HABITAT destruction is the major cause of species extinctions1–3. Dominant species often are considered to be free of this threat because they are abundant in the undisturbed fragments that remain after destruction. Here we describe a model that explains multispecies coexistence in patchy habitats4 and which predicts that their abundance may be fleeting. Even moderate habitat destruction is predicted to cause time-delayed but deterministic extinction of the dominant competitor in remnant patches. Further species are predicted to become extinct, in order from the best to the poorest competitors, as habitat destruction increases. More-over, the more fragmented a habitat already is, the greater is the number of extinctions caused by added destruction. Because such extinctions occur generations after fragmentation, they represent a debt—a future ecological cost of current habitat destruction.

Habitat destruction and the extinction debt

Connectivity, or the exchange of individuals among marine populations, is a central topic in marine ecology. For most benthic marine species with complex life cycles, this exchange occurs primarily during the pelagic larval stage. The small size of larvae coupled with the vast and complex fluid environment they occupy hamper our ability to quantify dispersal and connectivity. Evidence from direct and indirect approaches using geochemical and genetic techniques suggests that populations range from fully open to fully closed. Understanding the biophysical processes that contribute to observed dispersal patterns requires integrated interdisciplinary approaches that incorporate high-resolution biophysical modeling and empirical data. Further, differential postsettlement survival of larvae may add complexity to measurements of connectivity. The degree to which populations self recruit or receive subsidy from other populations has consequences for a number of fundamental ecological processes that affect population regulation and persistence. Finally, a full understanding of population connectivity has important applications for management and conservation.

Larval Dispersal and Marine Population Connectivity

We review the effects of fishing on benthic fauna, habitat, diversity, community structure and trophic interactions in tropical, temperate and polar marine environments and consider whether it is possible to predict or manage fishing-induced changes in marine ecosystems Such considerations are timely given the disillusionment with some fishery management strategies and that policy makers need a scientific basis for deciding whether they should respond to social, economic and political demands for instituting or preventing ecosystem-based management Fishing has significant direct and indirect effects on habitat, and on the diversity, structure and productivity of benthic communities These effects are most readily identified and last longest in those areas that experience infrequent natural disturbance The initiation of fishing in an unfished system leads to dramatic changes in fish community structure As fishing intensity increases the additional effects are more difficult to detect Fishing has accelerated and magnified natural declines in the abundance of many forage fishes and this has lead to reduced reproductive success and abundance in birds and marine mammals However, such donor-controlled dynamics are less apparent in food webs where fishes are the top predators since their feeding strategies are rather more plastic than those of most birds and mammals Fishers tend to target species in sequence as a fishery develops and this leads to changes in the composition of the fished communities with time The dramatic and apparently compensatory shifts in the biomass of different species in many fished ecosystems have often been driven by environmental change rather than the indirect effects of fishing Indeed, in most pelagic systems, species replacements would have occurred, albeit less rapidly, in the absence of fishing pressure In those cases when predator or prey species fill a key role, fishing can have dramatic indirect effects on community structure Thus fishing has shifted some coral reef ecosystems to alternate stable states because there is tight predator–prey coupling between invertebrate feeding fishes and sea urchins Fishing has reduced, and locally extirpated, populations of predatory fishes These reductions do not have a consistent effect on the abundance and diversity of their prey: environmental processes control prey populations in some systems, whereas top-down processes are more important in others By-catch which is discarded during fishing activities may sustain populations of scavenging species, particularly seabirds We conclude by identifying the circumstances in which new research is needed to guide managers and stress the importance of unfished control sites for studies of fishing effects We discuss the advantages and disadvantages of closed area management (marine reserves) and the conditions under which such management is likely to provide benefits for the fishery or ecosystem

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The effects of fishing on marine ecosystems

We present a model of community regulation that incorporates the effects of abiotic disturbance, predation, competition, and recruitment density. We assume that mobile organisms (i.e., consumers) are more strongly affected by environmental stress than are sessile organisms and that food-web complexity decreases with increasing stress. The model makes three predictions under conditions of high recruitment. First, in stressful environments, consumers have no effect because they are absent or inactive, and competition for space is prevented. Both mobile and sessile organisms are regulated directly by environmental stress. Second, in moderate environments, consumers are still ineffective, but sessile organisms are less affected by stress and frequently attain high densities, leading to competition for space. Finally, in benign environments, consumers prevent competition for space unless the prey can escape a predation bottleneck and reach a high abundance. A reduction in recruitment density reduces the import...

Community regulation: variation in disturbance, competition, and predation in relation to environmental stress and recruitment

Most surveys of mitochondrial DNA (mtDNA) in marine fishes reveal low levels of sequence divergence between haplotypes relative to the differentiation observed between sister taxa. It is unclear whether this pattern is due to rapid lineage sorting accelerated by sweepstakes recruitment, historical bottlenecks in population size, founder events, or natural selection, any of which could retard the accumulation of deep mtDNA lineages. Recent advances in paleoclimate research prompt a reexamination of oceanographic processes as a fundamental influence on genetic diversity; evidence from ice cores and anaerobic marine sediments document strong regime shifts in the world’s oceans in concert with periodic climatic changes. These changes in sea surface temperatures, current pathways, upwelling intensities, and retention eddies are likely harbingers of severe fluctuations in population size or regional extinctions. Sardines (Sardina, Sardinops) and anchovies (Engraulis) are used to assess the consequences of such oceanographic processes on marine fish intrageneric gene genealogies. Representatives of these two groups occur in temperate boundary currents on a global scale, and these regional populations are known to fluctuate markedly. Biogeographic and genetic data indicate that Sardinops has persisted for at least 20 million years, yet the mtDNA genealogy for this group coalesces in less than half a million years and points to a recent founding of populations around the rim of the Indian–Pacific Ocean. Phylogeographic analysis of Old World anchovies reveals a Pleistocene dispersal from the Pacific to the Atlantic, almost certainly via southern Africa, followed by a very recent recolonization from Europe to southern Africa. These results demonstrate that regional populations of sardines and anchovies are subject to periodic extinctions and recolonizations. Such climate-associated dynamics may explain the low levels of nucleotide diversity and the shallow coalescence of mtDNA genealogies. If these findings apply generally to marine fishes, management strategies should incorporate the idea that even extremely abundant populations may be relatively fragile on ecological and evolutionary time scales.

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Shallow population histories in deep evolutionary lineages of marine fishes: insights from sardines and anchovies and lessons for conservation

A long-term, large-scale empirical test of the recruitment limitation hypothesis was done by sampling fish populations from the southern Great Barrier Reef after having monitored their recruitment histories for 9 years. After adjustment for demographic differences, recruitment patterns explained over 90 percent of the spatial variation in abundance of a common damselfish among seven coral reefs. The age structures from individual reefs also preserved major temporal variations in the recruitment signal over at least 10 years. Abundance and demography of this small fish at these spatial and temporal scales can be explained almost entirely as variable recruitment interacting with density-independent mortality.

https://science.sciencemag.org/content/sci/263/5149/935.full.pdf

An empirical test of recruitment limitation in a coral reef fish.

The Great Barrier Reef (GBR) is a continental archipelagic system of 5000 reefs and shoals stretching >2000 km along the east Australia coast. The interconnectivity of these reefs should determine the choice of biological management units, which for most biota will reflect the dispersal of their eggs and/or larvae. A comparative approach using population genetics was used to ask whether the along-shore dispersal of coral reef fishes is influenced by the duration of this mobile phase. Seven species of coral reef fish, selected from three families to provide a range of taxonomic diversity and pelagic larval durations, were tested for genetic homogeneity between two regions of the GBR separated by 1000 km. A spectrum of potential dispersal capabilities was analyzed from that of Acanthochromis polyacanthus, a damselfish with brood care that uniquely lacks pelagic larvae, to that of Ctenochaetus striatus, a surgeonfish with large, specialized larvae that spend several months in the plankton. A total of 19 enzyme systems and general proteins were examined from multiple populations in each region to provide a base of 32 loci for these comparisons. With one exception, species sampled from different coral reefs within regions showed statistically significant heterogeneities across multiple loci, indicative of chaotic genetic patchiness among the samples. The exception was an anemonefish, Amphiprion melanopus, that had to be collected from large areas on each reef because of its low densities. The homogeneity of allele frequencies at local scales for this species suggests that the genetic patchiness observed in others may be a within-reef phenomenon that was manifested at the reef scale by our pseudoreplicated sampling strategy. After pooling local variability, all but two species showed significant regional differ- ences. The exceptions were the pair (Ctenochaetus striatus, Pterocaesio chrysozona) with the longest larval durations. Acanthochromis polyacanthus showed increased variation at this larger scale, consistent with a major stock division between the two regions. The logarithm of genetic variation between northern and southern populations (measured by Weir and Cockerham's Fst)was correlated with mean larval duration by an inverse linear relationship that explained 85% of the variance in the global data set. Comparison with an outgroup (Amphiprion melanopus from the Chesterfield Reefs, 1000 km east in the Coral Sea) confirmed the genetic cohesion of mainland populations for the species with shortest larval duration and shows that our empirical relationship applies only within the context of the highly connected GBR. On this basis, calculations of gene flow (Nem, the number of effective migrants per generation) between geographic regions predict panmixis for species with larval durations exceeding 1 mo. Many common species have shorter dispersal times, from which classical "isolation-by-distance" models predict differentiation between northern and southern pop- ulations at genetic equilibrium. Given that modern populations on the GBR are <10000 yr old, however, there has not been sufficient time for such differences to evolve in situ and we consider alternative scenarios for the observed heterogeneities. Comparisons with invertebrate taxa sampled over the same spatial scales imply lower gene flows in fish despite longer pelagic durations. This suggests that fish larvae may use their greater mobility to retard, rather than enhance, dispersal due to hydrodynamic advection.

Gene flow and larval duration in seven species of fish from the great barrier reef

Spatial and temporal patterns in recruitment

The spatial distributions of two common damselfishes, Potnacentrus wvardi and P. flavicauda, suggest that they compete for common resources within lagoons of the southern Great Barrier Reef. Both fishes are herbivores that defend territories on rocky substrata covered with shallow water, but are segregated by microhabitat. When young P. flavicauda recruit into the habitat where P. w'ardi are most numerous, they have lower persistence than counterparts on reefs where conspecifics predominate. Several experiments were done, using as replicates the large patch reefs populated by P. wiardi, to determine what effects territory-holding individuals have on the distribution and abundance of conspecifics, P. flatvicauda, and other grazing fishes. Total and selective removal of the numerically dominant P. wardi revealed that these reefs are mostly repopulated by larval fishes (recruitment), rather than by already recruited fishes (immigra- tion). P. wardi are the most frequent recruits. The removals also showed that resident P. wtnardi do not determine the numbers of nonspecific larvae invading their territories, and do not reduce their survival after recruitment (at least for 300-400 d). They do determine the growth of such juveniles. Despite this interaction, there was no evidence that either density or biomass is usually regulated in these populations. Both measures vary greatly among replicate reefs. The lack of numerical equilib- rium, within the study period, was caused by a patchy and limiting supply of larval recruits. Manipulations also showed that resident P. bxardi do not limit the recruitment or reduce the postrecruitment survival of P. flavicauda on large patch reefs. An unknown density-independent cause is implicated in the observed habitat segregation and in the failure of P. flavicauda to reach breeding size on such reefs. The removal of P. wardi produced different results for the fish grazers from other families, de- pending upon their feeding strategy. For example, solitary acanthurids concentrated their grazing activities on reefs with fewer damselfishes, but a schooling parrotfish did not. The outcomes of these perturbations support a nonequilibrial view of reef fish communities, rather than hypotheses that emphasize the importance of competition among populations usually at carrying capacity.

Peter Doherty

Papers

An empirical test of recruitment limitation in a coral reef fish.

Gene flow and larval duration in seven species of fish from the great barrier reef

Spatial and temporal patterns in recruitment

Tropical Territorial Damselfishses: Is Density Limited by Aggression or Recruitment?

Light-traps: selective but useful devices for quantifying the distributions and abundances of larval fishes