Herbivory, Nutrients, Stochastic Events, 

and Relative Dominances of Benthic 

Indicator Groups on Coral Reefs: 

A Review and Recommendations

Mark M. Littler, Diane S. Littler, 

and Barrett L. Brooks

ABSTRACT. Threshold levels (i.e., tipping points where the probability of community 

phase shifts is increased and the potential for recoverability is reduced) for critical bottomup interactions of productivity (e.g., nutrients) and those for top-down disturbances (e.g., 

herbivory) must be known to manage the competitive interactions determining the health 

of coral-dominated reefs. We further posit that latent trajectories (reduced resiliencies/

recoverability from phase shifts) are often activated or accelerated by large-scale stochastic disturbances such as tropical storms, cold fronts, warming events, diseases, and 

predator outbreaks. In highly diverse and productive reef ecosystems, much of the overall 

diversity at the benthic primary producer level is afforded by the interaction of opposing 

nutrient-limiting/nutrient-enhancing and herbivory controls with the local physical and 

spatial variability, such that a mosaic of environmental conditions typically occur in close 

proximity. Although the relative dominance model (RDM) appears straightforwardly 

simple, because of the nature of direct/indirect and stimulating/limiting factors and their 

interactions it is extremely complex. For example, insuffi cient nutrients may act directly 

to limit fl eshy algal domination (via physiological stress); conversely, abundant nutrients 

enhance fl eshy algal growth, with the opposite effect on reef-building corals (via toxic 

inhibition or increased diseases). Furthermore, the effects of controls can be indirect, 

by infl uencing competition. Even this seemingly indirect control can have further levels 

of complexity because competition between algae and corals can be direct (e.g., overgrowth) or indirect (e.g., preemption of substrate). High herbivory (via physical removal) 

also acts indirectly on fl eshy algae through reduced competitive ability, whereas lowered 

herbivory and elevated nutrients also indirectly inhibit or control corals and coralline algae by enhancing fl eshy algal competition. Other ecologically important bottom-up factors, such as reduced light, abrasion, allelopathy, disease vectoring, and sediment smothering, also result from indirect side effects of fl eshy algal competition. These factors tend 

to selectively eliminate the long-lived organisms in favor of weedy fast-growing species, 

thereby reducing desirable complexity and biodiversity.

INTRODUCTION

There has been an exhaustive debate in the coral reef literature over the relative importance of forces that regulate community structure and resilience (i.e., 

the potential to resist stresses and to recover following disturbances). The expansion of the human population and associated increases in destructive fi shing 

Mark M. Littler, Diane S. Littler, and Barrett L. 

Brooks, Department of Botany, National Museum of Natural History, Smithsonian Institution, 

P.O. Box 37012, MRC 166, Washington, D.C. 

20013-7012, USA. Corresponding author: M. 

Littler (littlerm@si.edu). Manuscript received 13 

May 2008; accepted 20 April 2009.

32_Littler_401-414_Lang.indd 401 2_Littler_401-414_Lang.indd 401 9/24/09 10:33/24/09 10:33
402 • SMITHSONIAN CONTRIBUTIONS TO THE MARINE SCIENCES

(Hughes, 1994) and nutrient loading (Lapointe, 1999), compounded with ocean warming (Hoegh-Guldberg, 1999) and 

stochastic environmental effects (Precht et al., 2005), have 

been broadly debated to explain the increasing degradation of coral reefs worldwide. Because human population 

growth is not expected to abate, discriminating among 

various stressors is critical to determine conservation 

strategies and to eventually ameliorate the accelerating 

degradation of coral reefs. What has been lacking is the 

ability to rigorously test and differentiate among the possible acute versus chronic stressors— leading to ongoing 

controversy. In an attempt to address this problem, several workers (Mora, 2008; Burkepile and Hay, 2006) have 

conducted broad correlative and statistical assessments 

of communities over large regional scales. These studies 

have suggested a clear interaction between eutrophication 

in conjunction with declining herbivorous organisms as 

direct causes for maintaining present undesirable phase 

shifts on coral reefs.

Such phase shifts have been devastating to the many 

uniquely specialized benthic photosynthetic symbionts 

dominating tropical reefs, which are responsible for some 

of the most productive natural ecosystems known. Four 

major space-occupying groups of benthic primary producers combine to create high coral-reef primary productivity: 

reef-building corals (containing symbiotic algae), crustose 

coralline algae, algal turfs (fl eshy fi lamentous and lowgrowing prostrate forms, and frondose macroalgae. Of 

these, photosynthetic corals create much of the structural 

heterogeneity and complexity and, with coralline algae, 

are primarily responsible for accretion of CaCO3 into the 

reef matrix— making them the most desirable functional 

groups from a management perspective.

A basic objective in management ecology is to determine the mechanisms by which natural and anthropogenic 

factors maintain or alter structure and interactions in biotic communities. Anthropogenic eutrophication and destructive overfi shing (i.e., herbivore removal by trapping, 

netting, poisoning, blasting) are the most tractable factors correlated with the marked global decline in tropical 

reef communities over the past two decades (see reviews 

in Ginsburg, 1994; Birkeland, 1997; papers in Szmant, 

2001). The theoretical framework involving “top-down” 

regulation by predators and “bottom-up” control by resource availability in terrestrial systems was fi rst proposed 

by Hairston et al. (1960), concepts that were later used 

(Atkinson and Grigg, 1984) to describe mechanisms that 

regulate the structure of coral-reef communities. These 

factors provide a valuable perspective (Figure 1) to assess 

and manage the human activities that affect the interactive mechanisms controlling stable states, tipping points, 

phase shifts, and recovery among the dominant functional 

groups of primary producers on tropical reefs.

In healthy coral-dominated reefs, nutrient concentrations are extremely low and attachment space is occupied 

by a broad diversity of three-dimensional overgrowing organisms. Given these conditions, the major tenets of the 

management model proposed by Littler and Littler (2006: 

fi g. 1, relative dominance model [RDM]) are (1) that competition for space and light is crucial in determining the relative abundances of major benthic photosynthetic organisms, 

and (2) that the outcome of competition for these resources 

is most often, but not exclusively, controlled by the complex 

interactions of biological factors (top-down controls such 

as grazing) and environmental factors (bottom-up controls 

such as nutrient levels). As suggested by Grime (1979) 

for terrestrial plants and expanded for marine macroalgae (Littler and Littler, 1984; Steneck and Dethier, 1994), 

primary producer abundance and evolutionary strategies 

are controlled by physical disturbances (i.e., factors that 

remove biomass) coupled with physiological stresses (i.e., 

factors that limit metabolic production). In the conceptual 

relative dominance model (RDM; see Figure 1), grazing 

physically reduces biomass (top-down) and nutrients control production (bottom-up). The complex natural interactions between herbivory and nutrients are most dramatically impacted by large-scale catastrophic disturbances 

such as tropical storms (Done, 1992), warming events 

(Macintyre and Glynn, 1990; Lough, 1994), cold fronts 

(Precht and Miller, 2007), diseases (Santavy and Peters, 

1997), and predator outbreaks (Cameron, 1977). These 

events serve to trigger or accelerate the ultimate long-term 

phase shifts postulated in the RDM. Such stochastic events 

selectively eliminate the longer-lived organisms in favor of 

faster-growing fl eshy macroalgae, which are often competitively superior (Birkeland, 1977). However, nutrients and 

herbivory, in the absence of large-scale disturbances, are 

both suffi cient to maintain phase shifts independently or 

in concert (Smith et al., 2001; Armitage and Fong, 2004; 

Littler et al., 2006a).

On undisturbed oligotrophic coral-reef habitats, the 

effects of well-documented top-down physical controls via 

intense herbivory prevail, where changes in grazing intensity often show acutely rapid effects. Conversely, bottom-up 

stimulatory controls are more chronic, the result of lack of 

nutrient availability, overcompensation by grazers, and a 

slower growth response, compared with acute physical destruction by herbivory. However, under persistent elevated 

nutrient conditions (relative to low [near-undetectable] 

concentrations), consistent coral declines can occur, con32_Littler_401-414_Lang.indd 402 2_Littler_401-414_Lang.indd 402 9/24/09 10:33

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NUMBER 38 • 403

comitant with algal increases that may lead to enduring 

states throughout all combinations of herbivory (Littler 

et al., 2006a). Changes in bottom-up controls and their 

interactions not only alter the dominance patterns of the 

major benthic functional groups on coral reefs but, hypothetically, could have profound long-term consequences 

mediated through structural transformations and chemical modifi cations to reef systems and their herbivorous 

fi sh populations. In other words, excessive nutrient enrichment not only increases the productivity and biomass of 

weedy macroalgae via bottom-up controls that alter patterns of competitive dominance (Littler et al., 1993) but, 

over the long term, may lead to coral habitat degradation 

through (1) reduced spatial heterogeneity by overgrowth 

(Johannes, 1975; Pastorok and Bilyard, 1985; Szmant, 

1997) and (2) nighttime anoxic conditions (tolerated by 

macroalgae, but not by coral competitors and herbivorous 

predators; Lapointe and Matzie, 1996) that could indirectly reduce top-down grazer effects. Furthermore, fl eshy 

macroalgal blooms, irrespective of how they are induced, 

decrease the growth and reproductive capacity of the more 

structurally complex reef-building corals (Tanner, 1995; 

Miller and Hay, 1996; Bellwood et al., 2006; Hughes et 

al., 2007), as well as inhibit coral larval recruitment (Birkeland, 1977; Tomascik, 1991; Ward and Harrison, 1997) 

and survival (Lewis, 1986; Hughes et al., 1987; Hughes, 

1989; Wittenberg and Hunte, 1992). Such complicated 

feedback loops following eutrophication (e.g., anoxia) are 

known to occur in seagrass meadows (Sand-Jensen and 

Borum, 1991; Duarte, 1995) and could also explain decreases in fi sh populations on coral reefs with long-term 

histories of eutrophication.

CORAL-REEF MANAGEMENT

The data relevant for long-term reef management consist of (1) many important short-term caging and feeding 

experiments (in the case of exceedingly well-documented 

top-down herbivory effects), (2) circumstantial evidence 

(Hallock et al., 1993), (3) correlative biogeographic surveys contrasting oligotrophic versus eutrophic systems 

(Littler et al., 1991; Verheij, 1993; Mora, 2008), (4) comparative experiments on systems containing natural nutrient gradients (Lapointe et al., 2004, 2005b; Vroom et al., 

2005), (5) physiological assays (Littler and Littler, 1990; 

Lapointe et al., 1997), and (6) logistically complicated, in 

situ, long-term, experimental/causality studies, in the case 

of bottom-up nutrient controls (Smith et al., 2001; Littler 

et al., 2006a). Top-down control by abundant populations 

FIGURE 1. The competition-based relative dominance model 

(RDM). All the functional indicator groups occur under the conditions of every compartment of the model; however, the RDM predicts which group will most often dominate. Light to dark shading indicates declining desirability of each functional group from 

a management perspective. Crustose coralline algae are posited to 

be competitively inferior and dominate mainly by default, that is, 

where fl eshy algae are removed by herbivores and some corals are 

inhibited by nutrients. The dashed lines approximate tipping points 

where declining herbivory and increasing nutrients reach critical levels that begin to reduce resilience to and recoverability from phase 

shifts. One vector can partially offset the other; for example, high 

herbivory can delay the impact of elevated nutrients, or low nutrients 

may offset the impact of reduced herbivory. As a baseline for healthy 

coral-reef habitats, herbivore population abundances and diversity 

should be high and palatable test plants should show at least greater 

than 50% loss 6 h1 (i.e., 6 h half-life) during a replicated series of 

midday in situ exposures. Hypothetical nutrient tipping points (i.e., 

thresholds that sustain algal growth) are thus far indicated to be quite 

low (i.e., 0.1 M soluble reactive phosphorus [SRP], 1.0 M dissolved inorganic nitrogen [DIN]), as suggested by laboratory growth 

experiments, case studies for macroalgal overgrowth of coral reef 

communities, and in situ experimental nutrient enrichment research 

(Bell, 1992; Bell and Elmetri, 1995; Lapointe et al., 1993, Bell et al., 

2007). We further posit that latent trajectories (reduced resilience/

recoverability from phase shifts) are often triggered or accelerated 

by large-scale stochastic disturbances such as tropical storms, cold 

fronts, warming events, diseases, and predator outbreaks. Although 

these are events from which coral reefs have recovered for millions 

of years in the absence of humans, when tipping points remain surpassed, less-desirable stable states can persist.

32_Littler_401-414_Lang.indd 403 2_Littler_401-414_Lang.indd 403 9/24/09 10:33/24/09 10:33
404 • SMITHSONIAN CONTRIBUTIONS TO THE MARINE SCIENCES

of large mobile herbivores is particularly well studied for 

coral reefs, beginning nearly fi ve decades ago with the caging study of Stephenson and Searles (1960 As examples, 

Sammarco et al. (1974), Ogden and Lobel (1978), Sammarco (1980), Carpenter (1986), Lewis (1986), Morrisson (1988), and numerous other workers (see review by 

McCook et al., 2001) have demonstrated that lowering 

herbivory in low-nutrient habitats (usually assumed) often 

results in rapid increases in low-growing stages of fl eshy 

macrophytes.

In the study of Lewis (1986) on the same reef fl at studied by Littler et al. (2006a, 2006b), increases in a dominant vegetative algal turf form (Vaughaniella stage) with 

its upright fertile Padina blades, not blooms of mixed 

macroalgae, followed short-term (11 week) reductions of 

herbivorous fi sh grazing under conditions of low nutrient 

levels. Lewis’ (1986) table 4 (although pseudoreplicated) 

shows statistically signifi cant, but relatively small, increases (26%) in the above Vaughaniella-turf stage and its 

reproductive Padina blades; however, in contrast to several literature citations, no signifi cant increases occurred 

in any of the abundant upright macroalgal dominants such 

as Turbinaria turbinata and Halimeda spp. Such low mats 

are unique in containing an abundance of nitrogen-fi xing 

blue-green algae that can enrich other members within 

the low-growing algal community (Adey and Goertmiller, 

1987; Adey, 1998). In presumably higher-nutrient environments, herbivore removals usually result in dramatic 

blooms of larger frondose macroalgae (Bellwood et al., 

2006: fi g. 4; Hughes et al., 2007).

Throughout the past decade, many biologists and 

managers have not recognized the importance of chronic 

nutrient enrichment and associated eutrophication problems facing coral reefs. A recent study (Littler et al., 2006b) 

provided a detailed review and discussion of the misinterpretations, misunderstandings, and suboptimal experimental designs that pervade the literature in regard to nutrient 

enrichment and the health of coral reefs. Overgrown 0.5 L 

porous clay-pot diffusers (“mini-reefs,” following a decade of recruitment, colonization, and competition) were 

utilized (Littler et al., 2006b) to evaluate protocols for 

studies of controlled nutrient enrichment on coral reefs. 

A commonly used nutrient source, Tree Food Stakes containing up to 6% chlorine, resulted in a signifi cant 11-

fold and 20-fold decrease of fl eshy algae and calcareous 

coralline algae, respectively, relative to the control treatments, while blue-green algae (Cyanobacteria) became 

signifi cantly (6 fold) more abundant. Osmocote-fi lled 

mini-reefs showed no signifi cant differences from the 

controls for any of the indicator groups. By avoiding the 

pitfalls of suboptimal study areas, insuffi cient duration of 

colonization/competition studies, inadequate nutrient detection limits, and inappropriate sources of enrichment in 

future research, the potential to provide new insights into 

the nutrient status of coral reefs will be greatly improved. 

Nutrient research is logistically diffi cult and, because the 

growth responses are relatively slow (i.e., chronic), requires more emphasis on multifaceted approaches carried 

out over suffi ciently long time periods. Optimally, studies 

should include in situ enrichment experiments that test the 

long-term competitive interactions of functional indicator 

groups on healthy coral-dominated reefs, in addition to 

precisely monitoring water column nutrient levels, tissue 

C:N:P ratios, and algal physiological response assays.

Although nutrient data are typically lacking in coralreef herbivory studies, natural background levels in conjunction with ample water motion are usually assumed to 

exceed levels that are limiting to macroalgal growth (Fong 

et al., 2003). As pointed out by Lewis (1986), large frondose macroalgae such as Sargassum and Turbinaria do occur in oligotrophic reef areas adjacent to coral colonies (see 

also Littler et al., 1986; McCook et al, 2001; Vroom at 

al., 2005); however, many of these frondose forms occupy 

microhabitats that generate increased current acceleration, 

such as the reef crest and tops of patch reef rocks, implicating higher nutrient fl uxes (Atkinson et al., 2001). Also, 

large biomass/standing stocks of slow-growing perennial 

macroalgae (e.g., rockweeds) can develop over time under 

low inorganic nutrient concentrations; rainforests are good 

illustrations of this as well. Furthermore, Sargassum spp. 

can coexist with corals in oligotrophic waters by utilizing 

particulate organic sources of nutrients (Schaffelke, 1999); 

therefore, in this particular situation, large plant biomasses 

of low diversity do not necessarily indicate detrimentally 

abundant dissolved nutrients. Tissue analyses of mid-shelf 

Sargassum transplants on the great barrier reef (McCook, 

1999) revealed a C:N ratio of 32:1 and a C:P ratio of 

1261:1, exceeding values for pelagic Sargassum in the nutrient-impoverished Sargasso Sea (C:P  877:1; Lapointe, 

1995), which are compelling for substantial N limitation 

and severe P limitation. A further consideration is the nowubiquitous presence of signifi cant anthropogenic nitrogen 

sources (from burning fossil fuels) in rainfall worldwide 

(Vitousek et al., 1997), making the term “pristine” relative, 

at best. The demise of copious coral cover (Pollock, 1928) 

and concomitant rise in frondose algae (Doty, 1971) and 

coralline algae (Littler, 1971) on the reef fl at at Waikiki, 

Hawaii, was the fi rst phase shift from coral to macroalgal 

domination that was postulated (Littler, 1973) as caused 

by increases in eutrophication (bottom-up control).

32_Littler_401-414_Lang.indd 404 2_Littler_401-414_Lang.indd 404 9/24/09 10:33/24/09 10:33
NUMBER 38 • 405

Eutrophication affects coral reefs to different degrees 

and on varying scales. Several studies (Atkinson et al., 

1995; Grigg, 1995; Steven and Broadbent, 1997; McCook, 

1999; Bongiorni et al., 2003) indicated no substantial adverse responses of coral species to elevated nutrients. However, other laboratory and fi eld experiments (Pastorok and 

Bilyard, 1985; Tomascik and Sander, 1987; Muscatine et 

al., 1989; Stambler et al., 1991; Jokiel et al., 1994; Koop 

et al., 2001) have concluded that corals are negatively affected by increased levels of nutrients and that diversity 

suffers. Numerous in situ observations exemplify the types 

of shifts from coral dominance to algal dominance that 

suggest linkages with chronic nutrient loading, including 

case studies in Hawaii (Littler, 1973; Banner, 1974; Smith 

et al., 1981; Maragos et al., 1985; Grigg, 1995), Venezuela (Weiss and Goddard, 1977), the Red Sea (Mergener, 

1981; Walker and Ormond, 1982), Barbados (Tomascik 

and Sander, 1985, 1987), American Samoa (Green et al., 

1997), Reunion Island (Cuet et al., 1988; Naim, 1993), 

Bermuda (Lapointe and O’Connell, 1989), the Great 

Barrier Reef (Bell, 1992), the Florida Keys (Lapointe et 

al., 1994), Martinique (Littler et al., 1993), and Jamaica 

(Goreau et al., 1997; Lapointe et al., 1997).

In a number of cases, herbivory patterns alone (similar to nutrient levels) do not explain the distribution and 

abundance of benthic algae on coral reefs (Adey et al., 

1977; Hay, 1981; Hatcher, 1983; Hatcher and Larkum, 

1983; Carpenter, 1986). Several studies (Hatcher, 1981; 

Schmitt, 1997; Lirman and Biber, 2000) found no signifi cant correlation between grazing intensity and algal 

biomass. A dramatic increase in algal biomass resulting 

from eutrophication, without any simultaneous reduction 

in herbivore populations, was reported (Fishelson, 1973). 

The importance of the very low nutrient levels involved in 

eutrophication (i.e., nutrient threshold hypothesis, NTH), 

either natural or anthropogenic, has only recently come to 

light (Bell, 1992; Lapointe et al., 1997; Small and Adey, 

2001; Bell et al., 2007) regarding the potential for phase 

shifts from corals toward macroalgal dominance. These 

kinds of biotic phase shifts also have been attributed to 

overfi shing of herbivore stocks (see Hughes, 1994 on 

Jamaican reef trends), in concert with cultural eutrophication (Goreau et al., 1997; Lapointe et al., 1997). It is 

now clear (Burkepile and Hay, 2006; Mora, 2008) that 

both herbivory and nutrient levels interact on large scales 

as major factors in maintaining or degrading coral-reef 

health.

We hasten to point out that individuals of all the functional indicator groups can and do occur under the conditions of every compartment of the RDM (see Figure 1); 

however, the model predicts which group most often will 

dominate (as does the very similar fi g. 2a in Bellwood et 

al., 2004). Such apparent presence/absence anomalies, 

on closer inspection, are often scientifi cally logical but 

have led to different perspectives. Following large coral 

bleaching events and die-offs in Belize, we have observed 

dramatic increases in chemically defended sponges (e.g., 

Chondrilla) and Cyanobacteria (blue-green algae) under 

high levels of grazing by sea urchins and fi shes. Other observations that appear counterintuitive include some corals 

growing in high-nutrient habitats, some large fl eshy macroalgae growing under low nutrients, certain turf algae exposed to high herbivory, and the frequent coexistence of 

crustose corallines and the other functional groups. We 

agree with these observations and have addressed such 

anomalies herein.

The general applicability as well as the limitations of 

the RDM can be demonstrated further in relationship to 

a number of recent studies. For example, nutrients and 

herbivory are not independent, and the positive effects of 

nutrients on marine plant productivity and growth can actually make plants more palatable and susceptible to grazers (McGlathery, 1995; Boyer et al., 2004). Furthermore, 

nutrient increases are sometimes associated with coral 

inhibition (Koop et al., 2001) as well as coral diseases 

(Harvell et al., 1999, 2002; Bruno et al., 2003), and algal 

blooms can serve as disease vectors (Nugues et al., 2004). 

The sophisticated enrichment study (ENCORE) on a large 

and carefully controlled scale (Larkum and Koop, 1997; 

Encore Group, 2001) did not produce supportive results 

because (1) ambient nutrient levels within the lagoon at 

One Tree Island are well above tipping-point concentrations that may be inhibitory to some corals, while being 

more than suffi cient to support luxuriant frondose macroalgal growth (Bell, 1992; Larkum and Koop, 1997; Bell 

et al., 2007) and (2) the test organisms were isolated on 

raised grids to measure growth rates, precluding natural 

encroachment, overgrowth, or other competitive interactions crucial to testing the RDM. However, all increases 

in nutrient levels did adversely affect coral reproduction 

(Koop et al., 2001). Additionally, several short-term (4 

months) studies (Thacker et al., 2001; Belliveau and Paul, 

2002; Miller et al., 1999; McClanahan et al., 2002) reported lack of algal stimulation following nutrient enrichment, further documenting the low ambient nutrient concentrations sustaining ample algal growth.

In contrast, two in situ experimental studies conducted over longer time scales in healthy coral-reef settings 

(Smith et al., 2001; Littler et al., 2006a), in conjunction 

with natural successional and competitive interactions, 

32_Littler_401-414_Lang.indd 405 2_Littler_401-414_Lang.indd 405 9/24/09 10:33/24/09 10:33
406 • SMITHSONIAN CONTRIBUTIONS TO THE MARINE SCIENCES

provided the most relevant causality data demonstrating 

the importance of both nutrient and herbivory infl uences; 

the present review builds on these fi ndings. The paper by 

Lapointe (1997) was the fi rst to put forth a convincing 

case for the effectiveness of the RDM in addressing harmful algal bloom issues on coral reefs. Additionally, highly 

diverse living model systems of coral-reef communities 

(i.e., mesocosms), operated for decades (Small and Adey, 

2001), clearly have demonstrated that minute increases 

in nitrogen and phosphorus reduce coral growth (sometimes causing substantial die-backs). Such self-contained 

systems require continuous removal of nutrients by algalturf scrubbers or protein skimmers in combination with 

an abundance of fi sh and invertebrate grazers to maintain 

a high coral and algal diversity. The burgeoning awareness of coral-reef degradation worldwide (see Ginsburg, 

1994; chapters in Birkeland, 1997; Gardner et al., 2003), 

particularly from coastal eutrophication (Bell, 1992; Windom, 1992; Nixon, 1995; Lapointe, 1997, 1999) and destructive overfi shing (Hughes, 1994; Jackson et al., 2001), 

makes this management perspective relevant and opportune (see Figure 1).

Although harmful macroalgal blooms on coral reefs 

have long been attributed to nutrient enrichment and 

eutrophication (Littler, 1973; Banner, 1974; Johannes, 

1975; Smith et al., 1981; Lapointe, 1997; Lapointe et al., 

2005a, 2005b), some reef biologists have countered that 

such changes in benthic community structure routinely 

result primarily from natural stochastic events (Precht et 

al., 2005), overfi shing of herbivorous fi sh stocks (Hughes, 

1994; Pandolfi et al., 2003; Lesser, 2004), or loss of keystone grazers, such as the long-spined sea urchin Diadema 

antillarum (Jackson et al., 2001). Although generally supported, these last observations are not typical of the majority of grazer reduction experiments in extreme oligotrophic 

environments (see Lapointe, 1999), most of which have 

reported an expansion of small low-growing algal forms 

rather than macroalgal blooms (as predicted in Figure 1). 

It is encouraging that the critical role of excess nutrients 

on coral reefs has begun to receive attention in recent review papers (Scheffer et al., 2001; Hughes et al. 2003; 

Bellwood et al., 2004; Pandolfi et al., 2005; Burkepile and 

Hay, 2006; Mora, 2008). Some scientists (e.g., Precht et 

al., 2005) downplay declining resilience issues, instead emphasizing fundamental stochastic factors such as upwellings, hurricanes, and cold fronts (see caption, Figure 1). 

These occurrences represent unmanageable events from 

which coral reefs have recovered for millions of years, but 

not in the presence of modern human infl uences such as 

destructive overfi shing and nutrient pollution (see Mora, 

2008). There are strong interactions between catastrophic 

stochastic factors and the roles of herbivores and nutrients 

that strongly impact reefs. For example, coral mortality 

following hurricanes and coral bleaching events opens up 

large amounts of new two-dimensional space readily colonized by fast-growing algae. Such increases in productivity and the area available for grazing hypothetically satiate the herbivore pressure over large areas, assuming that 

natural herbivore populations have an upper limit in the 

amount of reef area that they can graze effectively (Williams et al., 2001; Mumby, 2006). This diluted grazing 

pressure and reduction in suitable shelter could in turn 

lead to further increases in algal cover and a decline in the 

recovery capacity (i.e., resilience) of coral communities. 

Thus, stochastic processes are unquestionably important 

factors in determining the trajectories of reef health and 

interact with the processes discussed herein.

To establish the baseline conditions and detect subsequent changes, a combination of environmental, survey, inventory, and bioassay data are essential to characterize and 

monitor the ambient nutrient and herbivory environments 

and antecedent nutrient history of a given management 

area. Valid and reliable data are the cornerstone needed 

to prioritize among different management strategies and 

motivate the local populace and politicians/lawmakers to 

support and implement the goals necessary for responsible 

management. The RDM provides a clear visual depiction 

that is easily understood and, therefore, can serve as a 

convincing illustrative aid. It is essential that assessment 

and monitoring methods should be both simple and rapid 

to use. Chlorophyll a concentration (determined by fl uorometric or spectrophotometric methods; see Bell and Elmetri, 1995) is an especially useful ancillary indicator of 

water column enrichment because phytoplankton blooms 

can rapidly attenuate critical light energy while buffering inorganic nutrient pulses. Along with nutrient levels, 

chlorophyll a serves as a valuable tipping-point indicator, 

where levels in excess of 0.2– 0.3 g L1 indicate approaching overabundances of nutrients (Bell et al., 2007).

Water column nutrient concentrations represent the 

net sum of internal cycling, algal assimilation, and external 

inputs, relative to macroalgal growth demands (Lapointe, 

1997), and therefore offer the most direct method to assess 

nutrient excesses on any given coral reef. Consequently, a 

nutrient threshold model based on nutrient concentrations 

(rather than on nutrient fl uxes) is not only valid but is 

likely the best index of nutrient status. Low-nutrient tipping points, where increasing nutrients reach hypothetically critical levels that begin to reduce recoverability from 

phase shifts (i.e., 1.0 M dissolved inorganic nitrogen 

32_Littler_401-414_Lang.indd 406 2_Littler_401-414_Lang.indd 406 9/24/09 10:33/24/09 10:33
NUMBER 38 • 407

[DIN]  nitrogen: 0.014 ppm N or 0.040 ppm NO3 and 

0.10 M soluble reactive phosphorus [SRP]  phosphorus: 0.003 ppm P or 0.007 ppm PO4), have been broadly 

corroborated (in developing the nutrient threshold hypothesis [NTH]; Bell, 1992; Lapointe et al., 1993; Bell et al., 

2007) for sustaining macroalgal overgrowth of seagrass 

beds and coral reefs. The physiological/kinetic basis for 

such low-nutrient tipping points is the hyperbolic Monod 

relation (Droop, 1985; Bell et al., 2007), which is also supported by controlled, high-fl ux, continuous-culture laboratory experiments (Caperon et al., 1971 DeBoer et al., 

1978; Lapointe and Tenore, 1981). In our experience, if 

modern analytical instruments can detect measurable nutrient levels, so can growth-limited macroalgae.

Additionally, a wealth of in situ coral-reef studies carried out in areas characterized by nutrient levels only moderately above the putative 0.1 M SRP and 1.0 M DIN 

tipping points (Larkum and Koop, 1997; Miller et al., 

1999; Thacker et al., 2001) have reported minimal algal 

stimulation following experimental nutrient enrichment, 

further documenting the low natural nutrient concentrations required for ample algal growth and their widespread 

applicability. Some corals can tolerate high levels of DIN 

and SRP; however, nutrient tipping points not much above 

the present analytical limits of detection represent levels 

of resource availability at which resilience begins to be reduced (Scheffer et al., 2001), such that stochastic or other 

disturbances and stresses can trigger coral-reef ecosystem 

shifts toward sustained dominance by macroalgal stable 

states. Moreover, the macroalgal overgrowth experimentally stimulated (Smith et al., 2001; Littler et al., 2006b) 

in reduced-grazing/elevated-nutrient treatments demonstrates that ambient nutrient concentrations inhibitory to 

growth under the natural turbulence levels found on coral 

reefs are similar to those reported above for other tropical marine algae. It should be noted that the remote reef 

in the northwestern Hawaiian Islands studied by Smith et 

al. (2001) had nutrient levels at or above the hypothetical 

levels needed to sustain macroalgal growth (i.e., 1.1 M 

DIN and 0.2 M SRP). This system, with its present lack 

of macroalgae and dominance by unbroken thickets of 

three branching and one massive coral species, may be the 

result of overcompensation by intense grazing and, consequently, could be susceptible to a future relative dominance reversal.

Littler et al. (2006a: tbl. 1) give typical baseline herbivorous fi sh assay and population density data contrasting natural Belize Barrier Reef sites of low and high 

herbivory. Based on similar experiments conducted worldwide on coral reefs by a range of workers (Hay, 1984; 

Lewis and Wainwright, 1985; Paul et al., 1987; Sluka 

and Miller, 2001; Littler et al., 2006a), Littler and Littler 

(2006 posited that less than a six hour half-life (50% 

mean loss per 6 h for palatable algae) during a series of 

in situ, midday, assay periods is indicative of a healthy 

level of herbivory for the particular habitat(s) tested. Herbivore abundances also should be enumerated by counting 

numbers of individuals (by species), from midmorning to 

midafternoon throughout a typical day for weather (Littler et al., 2006a, see their table 1), at fi xed distances on 

either side of random replicates of standardized transect 

lines. Video transects are quick; enumeration can be done 

later in the laboratory, and the videos provide a permanent record of the target species (Littler et al., 1986).

FUNCTIONAL INDICATOR GROUPS

The fast growth and turnover rates of fl eshy algae 

compared to other reef organisms suggest their value as 

early-warning indicators of reef degradation. Representatives of ubiquitous algal form/function groups (from 

Littler and Littler, 2006) are increasingly encountered as 

dominants on reefs, particularly those subjected to human 

activities (see Littler and Littler, 2006: fi g. 2).

REEF-BUILDING CORALS (CNIDARIA)

A predominance of diverse corals and calcareous 

coralline algae are universally accepted as the most desirable components of biotic reefs because of (1) their 

three- dimensional architecture, which provides habitats 

for a myriad of other reef organisms (largely responsible 

for much of the heterogeneity/high biodiversity), (2) their 

roles in producing the massive carbonate structure of 

reefs, and (3) their aesthetic qualities. The vertical structure and horizontal canopies of branching forms allow 

abundant populations of shade-dwelling crustose coralline 

algae to co-occur. Reef-building corals, while preyed upon 

by a few omnivorous fi shes and specialist invertebrates 

(e.g., crown-of-thorns sea star), generally achieve dominance under the top-down control of intense herbivory 

(Lewis, 1986; Lirman, 2001) and extremely low nutrient 

concentrations (Bell, 1992; Lapointe et al., 1993). Massive corals are resistant to grazing at the higher levels of 

herbivory (Littler et al., 1989). Hard mound-shaped forms 

show relatively little colony mortality under high grazing 

pressure, even though occasionally rasped by parrotfi shes. 

Contrastingly, some delicately branched corals such as 

Porites porites are quite palatable and readily eaten by 

32_Littler_401-414_Lang.indd 407 2_Littler_401-414_Lang.indd 407 9/24/09 10:33/24/09 10:33
408 • SMITHSONIAN CONTRIBUTIONS TO THE MARINE SCIENCES

parrotfi shes (e.g., Sparisoma viride; Littler et al., 1989; 

Miller and Hay, 1998). Nutrient increases are sometimes 

associated with coral diseases (Harvell et al., 1999, 2002; 

Bruno et al., 2003). As mentioned earlier, numerous corals tolerate elevated nutrient levels (Atkinson et al., 1995; 

Steven and Broadbent, 1997; Bongiorni et al., 2003), but 

their diversity suffers. Conversely, others are physiologically inhibited by increases in nitrate (e.g., Montastrea annularis and Porites porites: Marubini and Davies, 1996), 

ammonium (e.g., Pocillopora damicornis: Stambler et al., 

1991; Muller-Parker et al., 1994), and orthophosphate 

(e.g., Porites compressa: Townsley, cited in Doty, 1969; 

P. damicornis and Stylophora pistillata: Høegh-Guldberg 

et al., 1997). Nutrient inhibition of coral larval settlement 

also has been shown for Acropora longicyathis (Ward and 

Harrison, 1997). During the extensive ENCORE program 

on Heron Island, all increases in nutrient levels adversely 

affected coral reproduction (Koop et al., 2001).

MACROALGAE

With an increase in nutrients, the growth of harmful fl eshy algae is favored over that of the slower-growing 

but highly desirable corals (Genin et al., 1995; Miller and 

Hay, 1996; Lapointe et al., 1997), and the latter become 

inhibited by competition for space and light, increased 

diseases, and physiological inhibition. On healthy oligotrophic coral reefs, even very low nutrient increases may 

exceed critical levels that can shift relative dominances by 

stimulating macroalgal production while inhibiting corals. 

As indicated earlier, large biomass, or standing stocks, of 

slow-growing perennial macroalgae (e.g., rockweeds) can 

develop over time under low inorganic nutrient concentrations (McCook, 1999), and Sargassum spp. can coexist 

with corals in oligotrophic waters by utilizing particulate 

organic sources of nutrients (Schaffelke, 1999). Therefore, 

in this particular situation, large plant biomasses do not 

necessarily indicate detrimentally abundant dissolved nutrients. Filamentous and frondose algae can outcompete 

corals (Birkeland, 1977; but see McCook et al., 2001), 

many of which are inhibited under elevated nutrient levels 

(reviewed in Marubini and Davies, 1996). Fast-growing algae are not just opportunists that depend on disturbances 

to release space resources from established longer-lived 

populations but become the superior competitors (Birkeland, 1977) when provided with suffi cient nutrients. As a 

result, frondose macroalgae as a group are now generally 

recognized as harmful to the longevity of coral reefs because of the linkage between excessive blooms and coastal 

eutrophication (ECOHAB, 1997). Potential competitive 

dominance of fast-growing macroalgae is inferred from 

their overshadowing canopy heights, as well as from inverse correlations in abundances between algae and the 

other benthic producer groups (Lewis, 1986), particularly 

at elevated nutrient concentrations (Littler et al., 1993; 

Lapointe et al., 1997). Macroalgae, such as Halimeda

spp., also gain competitive advantage by serving as carriers of coral diseases (Nugues et al., 2004). The fl eshy 

macroalgal form-group has proven to be particularly attractive to herbivores (see Hay, 1981; Littler et al., 1983a, 

1983b) and only becomes abundant where grazing is decreased or swamped by excessive algal growth (chemically 

defended forms, e.g., Cyanobacteria, are exceptions). Such 

overcompensation by herbivory may explain some of the 

reported cases (Crossland et al., 1984; Szmant, 1997; 

Smith et al., 2001) of specifi c corals surviving high-nutrient reef environments.

CRUSTOSE CORALLINE ALGAE

The predominant members of this indicator group, 

the coralline algae, tend to be slow-growing, competitively 

inferior taxa abundant in most reef systems (Littler, 1972). 

However, they span a spectrum of morphotypes from thin 

sheet-like crusts to thick massive pavements to upright 

branched and columnar coral-like heads that contribute 

to both cementation and bulk. This functional group is 

highly resilient and is able to recover or restore the coralreef system relatively more quickly, given that some crustose coralline algae chemically attract and facilitate the 

survival of coral larvae (Harrington et al., 2004) whereas 

the other two algal functional groups inhibit larval settlement. Because crustose corallines continually slough upper surface layers, they play a key role, as do fi lter-feeding 

corals, in physically preventing the settlement and colonization of many undesirable fl eshy fouling organisms on 

coral reefs (Littler and Littler, 1997). Crustose corallines, 

because of their slow growth rates, tolerate low nutrient 

levels and generally are conspicuous, but not dominant, 

under low concentrations of nutrients and high levels of 

herbivory (Littler et al., 1991). Accordingly, they do well 

under both low and elevated nutrients; that is, most are 

not inhibited by nutrient stress and many are maintained 

competitor free by surface cell layer shedding (Johnson 

and Mann, 1986), even at lower levels of grazing (Littler 

and Littler, 1997). Therefore, crustose coralline algae do 

not require elevated nutrients, as might be inferred from 

the RDM (Figure 1); instead, their rise to dominance is 

largely controlled indirectly by the factors infl uencing 

the abundances of the other groups, primarily corals and 

32_Littler_401-414_Lang.indd 408 2_Littler_401-414_Lang.indd 408 9/24/09 10:33/24/09 10:33
NUMBER 38 • 409

fl eshy macroalgae. The key point is that crustose corallines 

predominate mainly by default (i.e., under conditions of 

minimal competition), where either corals are inhibited by 

elevated nutrients or fl eshy algae are removed by intense 

herbivory. In independent corroboration of the herbivory 

portion of the RDM, a gradient of frondose- to turf- to 

coralline algal groups was closely correlated with escalating herbivory on coral reefs (Steneck, 1989).

LOW-GROWING AND TURF ALGAE

The turf algae are mostly dense fi lamentous and lowgrowing frondose members of all four algal phyla and tend 

to become dominant under minimal inhibitory top-down 

and stimulatory bottom-up controls. Domination by lowgrowing algae suggests desirably low nutrient levels but an 

inadequate herbivory component. Their relatively small 

size and rapid perennation results in moderate losses to 

herbivory at low grazing pressures. They have opportunistic life history characteristics, including the ability to maintain substantial nutrient uptake and growth rates under 

low-nutrient conditions (Rosenberg and Ramus, 1984), 

and also contain an abundance of nitrogen-fi xing Cyanobacteria (Adey and Goertemiller, 1987; Adey, 1998) that 

can enrich other low-growing members of the dense turf 

community. Algal turfs have been shown to be favored 

under reduced nutrient-loading rates (Fong et al., 1987) 

or infrequent nutrient pulses (Fujita et al., 1988) and can 

form extensive horizontal mats.

DISCUSSION

This paper directly addresses the goals of an imperative research agenda (ECOHAB, 1997) by providing a 

management perspective and assessment strategies for the 

mechanisms that initiate and sustain harmful blooms of 

algae that degrade coral-reef ecosystems. The complex interactions of herbivory and nutrients can change gradually 

with no apparent effects to induce subtle declines in resiliency and recoverability of coral/coralline-dominated reef 

systems (Scheffer et al., 2001). As mentioned, these systems then become vulnerable to catastrophic impacts by 

large-scale stochastic disturbances that typically trigger or 

accelerate such low-resilience reef systems (Scheffer et al., 

2001; Bellwood et al., 2004). Most importantly, recovery 

to coral domination cannot occur unless tipping points are 

returned to healthy levels, and even then alternative stable 

states may persist. For example, when catastrophic events 

selectively eliminate the longer-lived organisms in favor of 

early-successional fl eshy algae (Littler and Littler, 1984), 

the settlement of coral planulae is prevented and the algae 

persist as competitively superior states (Birkeland, 1977; 

Lewis, 1986). For completeness, we also point out the obvious devastating effects of toxic spills, carbonate mining, 

land-fi ll, and sediment inundation, some of which also are 

associated with nutrient pollution and algal blooms.

Because of global-scale degradation of coral-reef ecosystems (Ginsburg, 1994; Wilkinson, 1999), it is important to obtain relevant information on tipping points for 

both top-down herbivory (relatively fast acting, acute) and 

bottom-up nutrient controls (slower acting, chronic), both 

of which are reemphasized. As the fi rst approximation, we 

posit that on a healthy reef system, herbivore abundances 

and diversity should be high, and palatable test plants 

should show at least a 50% mean loss per six hours (i.e., 

6 h half-life) during a series of midday in situ assays. 

Table 1 in Littler and Littler (2006 summarizes baseline 

assay and critical fi sh population data of this sort for two 

natural coral-reef zones of low and high herbivory.

Nutrient threshold points (where increasing water 

column nutrients reach critical resilience levels such that 

they reduce recovery from phase shifts) have been widely 

postulated (as 1.0 M DIN and 0.10 M SRP [NTH]; 

Bell, 1992; Lapointe et al., 1993; Bell and Elmetri, 1995) 

for potential macroalgal overgrowth of coral-reef communities. As mentioned earlier, a further useful tipping-point 

indicator is water column chlorophyll a, where levels in 

excess of 0.2– 0.3 g L1 also indicate detrimental overabundances of nutrients (Bell and Elmetri, 1995).

CONCLUSIONS

Assessment protocols for determining and monitoring 

the status of any given coral reef are suggested: these include (a) herbivore population assessments, (b) herbivory 

assays, (c) water column nutrient levels, and (d) standing 

stocks of functional indicator groups. These measurements can reveal quantitative tipping-point levels beyond 

which resilience to and recovery from undesirable phase 

shifts begin to become critically reduced. Tipping-point 

approximations are reviewed and posited both for inorganic nutrients and for herbivory.

This review specifi cally addresses the relatively acute 

top-down effects of herbivory and the more chronic 

bottom -up effects of nutrient enrichment on critical indicator groups of benthic primary producers: reef-building 

corals, crustose coralline algae, dense turf algae, frondose 

macroalgae, and herbivore associates.

32_Littler_401-414_Lang.indd 409 2_Littler_401-414_Lang.indd 409 9/24/09 10:33/24/09 10:33
410 • SMITHSONIAN CONTRIBUTIONS TO THE MARINE SCIENCES

A predominance of massive corals and calcareous coralline algae relative to frondose macroalgae and low-growing 

algae indicates a healthy spatially heterogeneous condition 

refl ecting low nutrients and high herbivory. With a few exceptions, an abundance of frondose macroalgae illustrates 

the least desirable condition of elevated nutrient levels and 

reduced herbivory, possibly refl ecting eutrophication in 

concert with destructive herbivore fi shing practices. A high 

coverage of coralline algae suggests healthy high herbivory 

levels but also suggests problems with elevated nutrients that 

may be inhibitory to some corals. Domination by dense lowgrowing and turf algae indicates desirably low nutrient levels but also suggests an inadequate herbivory component.

From a management perspective, levels of herbivory 

and herbivore populations and of nutrients rank among 

the most useful quantitative indicators of coral-reef resilience and recoverability, whereas the degree of health, 

degradation, and mortality are inferred by the relative 

abundances of functional indicator groups.

The bioassay and indictor group monitoring approaches provide powerful perspectives and essential 

measurement criteria to enable resource managers to protect coral reefs and similar coastal systems from eutrophication, destructive overfi shing, and initiation of harmful algal blooms. Human population growth has always 

been accompanied by changes in land and sea use and 

by increased exploitation of natural resources, attitudes 

that continue to cause broad alterations in the structure 

of coral-reef communities. Unless curbed, anthropogenically induced phase shifts will expand geographically at 

an accelerated pace. However, solutions are available, 

which include the use of Marine Protected Areas, banning 

of destructive fi shing practices (e.g., trapping, poisoning, 

blasting, netting), and regulations protecting keystone herbivorous fi sh species (e.g., parrotfi sh, surgeonfi sh) from 

market exploitation. Fisheries controls must be backed up 

by strategies to regulate the effects of pollution along with 

an international commitment to reduce the emission of 

greenhouse gases and, fi nally, the implementation of longterm strategies to reduce or stabilize the ultimate cause of 

all these stressors, the world’s human population growth.

ACKNOWLEDGMENTS

Support for this work came from a Scholarly Studies 

Grant (Smithsonian Institution, Offi ce of Fellowships and 

Grants), the Caribbean Coral Reef Ecosystems (CCRE) 

Program (administered by Klaus Ruetzler, the Smithsonian Marine Station at Ft. Pierce (Valerie Paul, Head Scientist), and the National Museum of Natural History. This is 

CCRE contribution number 847, supported in part by the 

Hunterdon Oceanographic Research Fund, and SMSFP 

contribution number 763.

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38_Marine_00cover.indd 1 
smithsonian contributions to the marine sciences • number 38

WASHINGTON D.C.

2009

Proceedings of the

Smithsonian 

Marine Science 

Symposium

Edited by 

Michael A. Lang, 

Ian G. Macintyre, and Klaus Rützler

00_FM_i-xii_Lang.indd i 0_FM_i-xii_Lang.indd i 9/24/09 9:19/24/09 9:19
ABSTRACT

Lang, Michael A., Ian G. Macintyre, and Klaus Rützler, editors. Proceedings of the Smithsonian 

Marine Science Symposium. Smithsonian Contributions to the Marine Sciences, number 38, 529 

pages, 217 fi gures, 47 tables, 2009.— The Smithsonian Marine Science Symposium was held on 

15– 16 November 2007 in Washington, D.C. It represented the fi rst major dissemination of marine research results since the establishment of the Smithsonian Marine Science Network (MSN). 

The 39 papers in this volume represent a wide range of marine research studies that demonstrate 

the breadth and diversity of science initiatives supported by the MSN. The fi rst section contains 

an overview of the MSN along with papers describing the multidisciplinary investigations spanning more than 37 years for the four Smithsonian marine facilities that constitute the Network: 

the Smithsonian Environmental Research Center at the Chesapeake Bay, Maryland; the National 

Museum of Natural History’s Smithsonian Marine Station at Fort Pierce, Florida; the Caribbean Coral Reef Ecosystems Program, with its Carrie Bow Marine Field Station in Belize; and 

the Smithsonian Tropical Research Institute in Panama. Subsequent papers represent fi ndings 

by Smithsonian scholars and their collaborators on overarching topics of marine biodiversity, 

evolution, and speciation; biogeography, invasive species, and marine conservation; and forces of 

ecological change in marine systems.

Cover images: (left) Aurelia aurita sea jelly with juvenile carangid jacks in its bell, Carrie Bow 

Cay, Belize; (middle) Dendronephthya soft corals and Anthias school, The Brothers Islands, Red 

Sea, Egypt; (right) grey reef shark Carcharhinus amblyrhynchos, Kingman Reef, Northern Line 

Islands (all photos by Michael A. Lang).

Published by Smithsonian Institution Scholarly Press

P.O. Box 37012

MRC 957

Washington, D.C._20013-7012

www.scholarlypress.si.edu

Library of Congress Cataloging-in-Publication Data

Smithsonian Marine Science Symposium (2007 : Washington D.C.)

 Proceedings of the Smithsonian Marine Science Symposium / edited by Michael A. Lang, Ian 

G. Macintyre, and Klaus Rützler.

 p. cm. — (Smithsonian contributions to the marine sciences, ISSN 0196-0768 ; no. 38)

 Includes bibliographical references and index.

 1. Marine sciences—Congresses. I. Lang, Michael A. II. Macintyre, Ian G. III. Rützler, Klaus. 

IV. Title

 GC2.S57 2007

 578.77—dc22

2009028023

ISSN (print): 0196-0768

ISSN (online): 1943-667X

The paper used in this publication meets the minimum requirements of the American National 

Standard for Permanence of Paper for Printed Library Materials Z39.48– 1992.

00_FM_i-xii_Lang.indd ii 0_FM_i-xii_Lang.indd ii 9/24/09 9:20/24/09 9:20