Ecosystems (2001) 4: 406 417 DOI: 10.

1007/s10021-001-0019-y

ECOSYSTEMS
2001 Springer-Verlag

Spatial Resilience of Coral Reefs

Magnus Nystro m1* and Carl Folke1,2
1

Department of Systems Ecology, Stockholm University, S-106 91, Sweden, and 2Beijer International Institute of Ecological Economics, Royal Swedish Academy of Sciences, Stockholm, Sweden

ABSTRACT
There have been several earlier studies that addressed the inuence of natural disturbance regimes on coral reefs. Humans alter natural disturbance regimes, introduce new stressors, and modify background conditions of reefs. We focus on how coral reef ecosystems relate to disturbance in an increasingly human-dominated environment. The concept of ecosystem resiliencethat is, the capacity of complex systems with multiple stable states to absorb disturbance, reorganize, and adapt to changeis central in this context. Instead of focusing on the recovery of certain species and populations within disturbed sites of individual reefs, we address spatial resiliencethat is, the dynamic capacity of a reef matrix to reorganize and maintain ecosystem function following disturbance. The interplay between disturbance and ecosystem resilience is highlighted. We begin the identication of spatial sources of resilience in dynamic seascapes and exemplify and discuss the relation between ecological memory (biological legacies, mobile link species, and support areas) and functional diversity for seascape resilience. Managing for resilience in dynamic seascapes not only enhances the likelihood of conserving coral reefs, it also provides insurance to society by sustaining essential ecosystem services. Key words: coral reefs; disturbance; resilience; spatial resilience; ecological memory; mobile links; management.

INTRODUCTION
During the last century, humans have gone from being a species with a minor inuence on coral reefs to a dominant source of disturbance (Hatcher 1999). As we move from the Holocene era toward the Anthropocene, a human-dominated biosphere, we have begun to challenge the capacity of coral reefs to perform a number of critical ecosystemlevel functions and to alter their ability to cope with disturbance (Nystro m and others 2000). The deterioration of coral reefs not only diminishes out biological heritage, it also represents the loss of a supporting base for functionally linked resources in a multiple-resource system that holds signicant promise for social and economic development (Moberg and Folke 1999). The signicance of disturbances in the shaping of ecological landscapes and ecosystems has been well

Received 25 February 2000; accepted 31 January 2001. *Corresponding author; e-mail: magnusn@system.ecology.su.se

documented (for example, see Connell 1978). Although our understanding of the effects of relatively small-scale disturbances has increased rapidly, our knowledge of the dynamics of large, infrequent disturbances is still in its infancy (Tumer and Dale 1998; Turner and others 1998; Franklin and MacMahon 2000). Although large-scale perturbations contribute to the development of ecological systems, they are rarely taken into account in management plans (Dale and others 1998). Nor are the combined effects and alterations in disturbance regimes generally included (Paine and others 1998). The effects of disturbance and the potential for the reorganization of ecosystem processes and functions following disturbance (Holling 1986) depend on a number of factors, such as the life histories of the reef participants (for example, Karlson 1999), the sum of their biological and structural legacies (Franklin and others 2000), and the degree of diversity within functional groups (Walker and others 1999). Hence, organisms and interactions between

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Resilience of Coral Reefs organisms that have persisted through the disturbance will be incorporated in the reorganization of the reef. Moreover, reorganization includes the dispersal and migration of animals and plants into the effected zone from adjacent reefs, where currents and the distance between reefs are key components. Thus, the reestablishment of an individual coral reef will depend on a matrix of reefs in the surrounding seascape and their resilience. Hence, the capacity of this matrix to sustain a reef in a coral-dominated state in the face of disturbance needs to be addressed. We need to understand the sources of this capacity, the matrix dynamics, and how such dynamics are affected by human activities. In seascapes increasingly dominated by humans, it will not be sufcient to measure the rates of recovery of individual reefs (Nystro m and others 2000); multiple scale interactions have to be analyzed and understood. The concept of ecological resilience or ecosystem resilience (Holling 1973; Gunderson 2000) is key here. Ecosystem resilience reects the ability of a system to undergo change and yet retain the same controls on function and structure (for example, to remain within a state of coral dominance) (Holling and others 1995). It includes the degree to which the system is capable of reorganizating and building its capacity to adapt to change (Gunderson 2000). The concept of ecosystem resilience has proven useful for addressing the dynamics of complex adaptive ecosystems (Levin 1998). The overall objective of this article is to discuss coral reef conservation in a human-dominated environment using the framework of complex adaptive ecosystems, with a focus on seascape resilience. We will recognize that disturbance and resilience are crucial for coral reef conservation. There is a dynamic interplay between disturbance and resilience and the ways in which humans modify them (Nystro m and others 2000). Disturbance edits the seascape, contributes to ecosystem reorganization, and builds adaptive capacity. But to sustain the positive effects of disturbance, there has to be ecosystem resilience. Otherwise the reestablishment of a disturbed reef will be hampered and the likelihood of phase shifts will increase (see, for example, Done 1992; Knowlton 1992; Hughes 1994; Karlson 1999). It is this interplay that we will address from a spatial resilience perspective. Spatial resilience is the dynamic capacity to cope with disturbance and avoid thresholds at spatial scales larger than individual ecosystems. Dynamic interactions and interdependencies between systems are taken into account by spatial resilience. Moreover, we will address the importance of ecological memory in this

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Figure 1. Spatial and temporal distribution of natural disturbance regimes in coral reefs. Based on Jackson (1991) and Hatcher (1997).

context. Ecological memory is the composition and distribution of organisms and their interactions in space and time and includes the life-history experience with environmental uctuations. Ecological memory is a part of spatial resilience and a critical component in the reorganization of ecosystems. In this paper, we initiate the identication of spatial sources of resilience in dynamic seascapes and emphasize the importance of their inclusion in coral reef management in increasingly human-dominated environments.

CORAL REEFS

IN THE

ANTHROPOCENE ERA

Coral reefs have experienced a large number of natural disturbances throughout their geological history (for example, see Grigg and Dollar 1990) (Figure 1). Disturbances have been a signicant component of coral reef development (Connell 1978), but they have also contributed to habitat destruction and mass mortality (for example, see Stoddart 1972; Jackson 1991; Karlson 1999). Today, most coral reefs exist in an environment dominated by humans where natural disturbance regimes are altered, new anthropogenic substances are introduced, and compounded perturbations are created (Paine and others 1998; Nystro m and others 2000). By prolonging the duration and increasing the frequency of natural disturbances, humans can change pulse events into more persistent, or even chronic, stress. Changes in the frequency, magnitude, duration, and spatial distribution of natural disturbance regimes can be devastating for the dynamics and development of coral reef communities (Nystro m and others 2000). Human alterations of the background reef environment, such as increased levels of nutrients, a

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M. Nystro m and C. Folke processes on different hierarchical levels, functional groups of species, and the variability of habitats (Naeem and others 1994; Done and others 1996; Chapin and others 2000). Ecosystem resilience is not only a buffer to disturbance in the sense of conserving the system, it also provides the sources for reorganization, renewal, novelty, and development after disturbance. Ecosystem resilience maintains exibility and opportunities for responding to environmental change and builds adaptive capacity (Gunderson 2000). Resilience, as it is commonly dened in the coral reef literature (that is, speed of return or recovery time to a single equilibrium), is of limited use for the study of complex adaptive ecosystems (Holling and others 1995), particularly in light of the increasing human inuence on coral reef environments. The concept of ecosystem resilience is of signicance in this context. Peterson and others (1998) have proposed that ecosystem resilience is generated by diverse, but overlapping function within a scale and by apparently redundant species that operate at different scales, thereby reinforcing function across scales. In a recent study of plant attribute diversity, ecosystem function, and resilience, Walker and others (1999) presented evidence that functional similarity between dominant and minor species and among minor species is important for ecosystem resilience. Under changing environmental conditions, ecosystem function is maintained when dominants decline or are lost because functionally equivalent minor species are able to substitute for them. Although this issue is still under debate, it appears that species diversity within functional groups is important to the ability of an ecosystem to buffer disturbance and maintain functions under changing environmental conditions (Nystro m and others 2000; McClanahan and others forthcoming). The importance of diversity within functional groups for coral reef resilience can be illustrated on all scales, from the level of genes to biogeographic regions. On a cellular level, for example, studies have shown that some Caribbean scleractinian corals may accommodate a multiple-species (or strains) zooxanthellae community (Rowan and Knowlton 1995; Baker and Rowan 1997; Rowan and others 1997). The composition of these microcommunities follows a gradient of environmental irradiance, with corals hosting the most optimal symbionts for the prevailing conditions (Rowan and Knowlton 1995; Rowan and others 1997). This mode of adjustment to environmental change is a rather rapid mechanism (less than 1 year) and increases the ability of corals to respond to change.

reduction in predatory and herbivorous sh abundance, and the release of toxic compounds, can have severe effects on the ability of reef communities to cope with new disturbances superimposed on those already existing (Brown 1997). Because most reef-building corals are virtually life-dependent on the photosynthesis of their symbiotic microalgae (zooxanthellae), periods of disruption (or instability) in this relationship have a major inuence on the corals health and survival (MullerParker and DElia 1997). For example, low levels of continuous pollution may cause physiological stress that can lead to reduced growth and reproduction (Loya 1990) as well as impaired defense against diseases (Peters 1997) and competitors (Brown 1997; Goreau and others 2000). By altering background conditions, the capacity of the reef to reorganize and reestablish after disturbance can be severely hampered (Loya and Rinkevich 1980; Loya 1990; Hughes 1994; Goreau and others 2000). Humans also increase the spatial distribution of disturbances. For instance, disturbances that occur on a local scale can interact and generate effects on regional (for example, eutrophication, pollution, overshing) or even global scales (for example, dust, global warming) (Buddemeier and Smith 1999; Hoegh-Guldberg 1999; Wilkinson 1999; Shinn and others 2000). Hence, humans not only tend to alter natural disturbance regimes and introduce new stresses, they also change ecosystem dynamics and resilience (Wilkinson 1999; Nystro m and others 2000). Their impact resulted in a worldwide decline in reef health (Connell 1997) and prompted questions about the long-term sustainability of reefs (Brown 1987).

ECOSYSTEM RESILIENCE

OF

CORAL REEFS

In the past, tropical coral reefs were viewed as stable ecosystems in areas with minor environmental uctuations (Odum and Odum 1955; Johannes 1975). However, current ecological paradigms suggest that coral reefs, just like other ecosystems, are complex adaptive systems (Holling and others 1995; Levin 1998) with nonlinear dynamics and multiple stable states (Hughes 1989, 1994; Done 1992; Knowlton 1992). The ability of a reef community to remain within its state, or stability domain, is determined by ecosystem resilience, or the amount of disturbance that can be absorbed by the coral reef ecosystem before a locally stable equilibrium shifts into another stability domain (Holling 1986). The buffering capacity to disturbance is determined by characteristics such as genetic variability, the number of species involved in ecological

Resilience of Coral Reefs Hence, physiological adaptation is not the only mechanism for corals to cope with environmental heterogeneity (Rowan and others 1997), and a shift toward more temperature resistant species is not the only response of a coral community. Depending on the number of zooxanthellae species (or strains) available, the response to change may differ between coral species (Muller-Parker and DElia 1997). This suggests that corals that host several species (or strains) of zooxanthellae are more resilient to these changes. When functional groups and diversity within functional groups are reduced, the capacity of the reef to absorb further disturbance is reduced (Holling and others 1995). For example, coral reefs with low diversity within functional groups (for example, Caribbean reefs) may still maintain ecological functions (Kinzie 1999); but when faced with an additional disturbance a critical threshold may be reached, shifting the ecosystem into another stability domain (Nystro m and others 2000). This seems to be the case particularly when a reef is subject to a disturbance that leaves large amounts of substratum available (for example, see Knowlton 1992) or when human-induced chronic stress slowly changes environmental conditions, thereby suppressing species assemblages of the reef community and/or favoring new species assemblages (Hughes 1994; Petraitis and Latham 1999). On a regional level, loss of ecosystem resilience can be illustrated by a case from Jamaica, frequently described in the literature, where the coral reefs shifted from being dominated by coral to become algae dominated (for example, see Lessios and others 1984; Carpenter 1990; Knowlton 1992; Hughes 1994). Overhavesting of predatory and resource-competing herbivorous shes in the Caribbean resulted in a dramatic expansion of the sea urchin (Diadema antillarium) population. Overshing led to reduced within-group diversity of the grazers (that is, reduced resilience due to loss of redundancy). In 1983 84, a species-specic pathogen caused a 95%99% reduction in the sea urchin population in its geographic range (Lessios and others 1984; Carpenter 1990). Although herbivorous sh populations increased (Carpenter 1990), the grazer group could not keep pace with invading algae in the absence of Diadema and the major sh species exploited by sheries. A thick mat of eshy algae colonized free space, inhibited coral recruitment, and even overgrew larger coral colonies. A phase shift to another stability domain took place. This shift was probably supported by the chronic input of nutrients into the surrounding coastal waters favoring algal growth (Bell 1992; Lapoint

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1997). Cases from other parts of the world have also described phase shifts from coral to algae communities (see review by Done 1992; McClanahan and Muthiga 1998; McCook 1999). Paine and others (1998) proposed that the Jamaican regime shift would never have developed if the disturbance events had occurred individually at intervals appropriate to the capacity of the coral community to reorganize and reestablish following disturbance.

SPATIAL RESILIENCE

OF

CORAL REEFS

There is ample literature on coral reef recovery after disturbance, particularly at the level of individual reefs. Although recovery following disturbance can be delayed (for example, see Loya 1990; Wilkinson 1999; Karlson 1999), it has generally been assumed that recovery will eventually occur. The sources of reorganization and reestablishment of reef organisms and community interactions in the seascape have, to a lesser extent, been investigated. In the following section, we review spatial links in the seascape that support reef resilience and development following disturbance.

Currents and Recruitment

Reorganization of a coral reef is related to the degree of openness to its surrounding. Openness depends on whether the reef is located in a shallow or semi-enclosed basin, on the margin of a continental shelf, or in the open ocean (for example, atolls). Openness is supported, or discouraged, by the prevailing currents (Roberts 1997). The degree to which these currents link areas depends on their magnitude and direction, the distance between ecosystems, and the inuence of primarily climatic disturbance regimes. The magnitude of variation in recruitment of corals at different spatio-temporal scales is poorly documented (Dunstan and Johnson 1998). Some authors suggest that the recruitment of corals, shes, and other reef organisms that display a pelagic larval phase depends mainly on the retention of recruits from the parental reef or reefs within a relatively limited range (for example, see Sammarco and Andrews 1988; Jones and others 1999; Swearer and others 1999; Cowen and others 2000; Barber and others 2000)a biological legacy approach. Others have attributed the geographical distribution pattern of corals to the ability of larvae to disperse between distant reefs and geographic regions (for example, see Veron 1985, 1995; Roberts 1997). Large-scale disturbance (for instance, hurricanes, severe El Nin o years, volcanic eruptions and so on)

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M. Nystro m and C. Folke This may explain the observation that although there are similar functional groups in the Caribbean and in the Indo-Pacic, there are fewer species within functional groups in the Caribbean and thus a reduced ability to buffer disturbance and reorganize (McClanahan and others forthcoming).

is likely to cause mass mortality. Such events reduce the chances for successful self-seeding and increase the importance of larvae import. Source and sink reefs are often discussed in this context. A source reef is an upstream reef that exports propagules of coral and other reef-related organism to downstream sink-reefs (Done 1995; Roberts 1997, 1998). Source reefs are important for genetic exchange between populations and for supplying propagules for recolonization after disturbance (Benzie and others 1995; Roberts 1997, 1998; McClanahan and others forthcoming). Coral larvae are poor swimmers (Chia and others 1984). Therefore, dispersal and settlement patterns of coral are to a large extent determined by prevailing currents and hydrological and oceanic conditions. Reef-building corals display different modes of reproduction (see review by Harrison and Wallace 1990; Richmond 1997), making a source reef within range for some species but out of reach for others (Hughes and others 1999). For example, asexual-reproducing corals (for example, by fragmentation) are generally very locally dispersed (Sammarco 1981; Done and Potts 1992), whereas species that reproduce sexually (that is, by the release of gametes or fully developed larvae) may disperse over much greater distances (Harrison and Wallace 1990; Ayre and Dufty 1994; Benzie and others 1995; Richmond 1997; Wilson and Harrison 1998). The interspecic variation in dispersal between corals will have a substantial inuence on the composition of coral species in the reorganization phase following disturbance. Disturbance effects are often species-specic, which will inuence coral species composition on the source reef and thus determine larvae composition available for export (Goreau and others 2000). Hence, alterations of functional diversity and resilience in upstream source reefs will have an inuence on reorganization elsewhere (Richmond 1993). The pattern of currents at different scales plays an important role in the diversity and resilience of an area. For example, the recruitment rate in the Caribbean is lower compared to many other areas (Hughes and others 1999). The shallow nature of the Caribbean Sea area, its relatively small size, and the relatively strong continental inuences make it vulnerable to anthropogenic impacts and compounded perturbations (Roberts 1993; Veron 1995; Paine and others 1998). On a regional scale, it suggests that the Caribbean is more isolated in terms of species or larvae import from areas outside the basin compared to other biogeographic regions, such as the Indo-Pacic region (Chadwick-Furman 1996; Birkeland 1997; Brown 1997; Connell 1997).

Building Spatial Resilience by Coral Reef Networks

Individual reefs with high resilience may be subject to mass mortality when faced with large-scale disturbance. In such situations, local ecological functions can only be maintained by resilience of a matrix of reefs in the seascape. For example, Jamaica had reefs located in bays protected from hurricanes and similar disturbances. Such storm-protected reefs were important sources for the reorganization of wind- and wave-exposed reefs hit by hurricanes. However, over the last few decades, overshing and impacts from land-use transformation, industrial development, and urbanization have degraded most of those reefs. As a consequence, the recovery rate of exposed reefs after relatively recent Hurricanes Allen (1980) and Gilbert (1988) has been much slower than expected (Goreau and others 1997). A reef network increases not only the chances for larger disturbance events to be buffered within the seascape, but also for destroyed reefs to be naturally restored by settlers and community interactions from surrounding reefs. Managing coral reefs from a matrix perspective entails support for the presence of a larger and more diverse species pool in which both primary and secondary successional organisms and the interactions between them are represented. A crucial issue for management is the degree to which the mosaic of coral reefs can be modied by disturbance and chronic stress without losing its capability to maintain coral ecosystem functions and support the reorganization and reestablishment of deteriorated individual reefs. We refer to this capacity as spatial resilience. Spatial resilience addresses the dynamic capacity of a reef matrix to avoid thresholds at a regional scale. Larger-scale processes, such as currents, play a critical role in determining spatial resilience by transporting nutrients, plankton, larvae, and juveniles. However, the same currents have a substantial effect on the distribution and dispersal of waterborne disturbances such as sediments, diseases, pollutants, and sewage, which may hamper the survival and recruitment of corals. Thus, processes that support spatial resilience may at the same time also expose the system to chronic stress and alter disturbance regimes in a way that may challenge

Resilience of Coral Reefs

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Figure 2. Conceptual gure of ecological memory (legacies, mobile links, support areas) of coral reefs.

the resilience of the area. This highlights the need for management plans for coral reefs to account for human activities outside the reef and to consider the impacts of such activities on functional diversity and resilience at the seascape level. It also underscores the need to understand ecological components and their interactions that contribute to resilience at broader scales than individual reefs (Peterson and others 1998).

ECOLOGICAL MEMORY RESILIENCE

AND

SPATIAL

Done and others (1991) state that given the importance of corals as framework builders, questions of whether or not damaged reefs return to coral dominance, the rates of such return, and the nature of the regenerated coral community, are of major interest. In this section, we will address this statement in the context of spatial resilience for reorganization following disturbance, focusing on what we refer to as the ecological memory. Ecological memory is the composition and distribution of organisms and their interactions in space and time, and includes the life-history experience with environmental uctuations. Memory reects the historical foundation of ecosystem resilience and is a key component of spatial resilience. Ecological memory consists of at least three basic and interacting parts (Figure 2). The rst

part includes biological legacies (for example, see Franklin and MacMahon 2000) that is, species and patterns that persist within an area hit by disturbanceand structural legaciesthat is, remaining dead structures such as coral framework and rubble. Among the most important legacies are the framework-building corals. The second is the mobile link (Gilbert 1980; Myers 1993; F. Moberg and others unpublished)that is, species that spread passively from one area to another (such as larvae, which spread through currents), or move actively between areas such as several species of sh and sea urchin. For example, schools of herbivorous shes accelerate the reorganization of a disturbed area by grazing down algae and thereby making room for coral larvae to settle (reviewed by Glynn 1990). The third is the support area for the mobile linkthat is, reefs and habitats such as sea grass beds and mangroves in the seascape matrix. Each of these components consists of several functional groups interacting as a dynamic ecological community in the seascape. The vulnerability of functional groups seems to be related to the redundancy of species within each group (Nystro m and others 2000; McClanahan and others forthcoming) and suggests that coral reef ecosystems have less resilience to disturbance when functional groups have low diversity. The rates of reorganization, the level of similarity

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M. Nystro m and C. Folke

Table 1. Examples of Functional Groups of Organisms and Their Role in Ecological Memory
Components of Ecological Memory Biological legacies Examples of Major Functional Groups Framework-builders (corals and coralline algae) Herbivores (sh and sea urchins) Predators (corallivor- and pelagic sh)

Examples of Functions Internal input for reorganization Species pool for dispersal, habitat, food resource Keep substratum open for recruitment and avoid algal overgrowth of adult corals Maintain high functional diversity of herbivores, dispersal of coral fragments and zooxanthellae, avoid competitive release of other organisms (for example sea urchin) Induce coral larvae settlement Add habitat complexity, substratum for settlement of larvae External input for reorganization Provision of settling organisms, genetic input Keep substratum open for recruitment, avoid algal overgrowth of adult corals, input of nutrients (feces) Maintain functional diversity, avoid competitive release of bioeorders, dispersal of coral fragments and zooxanthellae Export of organisms of different functional groups with different or similar life histories

Structural legacies

Settling facilitators (bacteria, diatoms, coralline algae, worms) Dead coral framework and coral rubble

Passive mobile links Active mobile links

Larvae of various functional groups (coral and sh) Herbivores (sh and sea urchins)

Predators (corallivor- and pelagic sh)

Support areas

Framework-builders and other reefassociated organisms

between the old and the new reef, and the resilience of the reef (that is, whether or not it will remain in the same stability domain) are a function of the extent of ecological memory. Thus, ecological memory is the combination of several functional groups of species (for example, predators, herbivores, reef-builders, decomposers), their dynamic interactions, and within functional group diversity. Ecological memory is internal (within reef) and external (between reefs and other habitats in the seascape matrix). Examples of species interactions and processes that contribute to ecological memory are provided in Table 1. The presence and dynamics of this network of interacting species is the result of previous experience and accumulated information in the life history of species to environmental change. For example, Pearson (1981) noted the importance of life history (for example, larval dispersal, availability, and settlement), microhabitat availability, diversity, and biological interactions for the reestablishment and survival of corals. In the words of Lockwood and Pimm (2000): Communities are not just the result of processes that operate today, but are also the products of a long, capricious history.

Human Alteration of Ecological Memory

Although successional mechanisms display very complex patterns (for example, see Connell and Slatyer 1977), evaluation of evidence in coral communities has indicated that there is a certain predictability in species replacement over time (Karlson 1999). It should be noted, however, that primary and secondary successional patterns in coral reefs are not as obvious as they are in many other ecosystems (Karlson 1999). Nonetheless, patterns of replacement over time may become radically altered when the ecological memory of the seascape is impacted by human use and abuse (Nystro m and others 2000). For example, pollution, eutrophication, sedimentation, overshing, and the introduction of new species may favor the development of new successional directionsfor example, toward algae dominance or bioeroder communities (Done 1992; Hughes 1994; Done and others 1996). Once such a phase shift has occurred, new species interactions can establish. This suggests that former interactions may get weaker over time (Lockwood and Pimm 2000) or even become locally extinct. This change will most likely have an impact on

Resilience of Coral Reefs ecosystem structure and performance (in terms of productivity, nutrient retention, grazing, species compositions, and diversity) and the delivery of ecosystem services. In theory, it also increases the risk that phase shifts become less reversible. As diversity within and between functional groups of biological legacies, mobile links, and support areas in the seascape is reduced, resilience is also reduced, and disturbance effects are likely to become more severe. Thus, whether a coral reef will be able to cope with the disturbance and then renew and reorganize itself afterward is strongly inuenced by the presence and diversity of the remaining ecological memory in the surrounding seascape mosaic. In the following section, we will present examples of ecological memory in terms of active mobile links and other species that facilitate reorganization.

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Species that Facilitate the Reorganization of Coral Reefs

A crucial component of the ecological memory of reefs is the presence of species that support coral growth and recolonization at the site of disturbance. These species perform functions that enhance the reorganization process after disturbance (Connell and Slatyer 1977). They serve as facilitators between biological legacies, the nearby environment, and mobile links such as coral larvae. For example, settling preferences differ among coral species. Some larval species of coral will only settle if the surface is colonized by, for example, diatoms, bacteria, or lamentous or crustose coralline algae (Morse and others 1988; Harrison and Wallace 1990; Hunte and Wittenberg 1992; Richmond 1997). Despite the absence of clear scientic evidence, it appears that these organisms serve as important facilitators for the reorganization process. The symbiotic zooxanthellae association is central for the existence of all reef-building coral communities, and any environmental factor that affects this mutualistic relationship affects the whole community (Richmond 1993). Zooxanthellae can be established in new corals by inheritance from the parental colony to the egg or planula larvae (sexual reproduction), by new polyps/fragments (asexual reproduction), or by capturing zooxanthellae from the surrounding waters (Harrison and Wallace 1990; Muller-Parker and DElia 1997). The acquisition of zooxanthellae by juvenile corals implies not only new genetic combinations of host/symbiont that differ from those of the parents but also the formation of novel associations with new species (or strains) of zooxanthellae (Buddemeier and Fautin 1993; Baker and

Rowan 1997). This diversication may contribute to an enhanced ecological memory among the corals and improve functional redundancy in the face of future environmental change. When corals are stressed, they may expel zooxanthellae (or the algae may lose pigments), which results in partial or complete bleaching (reviewed by Glynn 1993). When partially bleached, colonies may recover by proliferation of residual zooxanthellae (Harrison and Wallace 1990; Muller-Parker and DElia 1997). If there is complete bleaching, the source of symbionts for reorganization is unknown. It has been suggested that even severely bleached corals contain a small number of zooxanthellae, or that free-living zooxanthellae may be captured by corals after the bleaching event (Buddemeier and Fautin 1993; Muller-Parker and DElia 1997). The availability of zooxanthellae is a crucial part of the ecological memory that facilitates reorganization after disturbance and contributes to sustaining the reef in a coral-dominated stability domain. Grazing by herbivorous shes and sea urchins plays a central role in the dynamics and resilience of modern coral reefs. They facilitate the reestablishment of corals by grazing off colonizing algae that would otherwise prevent coral larvae from settling or overgrow adult corals (Hay 1984; Lessios and others 1984; Glynn 1990). Grazing organisms are not only signicant factors for reorganization, they are also important during later successional stages of the reef. For example, if the number of grazers is reduced, algae may increase in abundance and reach a size that is unpalatable to herbivores (McClanahan and others 1999), causing the system to slide into another stability domain of algae dominance. Thus, the presence of a functional group of grazers is an important component of the ecological memory of reefs, just as the functional group of corals provides a supply of larvae to disturbed reefs.

Mobile Links and the Reorganization of Coral Reefs

Mobile links are species that provide, or support, essential functions by connecting one area to another. There are passive mobile links, such as the larvae transported by currents. Despite being more or less planktonic, they are able to actively select sites that are appropriate for settling (see review by Harrison and Wallace 1990). There are also active mobile links, such as bees, moths, bats, hummingbirds, and bears, which inuence dispersal, reproductive success, and productivity for a wide array of terrestrial plants (Baskin 1997). Active mobile linksthat is, species that move by themeselves between habitatssupport spatial resilience by in-

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M. Nystro m and C. Folke the development of coral reefs on otherwise unstable substrata. This implies that these worms are not only important as mobile links in transporting corals from one area to another but may also serve as important facilitators in initiating the larger reefbuilding process. Large predator shes connect coral reefs with adjacent mangroves and seagrass beds (Ogden and Gladfelter 1983; Parrish 1989). These large carnivores are the primary target of reef sheries and are easily overshed (Roberts 1993; Jennings and Polunin 1996). Corallivor and scraping shes might contribute to moving coral fragments when foraging on living corals. Overshing of large sh predators may cause competitive release of their prey, as witnessed in expanding sea urchin populations. This was the case in the Caribbean (Hay 1984; Lessios and others 1984), the Red Sea (Ormond and others 1973), and Kenya (McClanahan and Muthiga 1988), where urchins outcompeted herbivorous shes, with a consequent loss of resilience within the functional group of grazers. Thus, large sh predators of coral reefs with large home ranges link reefs, regulate functions, maintain resilience, and may indirectly facilitate reorganization following disturbance. It is such interactions within and between functional groups of facilitating species and mobile links that contribute to the ecosystem resilience of coral reefs.

creasing the connectivity between habitats and ecosystems. They speed up the reorganization process and can be critical in sustaining ecosystems within a stability domain (F. Moberg and others unpublished). Mammals and shes are examples of active mobile links. Their behavior and life history are part of the ecological memory of reefs. For example, under normal conditions, zooxanthellae are likely to be found in quite low concentrations over reefs (Muller-Parker and DElia 1997). Predatory and herbivorous shes concentrate and transport zooxanthellae within (for example, between colonies or different reef zones) and between reefs. The success of indirect acquisition of zooxanthellae by juvenile corals can be supported by the ingestion of fecal material arriving from predatory and herbivorous shes that contains zooxanthellae (Mu ller-Parker and DElia 1997), from fragments caused by shes foraging on neighboring corals (Parker 1984), or from zooplankton prey containing zooxanthellae (Mu ller-Parker and DElia 1997). Migrating herbivorous organisms are among the most important mobile links in coral reefs, providing open substratum for the recolonization of corals and avoiding overgrowth by algae. As with rivermigrating salmon, it has been suggested that high densities of migrating herbivorous coral reef shes provide essential nutrients to primary producers in nutrient-poor areas or transport limiting nutrients from one part of the reef to another (for example, see Meyer and Schultz 1985). For example, juvenile French and white grunt feed at night in surrounding sea grass beds and then excrete and defecate nutrients over the reef during the day (Meyer and others 1983; Meyer and Schultz 1985). Fish species, including some damselsh, may also contribute with essential minerals captured outside the reef system (Geesey and others 1984). However, because of the increased release of nutrients due to human activities, the function of shes as mobile fertilizers may be more essential in remote and unexploited areas, such as atolls or barrier reefs. In contrast to human-induced chronic nutrient stress, shes provide a pulse of nutrient input in a limited area. In a recent publication, Chisholm and Kelley (2001) showed that marine eunicid worms can gather and glue together lumps of corals to form a large and secure habitat for themselves. By doing so, the worms create suitable conditions for new corals to settle and other organisms to follow. The authors argue that removing and replanting of corals might be a plausible explanation for patchy distribution of benthic communities in general and

CONCLUSION
Coral reef dynamics are increasingly inuenced and driven by human activities. Many of the worlds coral reefs that were once assumed to be pristine are now showing signs of overshing (McManus and others 2000) and may have been overshed even before scientic investigations began (Jackson 1997). Changes in the magnitude, frequency, and duration of disturbance regimes and alterations of ecosystem resilience, often as a consequence of human actions, pose major challenges to the management of reefs for conservation and sustainable use (Nystro m and others 2000). In addition, reefs with no obvious human impacts may suffer from indirect human inuences at scales reaching far beyond the border of the individual reef, such as global warming, increased levels of carbon dioxide (Wilkinson 2000), and dust (Shinn and others 2000). Complex interactions of a number of factors can lead to a loss of ecosystem resilience that is difcult to detect until a reef shifts to another stability domain after a disturbance that previously could have been absorbed (McCook 1999). Thus, what we experience as a fast transition (within months) (for

Resilience of Coral Reefs example, see Ostrander and others 2000) from one state to another might be the result of a long-term gradual change over years, decades, or even centuries (Nystro m and others 2001). Clearly, focusing on rates of recovery in disturbed sites will provide only partial directions for effective management and conservation. Coral reef management for conservation must expand beyond individual reefs towards cross-scale interactions within a matrix of reefs in dynamic seascapes and to an understanding of how the shifting mosaic of reefs contributes to ecosystem resilience. In this article, we have outlined a theoretical perspective that emphasizes the signicance of spatial resilience for the reorganization and development of coral reefs following disturbance. We have highlighted the dynamic interplay between disturbance regimes and ecosystem resilience, and stressed the signicant role played by the ecological memory of biological legacies, mobile links, and support areas in the seascape. Managing for ecosystem resilience in dynamic seascapes has the potential to not only enhance the likelihood of conserving reefs but also to increase the likelihood that essential coral reef ecosystem services will be sustained for society (Moberg and Folke 1999). The dynamic seascape approach presents great challenges in developing, combining, and fostering our knowledge of complex ecosystems and creating incentives and frameworks for intersectoral collaboration. This perspective also provides opportunities for directing socioeconomic development and integrated coastal zone management toward sustainability.

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ACKNOWLEDGMENTS
We thank F. Moberg, K. Fabricius, T. McClanahan and two anonymous reviewers for valuable comments on the manuscript. We are also grateful to Jan Bengtsson, Thomas Elmqvist, Fredrik Moberg, colleagues of the Resilience Alliance, and others who, during creative and enlightening discussions, contributed their ideas to this paper. M. N.s work is funded by Sida/SAREC (Swedish International Development and cooperation Agency). C. F.s work is partly supported by the Pew Charitable Trusts. This article is a product of the Resilience Network of the University of Florida (Gainesville, Florida, USA) and the Beijer Institute, (Stockholm, Sweden), supported by the John D. and Catherine T. MacArthur Foundation, USA, and the Marcus Wallenberg Foundation for International Cooperation in Science, Sweden.

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