Coral Reefs (1999) 18 : 357}367
( Springer-Verlag 1999
REV I EW
L. J. McCook
Macroalgae, nutrients and phase shifts on coral reefs: scientific issues and management consequences for the Great Barrier Reef
Accepted: 13 August 1999
Abstract Degradation of coral reefs often involves a &&phase shift'' from abundant coral to abundant macroalgae. This paper critically reviews the roles of nutrient increases in such phase shifts. I conclude that nutrient overloads can contribute to reef degradation, but that they are unlikely to lead to phase shifts simply by enhancing algal growth rates and hence allowing overgrowth of corals, unless herbivory is unusually or arti"cially low. Concentrations of dissolved inorganic nutrients are poor indicators of reef status, and the concept of a simple threshold concentration that indicates eutrophication has little validity. I discuss the signi"cance and consequences of these assessments for reef management, focusing on the Great Barrier Reef, and conclude with some speci"c recommendations, including protection of herbivorous "shes, minimisation of terrestrial runo!, and protection of coastal reefs. Key words Macroalgae ' Phase shifts ' Nutrients ' Herbivory ' Degradation ' Overgrowth
Introduction Benthic macroalgae play important roles on both healthy and degraded coral reefs, and the abundance and composition of reef macroalgae are critical to the reefs' ecological, environmental, aesthetic and socioeconomic value. On &&healthy'' reefs, tur"ng and calci"ed algae are the major contributors to reef primary production and nitrogen "xation, make important contributions to calci"cation and reef building, and often occupy large proportions of space (e.g. Adey 1998).
L.J. McCook Australian Institute of Marine Science and CRC: Reef Research, PMB 3, Townsville M.C., Qld, 4810, Australia e-mail:
[email protected]
Degrading reefs often undergo a &&phase shift'' in which the abundance of corals declines, and the composition of macroalgae changes, with an increase in abundance of larger, #eshy (corticated) macroalgae (e.g. Done 1992; Hughes 1994a). These algal-dominated reefs usually have lower "sh stocks, less tourism appeal and coral biodiversity, and there is widespread scienti"c, management and public concern that such apparent degradation is the result of human impact. There are numerous examples of such phase shifts (e.g. Smith et al. 1981; Hatcher et al. 1989; Done 1992; Hughes 1994a; Genin et al. 1995; Lapointe 1997), with two factors causing particular concern: (1) reduction in herbivory, due to over-"shing and (2) eutrophication, or increases in nutrient and/or sediment inputs due to human land-use. On the Great Barrier Reef (GBR) in particular, there is concern that abundant macroalgae on inshore fringing reefs indicates degradation due to anthropogenic increases in terrestrial inputs of sediments and nutrients (Bell and Elmetri 1995, reviewed in McCook and Price 1997a, b; Wachenfeld 1998). The distribution and abundance of benthic marine species, including algae, are principally in#uenced by "ve inter-related sets of factors: resource availability (e.g. light, nutrients, substrate); &&supply-side'' (sensu Lewin 1986) factors (fecundity, dispersal, settlement and recruitment); physical stress gradients and disturbance regimes (e.g. depth, wave exposure and cyclones, temperature, freshwater, sediment deposition); species interactions (especially competition and herbivory); and the historical e!ects of and interactions among these factors. For coral reef macroalgae, attention has focused on two factors: water quality, particularly the nutrients nitrogen and phosphorus; and herbivory (e.g. McCook and Price 1997b for GBR; Littler and Littler 1984; Genin et al. 1995; Lapointe 1997; Szmant 1997; Hughes et al. in press). This focus re#ects concerns about eutrophication and over"shing, but to some extent has precluded consideration of other factors.
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This paper aims to provide a critical perspective on the implications for reef management of current scienti"c information about coral reef algal ecology. Using the Great Barrier Reef as a case study, the paper focuses on the following, inter-related questions: 1. What factors cause abundant macroalgae on coral reefs? Does increased supply or concentration of nutrients lead to algal dominance and if so: Is this simply due to nutrient enhancement of algal growth, with consequent overgrowth of corals? Or: What alternative mechanisms can lead to algal dominance, based on consideration of a more complete range of ecological factors. 2. What do the answers to these questions mean in terms of management of the GBR? Does it matter how nutrients act, in terms of reef science or management? Are there generally applicable &&threshold'' concentrations of nutrients that indicate reef degradation? What speci"c recommendations can be made, based on the answers to these questions? As a management-oriented perspective, the discussion explicitly includes my own interpretations of both scienti"c results and their implications for management. The term macroalgae here refers to all benthic algae whose individuals are visible to the naked eye, thus including &&EACs'' (epilithic algal communities sensu Hatcher 1981), "lamentous, tur"ng, blue-green and crustose algae as well as the larger, frondose groups.
Does increased supply or concentration of nutrients lead to algal dominance: mechanisms for nutrient effects on algal abundance and phase-shifts There is a widespread view that oversupply of nutrients or sediments will lead directly to macroalgal overgrowth of corals (e.g. Bell 1992 for GBR; Lapointe 1997; Adey 1998) through enhanced competitive ability of the macroalgae. Whilst simple and intuitive, this view is poorly supported by empirical data, and does not stand up to critical analysis. There are at least six alternatives to this &&direct e!ects on algal competition with corals'' paradigm: herbivore declines; reductions in topographic and trophodynamic complexity; indirect e!ects of sediments or nutrients on macroalgae: inhibition of competitors or herbivores; &&supply-side'' e!ects; combined e!ects of natural disturbance and eutrophication; interactions and synergistic e!ects. I argue that the available data and anecdotal reports provide convincing evidence that nutrients have important roles in algal ecology and coral-algal phase shifts, but provide little indication of what those roles are. In particular, I suggest that nutrient increases alone are unlikely to tip the balance of competition between
macroalgae and established corals, and that this view provides a risky basis for management. The &&direct e!ects of nutrients on algae'' paradigm
Although the simplest mechanism considered, this process involves three distinct steps (Fig. 1): (1) increased nutrients (and/or sediments) are assumed to lead to increased algal growth (i.e. rates of growth or production: biomass per unit time); (2) increased growth is assumed to lead to an increase in standing crop (i.e. biomass per unit area); (3) increased biomass is then assumed to lead to increased competitive success over corals, with a consequent increase in coral mortality and decline in coral abundance. Stabilisation and persistence of the reversal in the relative abundances of corals and algae amounts to a phase shift. However, the following summary of the evidence for each of these steps shows that the pathway overall is unlikely to explain coral-macroalgal phase shifts in general. Increases in sediments or nutrients enhance algal growth rates
Sediments The common observation that reefs in high sediment conditions often have high relative abundance of macroalgae (e.g. McCook et al. 1997), suggests that increases in sediment loadings might enhance algal growth. However, the little information available on sediment e!ects on coral reef algae indicates that sediments are directly deleterious to macroalgae. For example, on inshore reefs of the GBR, sediment deposition inhibited Sargassum recruitment and growth (Umar et al. 1998), as predicted from temperate work. Given that most benthic macroalgae require stable substratum for attachment, and the probable e!ects of
Fig. 1 Nutrient enhancement of algal dominance: The &&direct e!ects on algae'' model. Diagram formalising the steps involved in a commonly accepted view of how nutrient eutrophication leads to algal overgrowth of corals, with consequent phase shifts and reef degradation (further explanation in the text). Critical review of available data suggests this model is #awed: nutrient enhancement is unlikely to lead to algal overgrowth of corals unless herbivory is low, naturally or due to human impacts
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suspended sediments on algal growth (reduced light due to turbidity, smothering by sediments on algal tissue), it is reasonable to assume that any bene"ts to the algae from sediments arise indirectly, either through nutrients associated with the sediments, or through reduced competition or herbivory (see later). Nutrients Increased nutrient concentration will increase algal growth, but only when growth is limited by supply of that nutrient, rather than by nutrient uptake, light availability or temperature (and only when growth rates are not already maximal). The limited data available for coral reef macroalgae suggest that this is often but not always the case. In a comprehensive series of "eld and laboratory experiments, Schaffelke and Klumpp (1997, 1998a, b) have shown that growth of Sargassum baccularia is enhanced by increased nutrient concentrations within the range of concentrations relevant to inshore fringing reefs of the GBR, but saturates at moderately high levels (5 lM NH , 0.5 lM PO ). Lapointe (1985, 1987; Lapointe 4 4 et al. 1987, also see 1997) also found that elevated nutrient concentrations enhanced growth of several taxa (including Dictyota, Gracilaria and Acanthophora), although using very high nutrient levels (up to 700 lM NH , 40 lM PO ). 4 4 However, nutrient concentrations do not always explain macroalgal growth rates in the "eld. Hatcher and Larkum (1983) found nitrogen addition signi"cantly a!ected EAC growth and standing crop in some reef zones and seasons, but not in others. McCook (1996) found that cross-shelf di!erences in nutrient inputs did not lead to di!erences in growth of Sargassum, apparently because nutrient supply rates were su$cient for growth on both coastal and o!shore reefs. Drew (1983) found that the standing crop of Halimeda increased with distance from terrestrial inputs. Russ and McCook (1999) found that di!erences in nutrient supply apparently explained temporal (inter-annual) di!erences in EAC growth rates but not spatial (cross-shelf ) patterns. Finally, in the &&ENCORE'' nutrient enhancement experiment, Larkum and Koop (1997) found that EAC growth rates were not enhanced by long-term nutrient additions, apparently because the EACs were nutrient-replete, or limited by di!usion across the boundary layer above the turf, and not by ambient, bulk-water concentrations. Thus, there is scant evidence that ambient nutrient concentrations do widely limit algal tissue production on coral reefs. Given the axiomatic high productivity of EACs on oligotrophic coral reefs (Hatcher 1988), maintained in spite of low nutrient concentrations, it is not clear that increased nutrient inputs should lead to increased growth. It is not nutrient concentration that is critical to growth, but nutrient supply and uptake, of which concentration is only one aspect. Thus algae may take up su$cient nutrients to achieve high growth rates, even in very low nutrient concentrations, if
advective supply and turbulent mixing across boundary layers are su$cient (Atkinson 1988; Larned and Atkinson 1997). Increased algal growth rates cause increased algal standing crop
This is the most critical and questionable step in this pathway, because increased growth or tissue production often does not lead to the accumulation of algal biomass on coral reefs. The distinction between production and growth (i.e. rate of tissue production) and standing crop (i.e. tissue biomass or plant abundance, the accumulation of growth) is critical (Carpenter 1988; Hatcher 1997). According to the conceptual model proposed by Littler and Littler (1984), large standing crops of macroalgae only occur in areas of low herbivory. There is now a considerable body of empirical data showing that under most circumstances algal standing crop on coral reefs is maintained at low levels by intense herbivory, often despite relatively high rates of tissue production (reviews in Hatcher 1983; Steneck 1988; Carpenter 1997; Russ and McCook 1999 for GBR). Transfer of algal primary production to herbivores is accepted to be one of the largest trophic #uxes on coral reefs (Hatcher 1981, 1988, 1997; Klumpp and Polunin 1990). Numerous experiments in the Caribbean have found algal abundance and assemblage composition to depend on grazing rates (e.g. Hay 1981; Sammarco 1982; Carpenter 1986; Lewis 1986). For the GBR in particular, large di!erences in Sargassum abundance at both large (*50 km) and medium (&50 m) scales, have been shown to depend strongly on the levels of herbivory, despite the availability of su$cient nutrients for growth (McCook 1996, 1997). Similarly, spatial (cross-shelf and within reef) and temporal (annual) variations in EAC growth rates were closely tracked by herbivore consumption, so that standing crop did not change, even after a "ve-fold increase in production following a cyclone-induced nutrient pulse (Russ and McCook 1999; also Scott and Russ 1987). Grazers also a!ected abundance, composition and nitrogen "xation of EACs at within-habitat scales on a mid-shelf reef (Sammarco 1983). There is some evidence that herbivore control of standing crop is not ubiquitous (e.g. Hatcher and Larkum 1983; McCook unpublished data for GBR inshore reef #ats), although this may re#ect compensatory e!ects of other guilds such as meso-herbivores (e.g. Brawley and Adey 1981), or e!ects too small for the experimental power (possible type II error). Algal biomass can only accumulate if tissue production exceeds total losses, including losses to herbivores (e.g. Hatcher and Larkum 1983). This can only occur if herbivory is reduced or naturally low, or if algal growth rate increases su$ciently to overwhelm ambient herbivory levels (or both). There have been numerous
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empirical examples of phase shifts following reductions in herbivory (e.g. Caribbean Diadema die-o!s, Carpenter 1990; Hughes 1994a etc). In contrast, phase shifts involving no decline in herbivory may be rare (see Discussion). Importantly, available evidence indicates that in most coral reef habitats, including those with relatively low herbivore abundances, even large di!erences in production of algal tissue are closely tracked by changes in consumption of algal tissue by herbivores (Hatcher and Larkum 1983; Carpenter 1986; Russ and McCook 1999). Thus factors which change algal production are unlikely to lead to changes in standing crop in most reef habitats, whereas factors which change herbivore consumption usually will. Further, where increased algal production does lead to increased standing crop within an area, this cannot be assumed to lead to increased areal extent of algal dominance. Increased standing crop of existing plants can mean enhanced competitive success within an area, but increased area requires either colonisation (dispersal and recruitment), or vegetative, lateral growth into the new area. Very little is known about the dispersal, recruitment or vegetative growth of most coral reef algae, so it can not be assumed that all macroalgal taxa are highly invasive. For example, invasion of new areas by Sargassum would require dispersal and recruitment of sexual propagules, which appears to be very limited outside areas of established adult populations (e.g. Kendrick and Walker 1991; McCook 1997; I.R. Price and McCook unpublished data). Although some temperate species of Sargassum have proven highly invasive, this is apparently strongly dependent on life-history characters such as reproduction (e.g. Paula and Eston 1987). In other circumstances, increased area of dominance could arise by means of a shift in relative composition of algal communities which previously co-existed with adjacent corals. For example, EACs on undisturbed reefs often include overgrazed fragments or recruits of large macroalgal taxa. If freed from herbivory, these &&dormant'' stages could develop into dominant macroalgal beds by vegetative growth alone (Hatcher 1984, 1990), and thus become potential competitors with corals. Thus, the potential for increases in extent of macroalgal dominance is dependent on the speci"c &&supply-side'' ecology of the macroalgae. Increased macroalgal standing crop leads to competitive overgrowth of corals
The "nal assumption of this model (Fig. 1) is that macroalgae and corals are competitors, so that increased abundance of macroalgae will necessarily lead to declines in coral populations. Available evidence suggests that macroalgal blooms generally will inhibit corals, but also that the mechanisms and outcomes of
the interaction vary with di!erent circumstances and life stages. Considerable correlative evidence shows that declines in coral abundance often coincide with increases in macroalgal abundance (e.g. Maragos et al. 1985; Cuet et al. 1988; Naim 1993; Hughes 1994a; Connell et al. 1997). However, this does not necessarily mean that it was the algae that killed the corals. In some cases, the increase in macroalgal abundance would appear to be a consequence, rather than a cause, of coral mortality (Kinsey 1988; Done 1992; Hughes 1994a). Further, abundances are not always negatively related, and abundant coral cover can sometimes coexist with abundant algae across a range of scales, (e.g. Fig. 2; Hatcher 1985). Experimental evidence indicates that competition with macroalgae can inhibit the growth or survival of established hard corals (Potts 1977; Hughes 1989; Tanner 1995; Miller and Hay 1996) and of coral recruits (Birkeland 1977; Hughes 1989, 1996; Miller and Hay 1996), although there has been surprisingly little experimental research. Evidence for causality also comes, "rstly from direct observations of corals harmed by direct contact, overgrowth or shading by macroalgae (e.g. Hughes 1994a Fig. 6; Keats et al. 1997 Figs. 1}2), and secondly from herbivore exclusion studies in which
Fig. 2 Cover of healthy hard corals and Sargassum on two fringing reefs of the central GBR. Data points from Goold Island (183 10.7@ S 1463 10.1@ E) and Cannon Bay (18341.1@ S 146335.2@ E), on Great Palm Island, are from 1 m2 quadrats placed in the zone of maximum Sargassum abundance (October 1997). Coral cover shows little relationship to cover of Sargassum, whether for all data, between reefs, or within reefs. Goold Island is close to coastal sources of terrestrial sediments and nutrients, and has very high turbidity and sedimentation; Cannon Bay has clearer water and less terrestrial runo!, yet reef #at coral cover is lower than at Goold Island. Cover of healthy coral at Goold Island has remained high underneath a nearly complete canopy of Sargassum for at least 7 years, strongly suggesting that the abundance of the seaweed is not leading to decline of the corals at this time scale
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coral cover declined, apparently in response to increased algal abundance (e.g. Sammarco 1982; Lewis 1986). However, other evidence shows variable outcomes of interactions between corals and macroalgae. Corals may also competitively inhibit macroalgal growth (De Ruyter van Steveninck et al. 1988). During the recent massive bleaching on the GBR (early 1998), experimental removal of Sargassum canopy showed that the canopy actually protected understory corals from bleaching (Jompa and McCook 1998, same sites as Fig. 2). Importantly, there are apparently no experimental comparisons of nutrient e!ects on competition between established corals and macroalgae (but see Birkeland 1977 for e!ects on recruitment). Given the diversity of coral and algal taxa and community compositions, their diverse physiologies and life histories, and the dependence of competitive interactions on speci"c circumstances, we should expect variable outcomes from coral-algal competition. In particular, it cannot be assumed that interactions between established corals and macroalgae are generally in such delicately balanced competition that elevated nutrients will always tip the interaction in favour of the algae. Alternative mechanisms for phase shifts, including indirect nutrient e!ects
Taken together, the evidence for each step in this model (Fig. 1) indicates that nutrients do not generally lead to phase shifts simply by directly enhancing algal competitiveness. However, this does not prove that nutrients have no e!ect, since there are a number of other mechanisms for phase shifts, including alternative and indirect mechanisms by which nutrients or sediments might contribute. Reduction in herbivory Given the well-documented, high primary productivity of coral reef algae in oligotrophic waters (e.g. Hatcher 1988), a substantial reduction in herbivory can be assumed to lead to increases in algal standing crop, as tissue production outweighs consumption by hervibores, even if there is no change in nutrient availability (also see Bell 1992). Numerous studies (cited previously) have shown increases in algal abundance in response to herbivore reduction with no change in nutrient supply, demonstrating that enhanced nutrients are not necessary for phase shifts at a wide variety of locations in the Caribbean and GBR. Combined increase in nutrient supply and reduction in herbivory As suggested by Littler and Littler's (1984) model, reduction in herbivory may have a greater e!ect if there is simultaneous nutrient enhancement and consequent increase in algal production. Reduction in topographic complexity Reductions in topographic complexity, and consequently in micro-
habitat diversity, may result in reduced densities of consumers, including not only "sh and invertebrate herbivores, but also other consumers, such as planktivores (e.g. Randall 1965; McCook 1997; Szmant 1997). Reductions in herbivory may lead directly to increased algal standing crop as mentioned, but Szmant (1997) has also suggested that reductions in other consumers may reduce the potential of a community to absorb high #uxes of nutrients without shifts in community composition. Thus communities may show symptoms of excess nutrients, such as phase shifts, without an increase in nutrient supply, if the habitat complexity is reduced. Indirect e+ects of nutrients or sediments on macroalgae: e+ects on competitors or herbivores Nutrients or sediments may indirectly bene"t macroalgae by inhibiting competitors or herbivores, even if the macroalgae do not bene"t directly. For example, sediment deposition inhibits Sargassum, but the e!ect is relatively mild (Umar et al. 1998), whereas sediment e!ects on corals are often severe (reviews by Rogers 1990, Sta!ordSmith 1993). If corals and macroalgae are competing for space, the overall impact may be an enhancement of macroalgal abundance, potentially explaining the more frequent dominance by macroalgae on heavily sedimented reefs (e.g. inshore GBR, Umar et al. 1998). In this scenario, algal enhancement is a consequence, not a cause, of coral decline. Similarly, if nutrients reduce the viability or fecundity of corals (Walker and Ormond 1982; Stambler et al. 1991), then macroalgal abundance might be enhanced to a greater degree than indicated by their response to nutrient enrichment in the absence of competion with corals (e.g. Miller and Hay 1996). Note that variability in nutrient impacts on both competitors may result in much greater variability in the overall competitive outcome. Reef waters with high suspended solids may also provide less suitable habitat for herbivorous "sh (e.g. Williams 1991). This would indirectly enhance macroalgal abundance, independent of any e!ects on algal growth (McCook et al. 1997). &&Supply-side'' ecology: impacts of eutrophication on fecundity, dispersal or recruitment of algae or corals Nutrients may have important impacts on establishment or maintenance of coral or algal populations through direct or indirect e!ects on fecundity, dispersal or recruitment, as distinct from e!ects on competition between established organisms or populations. For example, nutrients may directly inhibit coral reproductive success and settlement (Harrison and Wallace 1990; Ward and Harrison 1997) and enhance growth of algal germlings (Scha!elke and Klumpp 1997). Impacts on macroalgal fecundity, dispersal or recruitment are potentially critical, but very di$cult to predict, given the paucity of information on the &&supply-side'' ecology of coral reef algae. Competitive interactions may also
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a!ect established and recruiting individuals di!erently. A macroalgal canopy (e.g. Fig. 2) which did not inhibit established corals may nonetheless inhibit coral recruitment, leading to a long-term and subtle decline in coral populations (e.g. Connell et al. 1997). Such &&supply-side'' impacts are likely to be most critical following acute disturbances. Combined e+ects of natural disturbance and eutrophication or over,shing Acute natural or anthropogenic disturbances can have impacts which act in synergy with longer-term, chronic stresses such as eutrophication (reviews for GBR in e.g. Done 1992, 1997; Done et al. 1997; Bell and Elmetri 1995). Coral reef communities are subject to frequent disturbance by events such as cyclones, coral bleaching, crown of thorns star"sh outbreaks, and #ood-driven freshwater or sedimentation events. Recovery of reef communities from such disturbances may be rapid under natural conditions (e.g. Connell et al. 1997), but may be critically hampered by eutrophication, over"shing or other anthropogenic stresses. In particular, macroalgal growth may be insu$cient to competitively exclude corals under stable, chronically eutrophic conditions, but may prevent coral regrowth or recolonisation after disturbance, especially if herbivory is reduced. In two of the best documented cases of coral-macroalgal phase shifts (Kaneohe Bay, Hawaii, and Discovery Bay, Jamaica), corals persisted despite longterm, chronic stress (from eutrophication and over"shing). In each case, acute disturbances (fresh-water runo! and hurricane, respectively) were major, immediate causes of coral mortality yet there can be little doubt that the long-term failure of recovery was due to the chronic human impacts (Kinsey 1988; Hughes 1994a; Steneck 1994; also Lapointe 1997). Human impacts which lead to failure to recover from acute disturbances are likely to be very important in terms of reef management (Done 1992; Hughes 1994a). Natural disturbances on coral reefs are frequent but very patchy and unpredictable in time and space (e.g. Connell et al. 1997). This means that human impacts on recovery are likely to be expressed piecemeal, as a gradual, &&ratchet fashion'' accumulation of small impacts, which are very di$cult to detect and attribute (also Hughes 1994a). Done (1995, 1997) and Done et al. (1997) provide conceptual synthesis and discussion of these ideas for the GBR, emphasising the potential importance of human impacts on the ratios between disturbance &&return times'' and impact recovery times, especially for the long-term sustainability of reef growth. Interactions between impacts, and stabilisation of phase shifts Many of the e!ects discussed may interact in complex ways, and where di!erent factors synergise, positive feedback may amplify otherwise relatively small or short-term changes, and the community may fail to recover. For example, human inputs to terrestrial
runo! generally increase both suspended sediments and nutrients. This may result in less suitable habitat for herbivorous "sh, as well as having direct e!ects on algal and coral growth and competition. Similarly, cyclones or other physical disturbances that injure and destroy corals will reduce the topographic complexity of the substratum and may thus reduce herbivory, releasing algal biomass from herbivore control (as described). The same disturbance may release nutrients from resuspended sediments, thereby enhancing algal growth rates (Russ and McCook 1999), and providing a competitive advantage to macroalgae. Development of macroalgal mats or beds may enhance sediment trapping (personal observation; S. Purcell, James Cook University, unpublished data), consequently inhibiting coral recolonisation and maintaining habitat unsuitable for herbivorous "shes.
Discussion: significance to reef science and management Does it matter how nutrients act?
The di!erences between direct and indirect nutrient e!ects are signi"cant, even if they lead to the same outcome (algal dominance and coral decline). In many cases, the simple direct e!ects paradigm is intended only as a simpli"cation or illustration, rather than a de"nitive, mechanistic explanation. However, uncritical acceptance of that view ignores the possible alternatives, and their consequences for understanding and responding to phase shifts.
Signi,cance of the mechanism of nutrient impacts to assessments of human impacts
Acceptance of over-simplistic models of ecological impacts increases the risk of false conclusions during assessments of those impacts. To use inshore reefs of the GBR as an illustration: widespread increases in terrestrial runo!, from agricultural and pastoral landuse, are potentially major threats to reef condition at very large scales. However, their impact may occur, not as a consistent and uniform process easily attributed to the land-use, but as failure to recover from relatively small-scale, spatially disjoint disturbances (such as coral bleaching, cyclones or freshwater kills). Thus the impact may involve a series of local impacts, apparently unconnected in time and space, but the overall impact at a regional-decadal scale might be widespread and extensive reef degradation. Assessment of the changes could demonstrate that the direct, proximal cause of coral loss was not adjacent land-use, but rather the natural disturbance event/s, and this could be taken as &&proof '' of no impact (especially in a political forum), despite a very real impact. These risks are accentuated
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by the subtle, piecemeal and long-term nature of the impacts, which make them di$cult to prove (especially at P: H (0.05). Common-sense dictates pre-emptive 0 measures to reduce the run-o!, but political pressure groups could oppose these measures based on the lack of evidence for direct impacts, and on the dramatic and often extensive impacts of the natural disturbances. At a smaller scale, similar risks apply to assessment of individual coastal developments. Signi,cance for prevention or reversal of phase shifts
The simple &&direct e!ects'' model suggests little or no need to protect or restore herbivore populations, yet they are certainly critical. Even if reef communities at Discovery Bay were eutrophic, they are unlikely to recover without restoration of herbivore abundances (Hughes 1994b; Szmant 1997; Hughes et al. in press; c.f. Lapointe 1997). This point is relevant to reefs in many developing nations where reefs are over"shed, and to reefs a!ected by urban sewage runo!. Management e!ort directed at reducing nutrient (sewage or fertiliser) runo!, without limiting sediment inputs or protecting herbivores, will probably prove ine!ective, and waste resources. (Inversely, restoration of herbivore populations may well require restoration of suitable water quality.) On the GBR, herbivorous "sh are not heavily "shed and thus management of runo! may be e!ective, but only as long as herbivorous "sh remain abundant. Signi,cance to reef rehabilitation
Development of e!ective, small-scale reef rehabilitation methods and strategies (e.g. Harriott and Fisk 1987) will also depend on the causal details of the degradation process. For example, coral transplantation may prove e!ective even in high nutrient areas, if herbivore abundance and topographic complexity are su$ciently protected, but may be ine!ective in oligotrophic areas that have been "shed heavily or using explosives. Eutrophication or herbivore reduction as su.cient single causes
Reviewing the various documented cases of anthropogenic eutrophication (e.g. Smith et al. 1981; Cuet et al. 1988; Lapointe and O'Connell 1989; Littler et al. 1992) it seems probable that most eutrophic reefs also have arti"cially low levels of herbivory, either directly due to "shing (especially in relatively poor countries), or indirectly due to unsuitable water conditions. For example, Stimson et al. (1996) suggested that the persistence of macroalgae at Kaneohe Bay was dependent on reductions in herbivorous "shes. Even if nutrient increases did contribute to algal blooms in Jamaica
(Lapointe 1997 but see Hughes et al. in press), those increases were certainly not the sole cause, given the evidence for e!ects of herbivore reductions (Hughes 1994a,b, Hughes et al. in press). In contrast, the absence of abundant, large macroalgae on reefs remote from anthropogenic nutrient sources does not depend on low nutrient availability, since those reefs can support high growth rates of large macroalgae in herbivore exclusions (e.g. Lewis 1986; McCook 1996). This suggests that either (1) reduced herbivory is su$cient cause for increased algal abundance, and nutrient availability is (naturally) widely suf"cient for growth, not widely limiting as previously thought (Atkinson 1988); or (2) that eutrophication is so widespread and large-scale as to a!ect those remote areas. Thus for the GBR (McCook 1996), the lack of nutrient depletion in Sargassum transplanted to o!shore reefs shows that nutrient availability is su$cient, but this does not preclude eutrophication of the entire GBR lagoon, as suggested by Bell (1992) and Bell and Elmetri (1995). Mechanisms and signi,cance of herbivory tracking algal production
The conclusion that consumption by herbivores can track and absorb even several-fold increases in algal production (reviewed in previous section) is particularly signi"cant because it suggests that abundant herbivore populations can bu!er and protect reef communities against changes in algal production. Russ and McCook (1999) suggest that the mechanism of this tracking is more likely to involve changes in individual consumption rates than changes in herbivore population densities, given the rapid time scale of the response (although herbivore populations may show some response in post-recruitment survival at time-scales of years e.g. Carpenter 1990; Robertson 1991). Assuming an upper limit on individual consumption rates, this in turn implies an upper limit on the potential of herbivore populations to absorb extra algal production. Thus the ability of herbivore populations to absorb extra algal production may also serve to suppress indications of shifts in trophic balance, delaying recognition of nutrient overloads until the reef is very stressed and vulnerable. This herbivore &&bu!er'' e!ect will be least e!ective on reefs or zones where populations are naturally or arti"cially low (such as fringing reef #ats on inshore continental islands of the GBR, McCook 1997).
