses to enrichment were interpreted to indi-cate that zooxanthellae in hospite are normally nu-trient-limited, but the long-term effects of releas-ing the algae from such limitation remain unclear.

The most ecologically significant effect of ele-vated nutrients on coral physiology has been re-duced calcification or skeletal extension rates, es-pecially under P or P plus ammonium enrichment(Lamberts 1978; Stambler et al. 1991; Stimson andKinzie 1991). Taylor (1978), however, reported anincrease or no change in growth with ammoniumor nitrate enrichment, respectively, and Stambleret al. (1991) found no change in growth with phos-phate only. Of the more recent work designed toinvestigate effects of enrichment, McGuire (1997)found no measurable effect on a number of coral

and zooxanthellae parameters at sustained expo-sure to 2 mM ammonium for 8 wk but did findvariable negative effects including decreasedgrowth rates at 5 and 10 mM ammonium. Ferrier-Pages et al. (2000) also found reduced growthrates of coral nubbins exposed to 20 mM ammo-nium and 2 mM phosphate, separately and togeth-er, for 10 wk, and that recovery after return to nor-mal nutrient levels was slow, especially for the cor-als exposed to phosphate. Marubini and Davies(1996) found a 25% to 50% decrease in growthrate for two species of coral exposed to as low as 1mM nitrate (other treatments were 5 and 20 mM),but that the effect of 20 mM nitrate or ammoniumenrichment were eliminated if 2 mM bicarbonatewas added to the seawater medium (Marubini andThake 1999). In work with a different species Ma-rubini and Atkinson (1999) found no effect ongrowth at 5 mM nitrate but did find large reduc-tions in calcification with decreased pH of seawa-ter. Atkinson et al. (1995) reported higher long-term growth rates of corals exposed to elevated nu-trients (5 mM nitrate, 2 mM ammonium, and 0.6mM phosphate) in the Waikiki Aquarium wherethe sea water was low in pH and supersaturated inCO2. There is increasing support for the hypothe-sis that reduced calcification rates, when they oc-cur under nutrient-enriched conditions, may bedue to competition for CO2 and/or carbonate be-tween the processes of photosynthesis and calcifi-cation.

Laboratory evidence shows that short-term ex-posure to significantly elevated nutrients, especiallyphosphate, can cause reductions in skeletal growthfor some species. Inconsistent results between in-vestigators may be due to different species used orexperimental conditions and laboratory artifactssuch as changes in the pH, carbonate equilibrium,and carbonate species concentrations, which werenot often measured or controlled. Most of thestudies only found significant changes in zooxan-thellae density or coral growth rate when they usedconcentrations of nutrients significantly higherthan those reported for heavily polluted reef areasor reef areas with intense upwelling (Table 1). Asmost of the laboratory studies lasted only 2 to 3mo, there is also the possibility of long-term ac-commodation to elevated nutrients by the coralsand their endosymbionts. Since decreased coralgrowth rates appear to be a consequence of in-creased zooxanthellae densities, eventually coraltissues could catch up and growth rates return tonormal or even increase. The sustained highgrowth rates of the corals in the Waikiki Aquariumsystem (Atkinson et al. 1995) suggest that this is arealistic expectation.

750 A. M. Szmant

TABLE 2. Subset of water quality characteristics reported byTomascik and Sander (1985) for a series of stations along thewest coast of Barbados characterized by the authors to representa gradient of eutrophication due to sewage discharge. The twomore polluted and two more pristine stations are ca. 15 kmapart along an open coastline. Values for nutrients are in mM,for chlorophyll a (chl a) are in mg l21, and for suspended par-ticulate matter (SPM) are mg l21.

StationType NO3 NH4 PO4 Chl a SPM

More polluted2122

0.824.42

0.982.70

0.100.21

0.901.04

7.117.32

More pristine2122

0.360.45

0.540.56

0.060.06

0.420.55

5.214.26

FieldGrowth rates of corals from eutrophic localities

along the coast of Barbados were lower than thoseof corals from nearby more pristine ones (Tomas-cik and Sander 1985). Average nutrient concentra-tions at the two most polluted and two most pris-tine stations are summarized in Table 2. Statisticalanalysis of their water quality data revealed that sus-pended particulate matter (SPM) had the stron-gest inverse correlation with coral growth rates,making it unclear that it is justifiable to attributethe decreased growth rates directly to nutrient ef-fects. They also proposed that the corals exhibitedthe highest growth rates at intermediate levels ofSPM, and suggested that the corals could be feed-ing on the suspended organic material. Lewis(1976) showed that corals can derive some nour-ishment from feeding on SPM, and recent reportsconfirm the potential importance of this foodsource to corals (Rosenfeld et al. 1999; Anthony2000).

There are several reports of reduced growthrates of corals in upwelling areas where nutrientconcentrations are elevated, but the low tempera-tures associated with upwelling conditions can alsoexplain the reduced growth rates. Glynn (1977) re-ported a linear relationship between temperatureand growth for Pocillopora sp. in the Gulf of Pana-má with the lowest growth rates during the up-welling season, but growth rates increased steadilyduring the non-upwelling season reaching ratescomparable to those of corals in the adjacent non-upwelling Gulf of Chiriquı́. If elevated nutrientsduring the upwelling season were in part respon-sible for the lowered growth rates associated withthe upwelling, their effect did not extend into laterseasons when nutrient concentrations returned tonormal. Wellington and Glynn (1983) subsequent-ly compared growth and calcification rates of an-other eastern Pacific reef coral, Pavona clavus, and

found that the corals from the Gulf of Panamá hadboth higher calcification and linear extension ratesin spite of the upwelling than those from the Gulfof Chiriquı́. This is surprising given the low tem-peratures under which the Gulf of Panamá coralsgrew during half the year, but indicates that ele-vated nutrients do not always have a negative effecton coral physiology. Wellington and Glynn (1983)suggested that increased food availability duringthe upwelling periods could stimulate both tissueand skeletal growth. They also reported an inversecorrelation between extension rate and skeletaldensity, a general relationship that has been re-ported for other corals (e.g., Dodge et al. 1993;Lough and Barnes 2000).

ENCORE Field ExperimentThe most ambitious field experiment to investi-

gate the effects of nutrient enrichment, as narrow-ly defined here, on a number of coral reef pro-cesses, organisms, and coral physiology was the EN-CORE (Elevated Nutrient on Coral Reefs Experi-ment) project on the Great Barrier Reef (GBR).An important aspect of this experiment is that nu-trient enrichment was done under what otherwisewere considered pristine conditions, without con-founding effects of increased sedimentation, highorganic loading, or overfishing that co-occur atmost anthropogenically disturbed reef sites. Twelvemicroatolls in the One Tree Island reef lagoonwere divided into four treatments (control, 1N,1P, 1N1P) and dosed with nutrients daily for over2 yr (Koop et al. 2001). Loading was increasedfrom 10 mM ammonium and 2 mM phosphate to20 mM ammonium and 4 mM phosphate in thesecond year because of the lack of clear effects bythe original level of enrichment on many (most)of the systems studied. Nitrate and ammonium lev-els in this lagoon have been reported to be season-ally naturally elevated (Hatcher and Hatcher1981).

It was apparent early in the experiment that themost expected result for a major shift in algal com-munity structure, biomass, and productivity wasnot being demonstrated (Larkum and Koop 1997;Koop et al. 2001). There were also no effects onrhodolith growth, phytoplankton biomass or pro-duction, fish grazing and reproductive effort, orbioerosion (Koop et al. 2001; Kiene 1997). As ex-pected, N-fixation increased with phosphate en-richment and denitrification increased with am-monium enrichment (Koop et al. 2001). Increasedrates of denitrification may be one reason why nu-trient concentrations did not build up during the2-yr enrichment.

The only studies that claimed major significanteffects of enrichment are those on the growth and


reproductive biology of various species of reef cor-al. It is important to examine critically this body ofwork because it is being cited as evidence that nu-trients have effects on coral and reef health (e.g.,Koop et al. 2001). It is apparent that in spite ofthe investigators’ best efforts, the results are weakand contradictory. Acropora palifera grew 30% morein the 1P and 1N1P treatments, and 10% to 20%less in the 1N treatment during the high level en-richment year (Steven and Broadbent 1997). Sty-lophora pistillata had 25% higher extension ratesand calcification rates in the 1N1P treatment,similar or higher extension rates in the 1N and1P treatments and lower calcification rates for oneof three growth intervals in the 1P treatment com-pared to controls during the lower enrichment pe-riod but none of the results were statistically sig-nificant because of high variability between coralclones and between microatolls within treatment(Hoegh-Guldberg et al. 1997). A third set of inves-tigators found no effect of ammonium enrichmenton linear growth of S. pistillata or A. aspera, andvariable effect on A. longicyathus depending on theseason, but no net effect on an annual basis (Koopet al. 2001). No attempt is made in the summarypaper (Koop et al. 2001) to reconcile or explainthe inconsistencies in the results yet their overallconclusion is that nutrient enrichment reducescoral growth.

In the study of coral reproduction, colonies ofA. longicyathus and A. aspera were transplanted intoeach microatoll and examined for various mea-sures of reproductive effort (Ward and Harrison2000). The authors also sampled colonies of thesecond species where they occurred naturally innine of the microatolls and of the donor coloniesin the lagoon from which the transplanted pieceswere taken. The misused orthogonal statisticalanalyses reported in the paper and the text de-scribing the results do not appear to agree with thebar graphs in which the data are presented. A di-rect comparison of A. longicyathus in the varioustreatments with their donor colonies (their Figs. 8–11) shows that the control, 1N and 1P corals hadvalues similar to or higher than those of their do-nor colonies and that only the 1N1P corals hadlower values compared to donor colonies, castingdoubt on the authors’ interpretation of the biolog-ical significance of the experimental results. Nat-urally occurring colonies of A. aspera inside the mi-croatolls did not exhibit the responses ascribed tothe experimentally transplanted corals of the samespecies. Interannual variation for controls was asgreat or greater as was reported for treatment dif-ferences, and their reported statistically significanttreatment effects were not reproducible from yearto year. Some of the reported significant negative

effects were for November 1993 after only 2 mo ofthe lower level of enrichment with no differencefor November 1994 after a whole year of enrich-ment, suggesting that the differences between cor-als in the various microatolls were not the result ofthe nutrient treatment. Inspection of the data doesnot lead me to conclude that the claimed nutrienteffects on fecundity were real or ecologically sig-nificant. Most of the statistical significance was theresult of underperformance of corals in the 1N1Ptreatment.

An equally viable explanation is that the envi-ronmental conditions in the microatolls assignedto the 1N1P treatment were unsuitable for thecorals transplanted there. Two of these microatollswere located towards the rear of the lagoon andlikely had different circulation and environmentalconditions from the rest. That corals had to betransplanted into the microatolls for these experi-ments suggests that the microatolls were not aplace where corals do well naturally (only 5% to18% natural coral cover), and A. longicyanthus wasnot one of the species reported to occur in them(Koop et al. 2001). Studies comparing reproduc-tive activity of two species of Porites and several spe-cies of Agariciidae in upwelling and non-upwellingzones off the coast of Panama found similar pat-terns of reproduction at the two types of sites(Glynn et al. 1994, 1996), showing that corals livingnaturally under recurring elevated nutrient con-ditions carry out normal gametogenic activity. Sim-ilar flaws exist in the work on nutrient effects oncoral fertilization, larval settlement, and post-settle-ment survivorship reported in Ward and Harrison(1997).

The ENCORE results unfortunately do not con-stitute a solid basis from which to judge the roleof nutrient enrichment on coral health or coralreef decline. There may have been confoundingexperimental factors such as a naturally high back-ground level of nitrate, differences between mi-croatolls in circulation due to their location withinthe One Tree Island lagoon (Larkum and Steven1994; Kiene 1997) as well as large differences inthe sizes and volumes of the microatolls used foreach treatment (73 range in microatoll volume,and 63 range in microatoll area; Koop et al. 2001).I conclude that neither ENCORE or the otherstudies cited above demonstrated that there aremajor biologically or ecologically significant effectsof nutrient enrichment on coral health at the lev-els of loading reported for reef areas suspected ofnutrification. Direct effects of nutrient enrichmenton coral physiology are unlikely to be a widespreadcontributor to coral reef decline.

752 A. M. Szmant

Indirect Effects on Reef Community Structure

Caging or some other way of excluding herbi-vores is necessary to study nutrient effects on algalcommunities and coral-algal competition giventhat herbivory on reefs can be so intense that theeffects of nutrient enrichment on algal growth maynot be measurable unless grazing is reduced. TheENCORE experiment did not include experimen-tal manipulation of grazing. Earlier enrichment ex-periments also did not use cages; results showedthat community productivity increased (accompa-nied by a reduction in community calcification),but that no changes in algal or coral communitystructure were obvious after one year of daily en-richment (Kinsey and Domm 1974; Borowitzka etal. 1978; Kinsey and Davies 1979). The study byHatcher and Larkum (1983) using a cage and en-richment design showed that for the outer slope,nutrients could influence algal turf biomass andproductivity but only if herbivores were excluded,and that in the lagoon neither nutrient availabilityor herbivory rates explained seasonal patterns ofalgal abundance.

Miller et al. (1999) used cages and partial cagesin the Florida Keys, with and without nutrient en-richment, to examine responses of the algal com-munities on artificial plates made of quarried lime-stone. The only effect of enrichment was a slightlyhigher percent cover by cyanobacteria (blue greenalgae), but only within the caged treatments. Theyfound that the strongest experimental effect wasdue to excluding large herbivores, and that enrich-ment-herbivory interactions did not result in dom-inance by macroalgae or CCA as predicted by theLittler and Littler (1984) relative dominance mod-el (Fig. 2a). Thacker et al. (2001) examined algalcommunity structure on natural substrate on aGuamanian reef after 4 mo of caging and enrich-ment. They found an effect of enrichment on per-cent cover (but not biomass) of the brown algaDictyota in caged and uncaged treatments (but notpartial caged ones) as well as small non-significantincreases in Halimeda biomass with enrichment inall treatments, but there was no effect of enrich-ment on total macroalgal cover or biomass. Theirmajor result was a shift in species dominance fromunpalatable species of cyanobacteria in uncagedtreatments to palatable species of cyanobacteriaand Padina in caged treatments. These results donot agree with the Littler and Littler model pre-dictions either. The Littler and Littler model wasgenerally upheld by the experimental results of an-other caging-enrichment factorial experiment con-ducted with artificial PVC substrates on a pristineHawaiian reef located within a no-take marine pre-serve (Smith et al. 2001). These investigators

found the greatest increase in total algal biomass,made up mostly of fleshy and calcareous forms,with combined enrichment and caging. Calcareousalgae increased most with enrichment in the pres-ence of herbivory (uncaged), suggesting that theywere nutrient-limited on that reef under ambientnutrient conditions, and outcompeted by fleshy al-gae in the absence of herbivory. These experi-ments demonstrate that in the presence of normalgrazing, moderate nutrient enrichment results inlittle change to algal community structure or bio-mass, but that when herbivory is reduced with orwithout nutrient enrichment, algal biomass may in-crease and there may be a shift to increased coverand biomass of fleshy algae. None of these exper-iments addressed the issue of coral-algal competi-tion and how it is influenced by nutrient enrich-ment.

McCook (1999) provides a thoughtful review ofthe processes by which macroalgal growth could bestimulated by nutrient enrichment to outcompetecorals, as well as several indirect ways in which thesame outcome could occur. He concludes thatthere is at best limited evidence for direct nutrient-mediated shifts, but does not rule out that nutri-ents could be indirectly contributing to communitystructure shifts, especially when coupled with re-duced herbivory, loss of topographic complexity bystorms, or other disturbances such as increasedsedimentation. Limitations to linking shifts in cor-al-algal dominance to nutrient enrichment includelack of good time series for the algal communitiesthemselves (before and after enrichment), as wellas experimental evidence that excludes other fac-tors (McCook and Price 1997; McCook et al.1997). Most studies that have examined coral-algalcompetition or reported algal overgrowth of coralshave not included nutrient enrichment as a con-tributing factor. Coral overgrowth by algae was re-ported by Lewis (1986) who used large mesh cor-rals to exclude herbivorous fishes from an area ofreef flat on Carrie Bow Cay, Belize, for a period of8 wk. She found shifts in species composition, in-creases in macroalgae abundance, and some over-growth of corals by algae, but also reported thatthe fishes grazed down the excess algae withinhours of the cages being removed. There is no in-dication that nutrients were elevated on this reefthat is about 30 km from land. In an experimentconducted on GBR reefs that differed in exposureto terrestrial nutrients, McCook (2001) manipulat-ed coral-algal interactions by artificially woundingcorals or removing turf algae. He found that coralscompetitively excluded the turf algae even on thereef closest to terrestrial influences, suggesting thatthe general belief that algae outcompete coralswhen exposed to elevated nutrients may not be


well founded. Both the functional type of alga(e.g., turf versus fleshy) and the coral species willdetermine the outcome of coral-algal interactions,and grazing pressure may be more important thannutrient enrichment in modulating these interac-tions. McCook et al. (2001) concluded that whilethere was ample evidence that corals and algae docompete, the direction of the outcome was highlydependent on the life-history characteristics of thespecific corals and algae involved. Nutrients alonedo not determine the outcome of the competitiveinteraction.

How Geographically Widespread is the Evidencefor Nutrient Enrichment Effects on Coral Reefs?

WESTERN PACIFIC AND SOUTHEAST ASIA

This region includes the center of biodiversity ofIndo-Pacific coral reefs. Because many of the reefsin this region are fringing reefs or near major land-masses, they are at high risk of being affected bythe whole gamut of human activities. There are fewstudies of nutrient conditions on reefs for this re-gion. An issue of Marine Pollution Bulletin (1994:1)dedicated to problems faced by Pacific coral reefsprovides some insight into the role of nutrientsand eutrophication in the degradation of thosereefs, but include few data on nutrients. While eu-trophication was among the factors listed by severalof the authors as being of localized concern, it wasof far less importance to most reefs than overfish-ing and sedimentation.

Hutchings et al. (1994) expressed concern oversewage effluent from pig farms entering FrenchPolynesian lagoons, but do not provide any nutri-ent data or evidence that it is causing a problem.They do cite several studies showing that sedimen-tation from runoff was affecting or killing near-shore reefs. The areas receiving increased sedi-ments and nutrients are also areas experiencinghigh levels of overfishing. Increased algal growthin these areas could be due to nutrient inputs oc-curring together with sedimentation and overfish-ing stresses. Goldman (1994) attributes most of thecoral reef problems on Yap to overfishing, and stat-ed that water quality problems were limited to themain harbor of Colonia. Zann (1994) reviewed theproblems on Western Samoa, Fiji, and Tonga. Henoted overfishing and destructive fishing practiceswere a concern in all areas, as well as poor land-development policies including destruction of wet-lands and mangroves. Sediments are filling in la-goons and killing nearshore reefs near major de-velopments. Sediments and nutrients are causingexpansion of mangroves and seagrass beds into ar-eas formerly characterized by corals. Water qualityin lagoons and major harbors has deteriorated, as

evidenced by higher chlorophyll and turbidity.These effects appear to be limited to the more de-veloped lagoons and harbors, and in the outer is-lands, eutrophication effects are limited to within100–500 m of a village or resort. Over the past 30yr, human population has doubled and fisheriesproduction tripled, so any effect of just nutrientsis difficult to separate from all the other anthro-pogenic activities.

The decline of Philippine coral reefs is also at-tributed to sedimentation stress from land devel-opment and destructive fishing practices, but nat-ural events such as typhoons and volcanic erup-tions have also taken their toll (Gomez et al. 1994).Sewage-associated nutrient effects appear to belimited to sheltered bays with restricted circulation.Gomez et al. state that the most significant causesof decline are coral extraction, dynamite and muroami fishing, and Malthusian overfishing. On near-by Papua New Guinea (PNG), overfishing is less ofa problem because local people do not depend onseafood as a major component of their diet, butdestructive land practices for logging and agricul-ture are a serious problem since most PNG reefsare fringing reefs (Huber 1994). Huber states thatwhile blast-fishing is considered by some as themost important threat to PNG reefs, in his opin-ion, sedimentation is the most extensive threat. Healso states that eutrophication is only of local im-portance near urban centers and large villages.

A clear case can be made for eutrophication be-ing one of several major causes for coral reef deg-radation in the Hong Kong area (Morton 1994).Coral mining was extensive before World War IIand likely responsible for much loss of reef in thearea. Coral mining stopped after the war, and reefsmight have had a chance to recover, but extensiveland development, dredging, and pollution of ma-jor Hong Kong harbors have prevented that. It isreasonable to expect that coral reefs near highlydeveloped areas of the China mainland have suf-fered a similar fate, but no literature was found.

Sewage discharge into a well-flushed channel inKoror Harbor, Palau, had no harmful effect on cor-al cover or diversity when re-surveyed 10 years afterthe sewage pipe was installed (Birkeland et al.1993).

Eutrophication (including nutrification) ap-pears to be a problem around major human de-velopments in the Indo-Pacific region, especiallylarge harbors (reduced circulation) with large set-tlements, but nutrient enrichment does not appearto be a widespread problem for the reefs in theregion, especially when compared with sedimen-tation, overfishing, and coral bleaching in recentyears.

754 A. M. Szmant

GREAT BARRIER REEF

Eutrophication is feared to be the cause of wide-spread decline of GBR coral reefs (Bell 1992; Belland Elimetri 1995), and proponents of this viewbase it on the perception that water column chlo-rophyll levels and algal cover on coral reefs haveincreased especially in inshore areas. No data todocument increases in algal cover or to show directcause and effect are presented in papers makingthese claims (see McCook and Price 1997; McCooket al. 1997), and the concept of widespread declinehas also been questioned (Done 1999). Furnas etal. (1995, 1997) have constructed nutrient budgetsfor major cross-shelf sections of the GBR, and es-timate riverine and sewage discharges into the areaas providing about 13% of the N demand and 20%of the P demand for water column primary pro-duction (requirements of benthic production aremissing from their budget). Rates of N loss by de-nitrification are estimated to be comparable tothose of riverine N input. Most of the nutrient de-mand appears to be supplied by resuspension andrecycling. A major unknown in their budget is theexchange of nutrients at the oceanic end of thesection (Furnas et al. 1997). If there is a net lossof nutrients from the system via lateral exchangeof water at the shelf break (e.g., offshore flux dur-ing storms greater than onshore flux due to up-welling), then nutrients would not be building upenough on the GBR shelf to cause eutrophication.There is no evidence that GBR sediments are be-coming enriched over time as happened in Kane-ohe Bay prior to outfall diversion (Smith et al.1981; Furnas et al. 1995; references cited in Furnaset al. 1997). Long-term studies of water columnchlorophyll levels show much interannual variabil-ity, with consistently higher levels inshore, but nolong-term trend of increase (Brodie et al. 1997).While there is considerable concern over the po-tential role nutrient enrichment and eutrophica-tion could have in causing decline of nearshoreGBR coral reefs, especially ones near river mouths,there is no evidence at this time to support anywidespread nutrient effect.

HAWAII

The Kaneohe Bay case is a clear example of nu-trient enrichment having caused coral reef decline,and it involved both increased water column chlo-rophyll concentrations and a large increase in ben-thic algal cover and overgrowth of corals by algae.After diversion of the sewage discharge to an off-shore ocean outfall, the water column of the baygradually regained its former chlorophyll levelsand transparency, substrate cover by Dictyosphaeriadecreased and coral cover increased (Laws 1992).

More recently, Dictyosphaeria cover has increasedon some reefs in the bay, and there is concernabout continued eutrophication. Stimson et al.(2001) found that abundance of this alga is low inthe southern part of the bay where sewage was for-merly discharged, and higher in the central reach-es of the bay. Here, it is inversely correlated withthe abundance of an introduced species of red algathat is a preferred food of herbivores. Where her-bivores are scarce they graze on the reds and Dic-tyosphaeria is more abundant. Where herbivoreabundance is high, they graze on both species, andalgal cover is low. Growth rates of Dictyosphaeria ap-pear at present to be unrelated to water columnnutrient concentrations since this species appearsto obtain most of it nutrients by intercepting dif-fusion from the substrate (Larned and Stimson1996; Stimson and Larned 2000). A sewage outfallin Mamala Bay also caused loss of coral cover with-in 4 km of the outfall (from 60% elsewhere to ,10% near the outfall) until the sewage treatmentwas upgraded and the outfall relocated into deeperwater in 1977 (Grigg 1995). Recovery proceededafter that, but coral cover in the entire bay wasreduced to , 20% by two major typhoons in 1982and 1992. Nutrient levels in the bay measured 15years after diversion are generally low (Table 1)except during rainy and high-wave events, but evenwhere they were elevated near Pearl Harbor theyare within the range of concentrations at whichcorals grew well in the Waikiki Aquarium (Atkin-son et al. 1995; Grigg 1995).

INDIAN OCEAN AND RED SEAKenyan coral reefs have been extensively studied

(McClanahan and Muthiga 1988; McClanahan andObura 1995, 1997; McClanahan et al. 2001). Thereefs are heavily affected by overfishing exceptwhere protected by marine parks, and they havebeen recently affected by bleaching (McClanahanet al. 2001). Sediments coming down the rivers af-fect coral community composition but not neces-sarily diversity (McClanahan and Obura 1997).Overgrazing of the substrate by sea urchins limitscoral recruitment on many reefs; sea urchins areoverabundant because of reduced predation.McClanahan states that sediments and eutrophi-cation are not currently major threats comparedto overfishing. In nearby Tanzania, a study of nu-trients in Zanzibar Town harbor reported veryhigh levels of phosphate (up to 10 mM close to thesewage discharge) with nutrient-enriched water be-ing transported to nearby reefs by tidal flushing (1to 4 mM phosphate maxima; with means of about0.1 to 0.2 mM) (Bjork et al. 1995). These research-ers reported a 60% decrease in CCA cover withproximity to sewage source and by phosphate con-


centrations above 0.2 mM. They also conductedlaboratory and field experiments that showed thatCCA growth rates declined by 50% at concentra-tions above 1.5 mM, but found no effect on growthwhen CCA were exposed to elevated nitrate or am-monium. They gave no information on coral ormacroalgal cover nor status of the areas’ coralreefs.

Nitrate-enriched groundwater is likely contrib-uting to the maintenance of a major shift from cor-al-dominated to algal-dominated community struc-ture that was precipitated by an extreme low tidein 1982 that killed reef flat corals on Reunion Is-land, Indian Ocean (Cuet et al. 1988; Naim 1993).While the groundwater seepage was not the causeof the coral death, and was present before the die-off, the researchers think it is contributing to thepersistence of the algal-dominated state. The po-tential relationship between grazer abundance andalgal dominance is only briefly discussed (Naim1993), but she states that herbivorous fishes aremore abundant and sea urchins less abundant onthe degraded reef compared to nearby non-de-graded reefs. No information is given about thespatial extent of the degraded reef, but from themaps in the papers it appears the effect of the con-taminated ground water in this case is localized.Nitrate-rich groundwater discharge into reef areashas also been reported for Mayotte Island, in theComoro Archipelago, and the lagoon has amongthe highest levels of nitrate, ammonium, and phos-phate reported for high-island lagoons (Vacelet etal. 1999). The status of the coral reef communitiesis not discussed, and it is not clear whether theseelevated nutrient fluxes have affected reef condi-tion. Coral reefs in the Indian Ocean suffered veryhigh coral mortality (ca. 90%) during the 1997–1998 bleaching events (Wilkinson 1998; Mc-Clanahan 2000; Edwards et al. 2001; Lindahl et al.2001; McClanahan et al. 2001), and bleaching-killed coral is quickly colonized by algae (e.g., Lin-dahl et al. 2001; McClanahan et al. 2001). Thereis reason for concern that high nutrient inputsfrom contaminated groundwater seepage could in-terfere with reef recovery here as it has in Re-union.

Nutrient pollution of Aqaba, in the Red Sea,comes from sewage and apatite dust from loadingfertilizer onto cargo ships. These are released intoa fringing reef resulting in elevated levels of phos-phate in reef waters (Walker and Ormond 1982).The affected area has low coral and high algal cov-er compared to reference reefs 10 km away. Walkerand Ormond concluded that poor water qualitycontributed to higher rates of coral death in thepolluted area, but that algae were not the directcause of coral mortality. Rather, algae colonized

the exposed coral skeletons quickly after death,and sediment trapping by the algae both prevent-ed coral recovery and contributed to further coraltissue loss.

CARIBBEAN AND TROPICAL AMERICASThe coral reefs at Discovery Bay, Jamaica are

among the most studied in the Caribbean, and thetime-course of their degradation has been record-ed. Jamaican reefs were characterized by high coralcover and diversity before a 1980 hurricane struckand was followed by the 1983 Diadema die-off(Hughes 1994). Several investigators were able tocarefully document the changes in algal cover andbiomass as grazing pressure was reduced (e.g.,Hughes et al. 1987; Liddell and Ohlhorst 1986;Morrison 1988; Hughes 1994). The devastatingstorm damage to branching reef corals prior to theDiadema die-off was a critical initial event in thedegradation sequence, coupled with pre-existingoverfishing of herbivorous fishes (Hughes 1994;Aronson and Precht 2000). The potential role ofnutrient enrichment in this phase shift was not giv-en much consideration until Lapointe (1997) ar-gued that the mostly top-down cause of reef de-cline reported by Hughes and others for DiscoveryBay reefs ignored the bottom-up contribution ofeutrophication. He provided data on nutrient anal-yses for a day in July 1989 compared to an earliernutrient study in 1980 (D’Elia et al. 1981). He alsopresented C:N:P tissue ratios for reef and grottoalgal species and nutrient-enhanced P-I curves thathe interpreted as evidence that nitrate enrichmentfrom groundwater seepage was the major cause ofincreased algal abundance. Lapointe’s paper wascritiqued by Hughes et al. (1999), who pointed outthat the temporal patterns of shifts in coral-algalcomposition were more consistent with reducedherbivory than with sudden enrichment, and thatthe temporal patterns of reef decline in Jamaicawere similar to those observed elsewhere wherenutrient enrichment was not suspect (e.g., St.Croix, U.S. Virgin Islands, Carpenter 1986; SanBlas, Panama, Shulman and Robertson 1996). Thiscritique was followed by a rebuttal in which La-pointe (1999) re-affirmed his position but addedthat he did not discount a role for reduced her-bivory in the story. This debate was followed byseveral papers that have shown recent large de-creases in algal cover on Discovery Bay reefs co-incident with the return of Diadema to densitiescomparable to those before the die-off (Woodley1999; Aronson and Precht 2000; Edmunds andCarpenter 2001). Reef zones where Diadema havereturned have lost algal cover and appear to beregaining coral cover, while those where Diademahave not returned still have high algal cover and

756 A. M. Szmant

fewer coral recruits (Edmunds and Carpenter2001). This evidence of recovery has occurredwithout any measurable change in grazing fishabundance nor reason to expect reduced anthro-pogenic nutrient inputs (no decreases in humanpopulation, no improvement to wastewater treat-ment, no change in rainfall; Aronson and Precht2000). While Lapointe may be correct with regardto the fact that anthropogenic nutrients are enter-ing the Discovery Bay coastal zone, the weight ofevidence does not suggest that those nutrients hada major role in the phase shift and decline of Dis-covery Bay reefs, since the recovery now evidentlyunderway is happening without any effort to re-duce nutrient loading.

Reef degradation at other Caribbean reef siteshas been documented over a similar time-frame asthe Discovery Bay reefs, but the role of hurricanesin initiating the decline did not occur at thosesites. On San Blas reefs, bleaching in the early1980s followed by the Diadema die-off are thoughtto be the major causes, although the authors ex-pressed concern about the possible role of sedi-mentation and nutrients due to increased defor-estation of coastal mountains (Shulman and Rob-ertson 1996).

Reefs on the Belize barrier reef suffered a majordecline in coral cover between 1986 and 1990, pri-marily due to loss of the staghorn coral Acroporacervicornis, presumably to white band disease(Aronson and Precht 2000), although the sam-pling time-frame provided in the paper cannotrule out that bleaching played a part in the loss.These authors propose that the phase shift fromcoral to algal domination widely observed through-out the Caribbean, requires a loss of coral to openup substrate for algal colonization, and that thishas occurred through major loss of the acroporidcorals to disease, bleaching, and storm damage.They also express a concern about a potential roleof eutrophication, but provide no evidence for itsoccurrence. The lagoon of the remote atoll, Glov-ers Reef, located 30 km offshore of the Belize bar-rier reef, also suffered a major decline in coral cov-er (about 75%) sometime between 1971 and 1996,primarily due to loss of acroporids, but all speciesof corals declined while the cover by fleshy erectbrown algae increased (McClanahan and Muthiga1998). While there is little possibility of local an-thropogenic eutrophication being the cause of thisparticular phase shift, many of the species of brownalgae found in the Glovers lagoon were the sameones claimed by Lapointe (1997) to be indicatorsof nutrification in Discovery Bay.

Hallock et al. (1993) have suggested that Carib-bean-wide coral reef decline is associated with ba-sin-wide eutrophication from destructive land-use

practices, increased deforestation, and contaminat-ed runoff into the semi-enclosed Caribbean Sea. Ifso, local enrichment could be less of a factor thanchronic basinwide elevated nutrient concentra-tions. Williams and Polunin (2001) found a stronginverse correlation between macroalgal cover andherbivorous fish biomass when they surveyed 19reefs within seven broadly distributed sites withinthe Caribbean (Fig. 4), which together with exper-imental work on grazing effects reviewed above,suggests that local herbivory rates are an importantdeterminant of macroalgal cover. They also founda positive correlation between herbivore biomassand cropped turf area. They noted that coral coverwas generally below 25% at most of their sites, like-ly from coral loss due to bleaching during recentyears, thus making most of the substrate availablefor algal colonization. They suggest that evenwhere reefs are not overfished, and herbivorousfishes are abundant, that fishes can only keep 60%of the substrate cropped. As corals lose groundfrom bleaching and disease mortality, more surfacearea is made available for algal colonization thanfishes alone can graze. Diadema abundance wasvery low (less than 0.01 m2) at their sites. The ma-croalgae that dominated at high algal cover siteswere those known to be chemically or structurallydefended against fish grazing (Dictyota, Halimeda,Lobophora), but algae that Diadema readily consumein laboratory and field experiments (Szmant un-published; Szmant and Miller unpublished).

Costa et al. (2000) provide a comparison on nu-trient concentrations and reef community struc-ture for two Brazilian reefs that differ in theamount of human development. Fishing pressureis similar and both are unprotected. Nutrient con-centrations at the more developed site were ex-tremely high compared to those reported for otheranthropogenically influenced sites (Table 1). Ma-croalgal cover was twice as high at the developedsite, coral cover was low at both, and the amountof bare substrate, dead coral, and sediment coverwas twice as high at the less developed site. Whilenutrient enrichment undoubtedly is a major causeof higher macroalgal cover at the developed site asthe authors suggest, nutrient levels at the less de-veloped site are also high, and it seems likely thatthere are factors other than nutrient enrichment,such as sedimentation and grazing, that are con-tributing to the differences in algal cover.

FLORIDA KEYSCoral reefs in the Florida Keys, like those in the

Caribbean region as a whole, have lost much coralcover in the past few decades (Dustan 1977; Dustanand Halas 1987; Porter and Meier 1992), and es-pecially since 1987 when coral bleaching became


Fig. 5. Sediment nitrogen and phosphorus concentrationsalong nine inshore to offshore transects in the northern andmiddle regions of the Florida Keys, sampled in spring–summer1996. Upper panel) Map of South Florida and Florida ReefTract showing the locations of the nine transects. The transectsare designated by the names of major charted offshore towersor navigation markers on offshore bank reefs, except for LKVwhich is named after the Long Key Viaduct in the Middle Keys.Middle panel) Total nitrogen content of sediment samples.Lower panel) Total phosphorus content of sediment samples.Two to five sediment cores or grab samples were collected fromeach station. Stations 1 to 3 along each transect were inshoreof Hawks Channel; stations 4 and 5 were on patch reefs onWhite Banks; station 6 was from the shallow fore reefs (10 mdepth) of the offshore bank reefs; KWC (Keys Wide Cruise)samples were from the deeper fore reefs (20 m depth) of theoffshore bank reefs. See Szmant and Forrester (1996) for detailsof sample collection and analysis.

an almost annual event. Because of the rapid ur-ban and agricultural development of South Floridasince the 1960s, many have been quick to blamewater quality degradation and nutrient enrichmentfor the loss of coral, implicating algal overgrowthof the corals as the cause of coral loss (e.g., Ward1990; Torrance 1991; Hallock et al. 1993; Lapointeand Clark 1992; Lapointe and Matzie 1996). TheU.S. Environmental Protection Agency (1992) hascatalogued the various types and sources of an-thropogenic nutrient inputs to the Florida Keys.There is no doubt that the porous limestone of theFlorida Keys allows sewage nutrients from septictanks, cesspools, and shallow injection wells to seepinto canal waters, and several studies have reportedhigher nutrient concentrations and other indica-tors of pollution in canal and inshore waters (La-pointe and Clark 1992; Paul et al. 1995; Lapointeand Matzie 1996; Szmant and Forrester 1996).Florida reefs are separated from inshore waters byHawk Channel, a deeper channel that runs thelength of the Florida reef tract 1–3 km from shore.It serves as a partial hydrographic barrier betweeninshore and offshore waters of the Florida reeftract lagoon (Pitts 1994; Smith 1994), and Szmantand Forrester (1996) found that offshore watershad significantly lower nutrient concentrationsthan inshore waters. The question is whether an-thropogenic nutrients are reaching Florida reefs atrates that can alter reef community structure. Oneapproach to addressing this question is to examinepatterns of nutrients in the sediments, since sedi-ment nutrient pools reflect long-term nutrient dy-namics, especially the balance between input andexport (Laws 1992; Fig. 3). Sediments in basinsand lagoonal areas become nutrient-enrichedwhen nutrient additions are sustained as was ob-served in Kaneohe Bay.

Szmant and Forrester (1996) found inshore sed-iments to be relatively enriched in N compared tomore offshore sediments, but that both inshoreand reef sediments had lower N concentrationsthan sediments from other reef sites consideredpristine. Offshore sediments tended to be moreenriched with P than inshore sediments but stilllow in comparison with reefs sediments from theBahamas and St. Croix, U.S. Virgin Islands. Re-peated sampling of the Florida transects in 1996and again in 1998 after Hurricane Mitch found nochange in nutrients from the levels measured in1990 and 1991 (Fig. 5; Szmant unpublished data).Hanisak and Siemon (2000) examined the C:N:Pratios of a large number of macroalgal samples col-lected from 12 inshore-offshore transects through-out the Florida Keys as an indicator of nutrientavailability to the plants. They found no pockets ofnutrient enrichment, but found a similar trend of

758 A. M. Szmant

higher tissue N/lower P content in algae collectedfrom inshore sites compared to offshore ones asSzmant and Forrester (1996) found in their sedi-ment samples. Szmant and Forrester (1996) sug-gested that upwelling could be an importantsource of nutrients, especially of phosphate, to off-shore Florida reefs, since major upwelling eventshave been documented for the Florida Keys (Smith1982; Lee et al. 1992, 1994). Leichter and Miller(1999) have shown upwelling events to be morefrequent during the summer, when Florida reef al-gae achieve higher cover and biomass (Lirman andBiber 2000; Szmant unpublished data).

There are no published historical data on algalcover and biomass on Florida reefs to documenttemporal trends in algal abundance, and none ofthe studies reporting coral loss include data on al-gal cover, or show that increased algal cover pre-ceded coral loss or caused the loss of coral. Porterand Meier (1992) report a high algal cover of13.8% at a station where Diadema abundance waszero, and only 4.2% at the same station when Dia-dema abundance increased to 0.4 m22. These valuesare low compared to other surveys that show algalcover to be generally much higher (70% to 80%cover) on Florida reefs (Chiappone 1996). Chiap-pone (1996) found the highest algal cover and thelowest coral cover on offshore reefs compared tomore nearshore patch reefs, and this is contrary tothe pattern one would predict if land-based nutri-ents were responsible for promoting algal abun-dance, but it could indicate that upwelling-sup-plied P is contributing to greater algal cover off-shore. Miller et al. (2000) found lower adult coralcover and coral recruitment on offshore reefs ofthe northern reef tract than on patch reefs, in spiteof higher temperature stress, nutrient concentra-tions and sediment resuspension closer to shore.Ginsburg et al. (2002) surveyed coral cover onshallow patch reefs throughout the Keys and foundno correlation between recent partial mortalityand proximity to urban centers. There are no datathat show a clear direct correlation between pre-sent day water quality conditions and coral healththat would explain general patterns of decline forFlorida reefs. The general patterns of decline aremore consistent with being due to regional bleach-ing stress.

An Integrated Conceptual Model for Productivity,Nutrient Dynamics, and Trophic Dynamics

INTERACTIONS ON CORAL REEFS

It is clear that nutrients are one of many factorsaffecting coral reef community structure and func-tion. While there is evidence that nutrient enrich-ment can and has affected coral reefs, this effect

appears to have been mostly localized. An under-standing of how and when nutrient enrichmentwill contribute to coral reef decline requires con-sideration of all of the mechanisms involved in nu-trient dynamics within coral reef ecosystems. If nu-trient enrichment is going to affect coral reef com-munity structure, it will most likely occur by alter-ing the productivity of certain algal groups. Thepatterns of productivity and normal fate of primaryproduction on coral reefs must be considered.

Coral reefs are often described as productive, di-verse, and complex ecosystems because of theirhigh rates of gross production as well as the largenumbers and diverse types of animals that dwellon them, yet at the same time recognized to havevalues of net excess production close to zero(Odum and Odum 1955; Lewis 1977; Kinsey 1985;Crossland et al. 1991; Hatcher 1997). In otherwords, reef heterotrophs consume most of the al-gal primary production on a daily basis (ratio of24 h photosynthesis to 24 h respiration ø 1; Lewis1977; Smith 1983; Kinsey 1985). It is impossible tomeasure community metabolism for entire coralreefs because of their large size, and hydrographicand spatial complexity, and most measurementshave been made on either reef flats or lagoons,where water flow is more constrained. It is recog-nized that some reef zones are more productivethan others because of their biotic composition orenvironmental conditions. Investigators have takenthis into account in generating ecosystem-wide es-timates of metabolism (Kinsey 1985; Johnson et al.1995), based on the premise that coral reefs arefunctionally integrated ecosystems with physical orbiological transport and exchange of materialsamong the various reef zones (Szmant-Froelich1983; Hatcher 1997). Kinsey (1985) proposed thatcoral reef flats have a modal standard performanceof gross production of 7 6 1 g C m22 d21, and P/R of 1.0 6 0.1 that is independent of species com-position. Pichon (1997) refuted this based on datafrom a diverse set of reefs from seven geographicregions. Interestingly, the reported values of com-munity gross production vary 20-fold over a rangefrom about 1 to 19 g C m22 d21 (Lewis 1977; Rog-ers 1979; Smith 1983; Kinsey 1985; Gattuso et al.1993 and references therein; Kraines et al. 1996;Pichon 1997; Gattuso et al. 1998). This broadrange in area-specific gross production can be ex-plained by the amount of substrate area availablefor autotrophs to grow on, which is a factor of boththe proportion of the substrate occupied by non-photosynthetic organisms, and the amount ofstructural complexity per planar area: the higherthe complexity the more surface area for algae togrow on (Pichon 1997; Szmant 1997); the sizes andtypes of dominant primary producers and their


biomass-specific rates of production (Hatcher1988, 1990; Steneck and Dethier 1994); physical-chemical conditions (e.g., nutrient fluxes, circula-tion and turbulence, light) that affect biomass spe-cific rates of production; or a combination of theabove, since they are not mutually exclusive.

For the P/R of coral reefs to remain close to oneregardless of absolute level of gross production,reefs with higher production must have a greaterrespiratory demand, i.e., a greater biomass of re-spiring organisms per unit area. As long as hetero-trophs consume most of the algal production andpass it up the food web (e.g., grazers feeding onalgae, microbes using mucus excreted by autotro-phic corals, detrital food webs based on algal frag-ments; Szmant 1997), algal biomass cannot in-crease on a reef.

When a reef has a high algal standing crop, itcan be inferred that at some point in time, algalproduction has exceeded the capacity of the het-erotrophic community to consume it. This canhappen if the rates of production of existing algalgroups increases (i.e., same species of algae, butgreater productivity due to more nutrients if nu-trient limited, more turbulence breaks down dif-fusion barriers, less turbid/more light); if moreproductive algal groups replace less productiveones (shifts in algal species composition: see Ste-neck and Dethier 1994); if more surface area be-comes available for algae to occupy (after storms,bleaching events or coral disease, exposed coralskeleton becomes available for algal colonization);if loss of grazers and other consumers (overfishing,Diadema die-off); or if shifts in algal compositiontowards species that are not palatable. These alter-natives are not mutually exclusive and can be syn-ergistic.

The question now is what potential role does nu-trient availability play in determining the gross eco-system production of a coral reef via any of theabove or other mechanisms? Nutrient recycling isaccepted as being the source of most of the nutri-ent demand for gross production (Smith 1983;Szmant-Froelich 1983; D’Elia 1988; Furnas et al.1995) but if all reef ecosystems are equally efficientat recycling, recycling cannot explain the largerange of gross production among reefs. The reefsystems with the highest reported rates of grossand net production are either those in upwellingareas (Smith 1983; Pauley 1997) or near high is-lands (Pichon 1997; Gattuso et al. 1998). Miocheand Cuet (1999) report that a nutrified reef hadhigher levels of gross production and consumptionthan a nearby unpolluted reef. Based on first prin-ciples and sparse data, it is reasonable to suggestthat higher nutrient fluxes will allow for greaterrates of gross production on coral reefs.

The simple conceptual model proposed here isbased on this assumption, that upper limits of grossproduction and levels of net production depend atleast in part on nutrient flux, and that there is anidealized linear relationship between primary pro-duction and nutrient supply rate. If we accept thaton pristine reefs the ratio of production-to-con-sumption will hover around one over a broadrange of rates of gross production as has beenmore or less empirically observed, then theamount of gross production transferred to the cor-al reef food web via herbivory will also increaselinearly with nutrient supply, up to a point deter-mined by the grazing capacity of the consumers,after which algae can overgrow the substrate (andcorals) and coral reef degradation begins (Fig. 6a).If the starting point is one of low algal biomass (thegeneral vision of a pristine coral reef), as long asmost of daily algal production is consumed, ma-croalgae will remain in low cover and biomass, andcorals, coralline algae, and highly grazed turfs willdominate the substrate if conditions are otherwisesuitable for these organisms (e.g., substrate typeand depth, temperature, light, circulation). Thissituation is represented in the left half of Fig. 6a.At some level of nutrient flux (5 Nk) the amountof production will be greater than what the her-bivore and detritivore communities can consumebecause their populations and biomass will ulti-mately be limited by factors other than food avail-ability, such as predation, shelter, or recruitmentdynamics. Above this nutrient flux, algal biomassand cover will gradually increase and coral coverdecrease by interactions as discussed previously(right side of Fig. 6a). The amount of productivitytransferred to the food web may decrease if non-palatable species begin to dominate over palatablespecies. The nutrient flux at which shifts in coralreef community structure become evident, Nk, willbe highly dependent on the grazer community’sability to consume the production supported bythe level of nutrient flux. The level of nutrient fluxat which coral reef decline begins can be viewedas a threshold level. Several investigators have pro-posed levels of nutrients (in units of concentration,not flux) above which coral reefs become degrad-ed (1 mM ammonium plus nitrate, 0.1 mM phos-phate; Bell 1992; Lapointe 1997), but the concep-tual threshold proposed here is not a fixed con-centration. Rather it is a range of fluxes that varydepending on the ability of the reef heterotrophsto consume the production. If conditions changesuch that greater grazing pressure can be accom-modated (heavy recruitment of herbivores, in-creased shelter for reef dwellers), then the nutri-ent flux needed to cause degradation would shiftupwards and corals will thrive at higher nutrient

760 A. M. Szmant

Fig. 7. Diagrammatic summary of sequence of events thatbegin with loss of coral cover and reef structural complexity dueto events such as bleaching or storm damage, with or withoutloss of herbivory, and can result in eventual dominance of thesubstrate by chemically or structurally defended macroalgae.Key to the community structure change in the right panel isthat grazing pressure per unit area of reef is lower because ofmore surface area available for algal growth, while there is lesshabitat available for herbivore shelter; in the Caribbean, thereis also the loss of an invertebrate herbivore that was less respon-sive to algal defenses than herbivorous fishes.

Fig. 6. Conceptual model of nutrient effects on coral reefcommunity structure mediated through interactions betweengross production and total community consumption includingherbivory. A) Representation of relative nutrient tolerance ofunfished, pristine coral reefs. This scenario represents the rangeof nutrient fluxes under which coral reefs would be able toform. Nk is the natural nutrient flux at which primary produc-tion would exceed the capacity of a healthy coral reef commu-nity to use the production, leading to a build-up of excess pro-duction in the form of algal biomass. Past that relative level ofnutrient flux, coral cover would decrease, algal cover increase,and at some level reef-building would cease. This model is con-ceptually similar to that of Birkeland (1988) shown in Fig. 2b.Such a model can explain changes in reef productivity andstructure associated with increasing latitude or upwelling zoneswhere nutrient supplies are higher. B) Representation of hownutrient tolerance and productivity of a reef could increase withincreased consumption, in this case increased herbivory. Notethat Nk moves to the right. Factors that could lead to increasedNk include increased substrate for primary producers coupledwith increased shelter for herbivores and other reef consumers.Increasing topographic complexity over time could lead to bothsuch changes. C) Model scenario for how coral reef responseto nutrient flux can be affected by loss of herbivory. This willresult in less production being passed on to the coral reef foodweb, and a shift from coral to algal dominance even at low nu-trient fluxes. Notice Nk moves to the left.

levels than before (Fig. 6b). If grazing pressure de-creases or if substrate available for primary pro-ducers increases faster than the size of the grazercommunity (e.g., overfishing of herbivores or Dia-dema die-off for the former; coral killed by bleach-ing, disease or storms for the latter), then shiftsfrom coral to algal dominance will occur even atlow nutrient fluxes (Fig. 6c). This last scenario canexplain the observed shifts in coral-algal abun-dance that have been observed so widely in theCaribbean even in remote areas where nutrient en-richment is highly unlikely.

Two scenarios of the conceptual model that arenot visually represented in Fig. 6 are the loss of livecoral due to extraneous causes, and effects of rel-ative algal palatability on shifts in algal communitystructure (Fig. 7). Williams et al. (2001) experi-mentally showed the positive relationship betweencoral cover and grazing pressure per area, and howa reduction in the percent substrate available toalgae caused a reduction in algal cover on the re-maining substrate. Many reef algae are chemicallyor structurally defended against fish grazers (Hay1997), and the species of macroalgae now domi-nating many Caribbean reefs belong to thosegroups (Halimeda, Dictyota, Lobophora). Many fisheswill graze on very small plants of these species(when they are in minute turf form) before theyhave a chance to build up chemical or structuraldefenses, but not once they get bigger. When sub-


strate available to algae is low (i.e., when coral cov-er is high), high grazing pressure on limited sub-strate keeps these species from growing to a de-fended size. As substrate for algal colonization in-creases when corals die from storm damage orbleaching, or as grazing pressure decreases due tooverfishing or herbivore die-off, grazing pressureper area is lower (Williams et al. 2001), and someof the non-palatable plants will reach a larger, non-grazed size. The non-palatable species can gradu-ally

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