Connectivity,regime shifts and the resilience of coral reefs

Connectivity of larvae among metapopulations in open marine systems can be a double-edged sword, allowing for the colonization and replenishment of both desirable and undesirable elements of interacting species-rich assemblages. This article studies the effect of recruitment by coral and macroalgae on the resilience of grazed reef ecosystems. In particular, we focus on how larval connectivity affects regime shifts between alternative assemblages that are dominated either by corals or by macroalgae. Using a model with bistability dynamics, we show that recruitment of coral larvae erodes the resilience of a macroalgae-dominated ecosystem when grazing is high, but has negligible effect when grazing is low. Conversely, recruitment by macroalgae erodes the resilience of a coral-dominated ecosystem when grazing is low, leading to a regime shift to macroalgae. Thus, spillover of coral recruits from highly protected areas will not restore coral cover or prevent flips to macroalgae in the surrounding seascape if grazing levels in these areas are depleted, but may be pivotal for re-building coral populations if grazing is high. Fishing restrictions and the re-introduction of herbivores should therefore be a prime conservation objective for preventing undesirable regime shifts. Connectivity by some components of coral reef assemblages (e.g., macroalgae, pathogens, crown-of-thorns starfish) may be detrimental to sustaining reefs, especially where overfishing and other drivers have eroded their resilience, making them more vulnerable to a regime shift.     

Regime shifts in marine ecosystems: detection, prediction and management

Regime shifts are abrupt changes between contrasting, persistent states of any complex system. The potential for their prediction in the ocean and possible management depends upon the characteristics of the regime shifts: their drivers (from anthropogenic to natural), scale (from the local to the basin) and potential for management action (from adaptation to mitigation). We present a conceptual framework that will enhance our ability to detect, predict and manage regime shifts in the ocean, illustrating our approach with three well-documented examples: the North Pacific, the North Sea and Caribbean coral reefs. We conclude that the ability to adapt to, or manage, regime shifts depends upon their uniqueness, our understanding of their causes and linkages among ecosystem components and our observational capabilities.     

Millennial-scale change in the structure of a Caribbean reef ecosystem and the role of human and natural disturbance

Caribbean coral reefs have transformed into algal-dominated habitats over the past half-century, but the role of specific anthropogenic drivers is unresolved due to the lack of ecosystem-level data predating human disturbance. To better understand the extent and causes of long-term Caribbean reef declines, we produced a continuous 3000-yr record of the ecosystem state of three reefs in Bocas del Toro, Caribbean Panama. From fossils and sediments obtained from reef matrix cores, we tracked changes in reef accretion rates and the taxonomic and functional group composition of fish, coral, urchin, bivalve and benthic foraminifera. This dataset provided a comprehensive picture of reef community and environmental change. At all sites, reefs shifted from systems with greater relative abundance of herbivorous fish, epifaunal suspension feeding bivalves and Diadema urchins to systems with greater relative abundance of micropredator fish, infaunal bivalves and Echinometra urchins. These transitions were initiated a millennium ago at two less-degraded reefs fringing offshore islands and ~250 yr ago at a degraded patch reef near the continental coast. Ecosystem shifts were accompanied by a decline in reef accretion rates, and at the patch reef, a decline in water quality since the 18th century. Within all cores, synchronous increases in infaunal bivalves and declines in herbivorous fish regardless of water quality suggest a loss of hard substrate and increasingly hypoxic sediment conditions related to herbivore loss. While the early timing of ecosystem transitions at the fringing reefs implicates large-scale hydrological change, the more recent timing of change and loss of water quality at the patch reef implicates terrigenous runoff from land-clearing. Our whole-ecosystem reconstruction reveals that reef ecosystem deterioration appears to follow a predictable trajectory whether driven by natural or anthropogenic disturbances and that historical local human activities have quickly unraveled reefs at a scale similar to longer-term natural environmental change.     

Regime Shifts in the Anthropocene: Drivers,Risks, and Resilience

Many ecosystems can experience regime shifts: surprising, large and persistent changes in the function and structure of ecosystems. Assessing whether continued global change will lead to further regime shifts, or has the potential to trigger cascading regime shifts has been a central question in global change policy. Addressing this issue has, however, been hampered by the focus of regime shift research on specific cases and types of regime shifts. To systematically assess the global risk of regime shifts we conducted a comparative analysis of 25 generic types of regime shifts across marine, terrestrial and polar systems; identifying their drivers, and impacts on ecosystem services. Our results show that the drivers of regime shifts are diverse and co-occur strongly, which suggests that continued global change can be expected to synchronously increase the risk of multiple regime shifts. Furthermore, many regime shift drivers are related to climate change and food production, whose links to the continued expansion of human activities makes them difficult to limit. Because many regime shifts can amplify the drivers of other regime shifts, continued global change can also be expected to increase the risk of cascading regime shifts. Nevertheless, the variety of scales at which regime shift drivers operate provides opportunities for reducing the risk of many types of regime shifts by addressing local or regional drivers, even in the absence of rapid reduction of global drivers.     

Marine regime shifts: drivers and impacts on ecosystems services

Marine ecosystems can experience regime shifts, in which they shift from being organized around one set of mutually reinforcing structures and processes to another. Anthropogenic global change has broadly increased a wide variety of processes that can drive regime shifts. To assess the vulnerability of marine ecosystems to such shifts and their potential consequences, we reviewed the scientific literature for 13 types of marine regime shifts and used networks to conduct an analysis of co-occurrence of drivers and ecosystem service impacts. We found that regime shifts are caused by multiple drivers and have multiple consequences that co-occur in a non-random pattern. Drivers related to food production, climate change and coastal development are the most common co-occurring causes of regime shifts, while cultural services, biodiversity and primary production are the most common cluster of ecosystem services affected. These clusters prioritize sets of drivers for management and highlight the need for coordinated actions across multiple drivers and scales to reduce the risk of marine regime shifts. Managerial strategies are likely to fail if they only address well-understood or data-rich variables, and international cooperation and polycentric institutions will be critical to implement and coordinate action across the scales at which different drivers operate. By better understanding these underlying patterns, we hope to inform the development of managerial strategies to reduce the risk of high-impact marine regime shifts, especially for areas of the world where data are not available or monitoring programmes are not in place.     

Coral reef disturbance and resilience in a human-dominated environment

Facing a human-dominated world, ecologists are now reconsidering the role of disturbance for coral reef ecosystem dynamics. Human activities alter the natural disturbance regimes of coral reefs by transforming pulse events into persistent disturbance or even chronic stress, by introducing new disturbance, or by suppressing or removing disturbance. Adding these alterations to natural disturbance regimes will probably result in unknown synergistic effects. Simultaneously, humans are altering the capacity of reefs to cope with disturbance (e.g. by habitat fragmentation and reduction of functional diversity), which further exacerbates the effects of altered disturbance regimes. A disturbance that previously triggered the renewal and development of reefs might, under such circumstances, become an obstacle to development. The implications of these changes for reef-associated human activities, such as fishing and tourism, can be substantial.     

Spatial Resilience of Coral Reefs

There have been several earlier studies that addressed the influence 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 resilience—that is, the capacity of complex systems with multiple stable states to absorb disturbance, reorganize, and adapt to change—is central in this context. Instead of focusing on the recovery of certain species and populations within disturbed sites of individual reefs, we address spatial resilience—that 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 identification 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. Received 25 February 2000; accepted 31 January 2001.     

Catastrophic regime shifts in coral communities exposed to physical disturbances: Simulation results from object-oriented 3-dimensional coral reef model

A 3-dimensional individual-based model, the ReefModel, was developed to simulate the dynamical structure of coral reef community using object-oriented techniques. Interactions among functional groups of reef organisms were simulated in the model. The behaviours of these organisms were described with simple mechanistic rules that were derived from their general behaviours (e.g. growing habits, competitive mechanisms, response to physical disturbance) observed in natural coral reef communities. The model was implemented to explore the effects of physical disturbance on the dynamical structure of a 3-coral community that was characterized with three functional coral groups: tabular coral, foliaceous coral and massive coral. Simulation results suggest that (i) the integration of physical disturbance and differential responses (disturbance sensitivity and growing habit) of corals plays an important role in structuring coral communities; (ii) diversity of coral communities can be maximal under intermediate level of acute physical disturbance; (iii) multimodality exists in the final states and dynamic regimes of individual coral group as well as coral community structure, which results from the influence of small random spatial events occurring during the interactions among the corals in the community, under acute and repeated physical disturbances. These results suggest that alternative stable states and catastrophic regime shifts may exist in a coral community under unstable physical environment.     

Mid-Holocene coral community data as baselines for understanding contemporary reef ecological states

Land-use changes and associated deteriorations in water quality are cited as major drivers of marine ecosystem change, and can modify community abundance and diversity on coral reefs. This study uses palaeoecological data derived from a mid-Holocene age coral reef in the Wet Tropics region of Australia's Great Barrier Reef to develop a record of coral community composition and diversity, from a period that significantly pre-dates European settlement in the region. Major changes in catchment sediment and nutrient yields since European settlement have been documented, and thus the data presented provides a baseline against which to compare contemporary ecological datasets. Natural variations in coral assemblage composition, as preserved in core records, clearly occurred in this mid-Holocene reef and were associated with the reef shallowing to sea level as it accreted vertically. Comparisons between modern and mid-Holocene coral community data from equivalent water depths did not reveal marked shifts in coral community composition and diversity, suggesting the long-term persistence of a resilient coral assemblage over these time periods.     

Is increased calcarinid (foraminifera) abundance indicating a larger role for macro-algae in Indonesian Plio-Pleistocene coral reefs?

An important question in coral reef ecology is whether algal abundance in coral reef eco-systems is a natural phenomenon, or has increased as a result of coral reef degradation ultimately resulting in coral–algal regime shifts. Regime shifts, from coral to macro-algae dominated, alter the three-dimensional habitat structure in coral reef ecosystems. Surprisingly, few studies have looked at the effects for species that inhabit the reefs without being the architects of the three-dimensional structure. In this study the effects of a change in habitat characteristics on the community structure of large benthic foraminifera (LBF) is compared between an area with high (Kepulauan Seribu) and lower (Spermonde Archipelago) anthropogenic influence. The results indicate a general relationship between habitat and LBF assemblage structure. The largest difference was observed in shallow habitats. Habitats dominated by algae are inhabited by a specific group of LBF, the Calcarinidae, and domination of this group increases with higher algal prevalence. The fossil record of this group indicates that they evolved following a major change in settings of the central Indo-West-Pacific coral reefs from land detached platforms to fringing reefs, about 5 million years ago. Understanding the biotic response to this transition in reef morphology and the associated increase in terrestrially derived nutrients forms an excellent challenge to gain insights in present-day threats to coral reef ecosystems.     

Reorganization of a large marine ecosystem due to atmospheric and anthropogenic pressure: a discontinuous regime shift in the Central Baltic Sea

Marine ecosystems such as the Baltic Sea are currently under strong atmospheric and anthropogenic pressure. Besides natural and human-induced changes in climate, major anthropogenic drivers such as overfishing and anthropogenic eutrophication are significantly affecting ecosystem structure and function. Recently, studies demonstrated the existence of alternative stable states in various terrestrial and aquatic ecosystems. These so-called ecosystem regime shifts have been explained mainly as a result of multiple causes, e.g. climatic regime shifts, overexploitation or a combination of both. The occurrence of ecosystem regime shifts has important management implications, as they can cause significant losses of ecological and economic resources. Because of hysteresis in ecosystem responses, restoring regimes considered as favourable may require drastic and expensive management actions. Also the Baltic Sea, the largest brackish water body in the world ocean, and its ecosystems are strongly affected by atmospheric and anthropogenic drivers. Here, we present results of an analysis of the state and development of the Central Baltic Sea ecosystem integrating hydroclimatic, nutrient, phyto- and zooplankton as well as fisheries data. Our analyses of 52 biotic and abiotic variables using multivariate statistics demonstrated a major reorganization of the ecosystem and identified two stable states between 1974 and 2005, separated by a transition period in 1988–1993. We show the change in Baltic ecosystem structure to have the characteristics of a discontinuous regime shift, initiated by climate-induced changes in the abiotic environment and stabilized by fisheries-induced feedback loops in the food web. Our results indicate the importance of maintaining the resilience of an ecosystem to atmospherically induced environmental change by reducing the anthropogenic impact.     

Climate warming, marine protected areas and the ocean-scale integrity of coral reef ecosystems

Coral reefs have emerged as one of the ecosystems most vulnerable to climate variation and change. While the contribution of a warming climate to the loss of live coral cover has been well documented across large spatial and temporal scales, the associated effects on fish have not. Here, we respond to recent and repeated calls to assess the importance of local management in conserving coral reefs in the context of global climate change. Such information is important, as coral reef fish assemblages are the most species dense vertebrate communities on earth, contributing critical ecosystem functions and providing crucial ecosystem services to human societies in tropical countries. Our assessment of the impacts of the 1998 mass bleaching event on coral cover, reef structural complexity, and reef associated fishes spans 7 countries, 66 sites and 26 degrees of latitude in the Indian Ocean. Using Bayesian meta-analysis we show that changes in the size structure, diversity and trophic composition of the reef fish community have followed coral declines. Although the ocean scale integrity of these coral reef ecosystems has been lost, it is positive to see the effects are spatially variable at multiple scales, with impacts and vulnerability affected by geography but not management regime. Existing no-take marine protected areas still support high biomass of fish, however they had no positive affect on the ecosystem response to large-scale disturbance. This suggests a need for future conservation and management efforts to identify and protect regional refugia, which should be integrated into existing management frameworks and combined with policies to improve system-wide resilience to climate variation and change.     

Historical reconstruction reveals recovery in Hawaiian coral reefs

Coral reef ecosystems are declining worldwide, yet regional differences in the trajectories, timing and extent of degradation highlight the need for in-depth regional case studies to understand the factors that contribute to either ecosystem sustainability or decline. We reconstructed social-ecological interactions in Hawaiian coral reef environments over 700 years using detailed datasets on ecological conditions, proximate anthropogenic stressor regimes and social change. Here we report previously undetected recovery periods in Hawaiian coral reefs, including a historical recovery in the MHI (~AD 1400-1820) and an ongoing recovery in the NWHI (~AD 1950-2009+). These recovery periods appear to be attributed to a complex set of changes in underlying social systems, which served to release reefs from direct anthropogenic stressor regimes. Recovery at the ecosystem level is associated with reductions in stressors over long time periods (decades+) and large spatial scales (>10(3) km(2)). Our results challenge conventional assumptions and reported findings that human impacts to ecosystems are cumulative and lead only to long-term trajectories of environmental decline. In contrast, recovery periods reveal that human societies have interacted sustainably with coral reef environments over long time periods, and that degraded ecosystems may still retain the adaptive capacity and resilience to recover from human impacts.     

Early detection of ecosystem regime shifts: a multiple method evaluation for management application

Critical transitions between alternative stable states have been shown to occur across an array of complex systems. While our ability to identify abrupt regime shifts in natural ecosystems has improved, detection of potential early-warning signals previous to such shifts is still very limited. Using real monitoring data of a key ecosystem component, we here apply multiple early-warning indicators in order to assess their ability to forewarn a major ecosystem regime shift in the Central Baltic Sea. We show that some indicators and methods can result in clear early-warning signals, while other methods may have limited utility in ecosystem-based management as they show no or weak potential for early-warning. We therefore propose a multiple method approach for early detection of ecosystem regime shifts in monitoring data that may be useful in informing timely management actions in the face of ecosystem change.     

Rehabilitation of coral reefs through removal of macroalgae: state of knowledge and considerations for management and implementation

Coral reef ecosystems are under increasing pressure by multiple stressors that degrade reef condition and function. Although improved management systems have yielded benefits in many regions, broad‐scale declines continue and additional practical and effective solutions for reef conservation and management are urgently needed. Ecological interventions to assist or enhance ecosystem recovery are standard practice in many terrestrial management regimes, and they are now increasingly being implemented in the marine environment. Intervention activities in coral reef systems include the control of coral predators (e.g. crown‐of‐thorns starfish), substrate modification, the creation of artificial habitats and the cultivation, transplantation, and assisted recruitment of corals. On many coastal reefs, corals face competition and overgrowth by fleshy macroalgae whose abundance may be elevated due to acute disturbance events, chronic nutrient enrichment, and reduced herbivory. Active macroalgae removal has been proposed and trialed as a management tool to reduce competition between algae and corals and provide space for coral recruitment, in the hope of restoring the spatial dominance of habitat‐forming corals. However, macroalgae removal has received little formal attention as a method of reef restoration. This review synthesizes available knowledge of the ecological role of macroalgae on coral reefs and the potential benefits and risks associated with their active removal.     

Rising variance: a leading indicator of ecological transition

Regime shifts are substantial, long-lasting reorganizations of complex systems, such as ecosystems. Large ecosystem changes such as eutrophication, shifts among vegetation types, degradation of coral reefs and regional climate change often come as surprises because we lack leading indicators for regime shifts. Increases in variability of ecosystems have been suggested to foreshadow ecological regime shifts. However, it may be difficult to discern variability due to impending regime shift from that of exogenous drivers that affect the ecosystem. We addressed this problem using a model of lake eutrophication. Lakes are subject to fluctuations in recycling associated with regime shifts, as well as fluctuating nutrient inputs. Despite the complications of noisy inputs, increasing variability of lake-water phosphorus was discernible prior to the shift to eutrophic conditions. Simulations show that rising standard deviation (SD) could signal impending shifts about a decade in advance. The rising SD was detected by studying variability around predictions of a simple time-series model, and did not depend on detailed knowledge of the actual ecosystem dynamics.     

The Reef Environment Centralized InFormation System (RECIFS): An integrated geo-environmental database for coral reef research and conservation

Motivation

Host to intricate networks of marine species, coral reefs are among the most biologically diverse ecosystems on Earth. Over the past few decades, major degradations of coral reefs have been observed worldwide, which is largely attributed to the effects of climate change and local stressors related to human activities. Now more than ever, characterizing how the environment shapes the dynamics of the reef ecosystem (e.g., shifts in species abundance, community changes, emergence of locally adapted populations) is key to uncovering the environmental drivers of reef degradation, and developing efficient conservation strategies in response. To achieve these objectives, it is pivotal that environmental data describing the processes driving such ecosystem dynamics, which occur across specific spatial and temporal scales, are easily accessible to coral reef researchers and conservation stakeholders alike.

Main types of variable contained

Multiple environmental variables characterizing various facets of the reef environment, including water chemistry and physics (e.g., temperature, pH, chlorophyll concentration), local anthropogenic pressures (e.g., boat traffic, distance from agricultural or urban areas) and sea currents patterns.

Spatial location and grain

Worldwide reef cells of 5 by 5 km.

Time period and grain

Last 3–4 decades, monthly and yearly resolution.

Major taxa and level of measurement

Environmental data important for coral reefs and associated biodiversity.

Software format

Interactive web application available at https://recifs.epfl.ch .     

Water column contributions to coral reef productivity: overcoming challenges of context dependence

Coral reefs are declining at an unprecedented rate. Effective management and conservation initiatives necessitate improved understanding of the drivers of production because the high rates found in these ecosystems are the foundation of the many services they provide. The water column is the nexus of coral reef ecosystem dynamics, and functions as the interface through which essentially all energy and nutrients are transferred to fuel both new and recycled production. Substantial research has described many aspects of water column dynamics, often focusing on specific components because water column dynamics are highly spatially and temporally context dependent. Although necessary, a cost of this approach is that these dynamics are often not well linked to the broader ecosystem or across systems. To help overcome the challenge of context dependence, we provide a comprehensive review of this literature, and synthesise it through the perspective of ecosystem ecology. Specifically, we provide a framework to organise the drivers of temporal and spatial variation in production dynamics, structured around five primary state factors. These state factors are used to deconstruct the environmental contexts in which three water column sub-food webs mediate ‘new’ and ‘recycled’ production. We then highlight critical pathways by which global change drivers are altering coral reefs via the water column. We end by discussing four key knowledge gaps hindering understanding of the role of the water column for mediating coral reef production, and how overcoming these could improve conservation and management strategies. Throughout, we identify areas of extensive research and those where studies remain lacking and provide a database of 84 published studies. Improved integration of water column dynamics into models of coral reef ecosystem function is imperative to achieve the understanding of ecosystem production necessary to develop effective conservation and management strategies needed to stem global coral loss.     

Temporal clustering of tropical cyclones on the Great Barrier Reef and its ecological importance

Tropical cyclones have been a major cause of reef coral decline during recent decades, including on the Great Barrier Reef (GBR). While cyclones are a natural element of the disturbance regime of coral reefs, the role of temporal clustering has previously been overlooked. Here, we examine the consequences of different types of cyclone temporal distributions (clustered, stochastic or regular) on reef ecosystems. We subdivided the GBR into 14 adjoining regions, each spanning roughly 300 km, and quantified both the rate and clustering of cyclones using dispersion statistics. To interpret the consequences of such cyclone variability for coral reef health, we used a model of observed coral population dynamics. Results showed that clustering occurs on the margins of the cyclone belt, being strongest in the southern reefs and the far northern GBR, which also has the lowest cyclone rate. In the central GBR, where rates were greatest, cyclones had a relatively regular temporal pattern. Modelled dynamics of the dominant coral genus, Acropora, suggest that the long-term average cover might be more than 13 % greater (in absolute cover units) under a clustered cyclone regime compared to stochastic or regular regimes. Thus, not only does cyclone clustering vary significantly along the GBR but such clustering is predicted to have a marked, and management-relevant, impact on the status of coral populations. Additionally, we use our regional clustering and rate results to sample from a library of over 7000 synthetic cyclone tracks for the GBR. This allowed us to provide robust reef-scale maps of annual cyclone frequency and cyclone impacts on Acropora. We conclude that assessments of coral reef vulnerability need to account for both spatial and temporal cyclone distributions.