Stephen R. Palumbi

Rebuilding Global Fisheries

Fighting for Fisheries In the debate concerning the future of the worlds fisheries, some have forecasted complete collapse but others have challenged this view. The protagonists in this debate have now joined forces to present a thorough quantitative review of current trends in world fisheries. Worm et al. (p. 578) evaluate the evidence for a global rebuilding of marine capture fisheries and their supporting ecosystems. Contrasting regions that have been managed for rebuilding with those that have not, reveals trajectories of decline and recovery from individual stocks to species, communities, and large marine ecosystems. The management solutions that have been most successful for rebuilding fisheries and ecosystems, include both large- and small-scale fisheries around the world. Catch restrictions, gear modification, and closed areas are helping to rebuild overexploited marine ecosystems. After a long history of overexploitation, increasing efforts to restore marine ecosystems and rebuild fisheries are under way. Here, we analyze current trends from a fisheries and conservation perspective. In 5 of 10 well-studied ecosystems, the average exploitation rate has recently declined and is now at or below the rate predicted to achieve maximum sustainable yield for seven systems. Yet 63% of assessed fish stocks worldwide still require rebuilding, and even lower exploitation rates are needed to reverse the collapse of vulnerable species. Combined fisheries and conservation objectives can be achieved by merging diverse management actions, including catch restrictions, gear modification, and closed areas, depending on local context. Impacts of international fleets and the lack of alternatives to fishing complicate prospects for rebuilding fisheries in many poorer regions, highlighting the need for a global perspective on rebuilding marine resources.

POPULATION GENETICS, DEMOGRAPHIC CONNECTIVITY, AND THE DESIGN OF MARINE RESERVES

Genetic analyses of marine population structure often find only slight geo- graphic differentiation in species with high dispersal potential. Interpreting the significance of this slight genetic signal has been difficult because even mild genetic structure implies very limited demographic exchange between populations, but slight differentiation could also be due to sampling error. Examination of genetic isolation by distance, in which close populations are more similar than distant ones, has the potential to increase confidence in the significance of slight genetic differentiation. Simulations of one-dimensional stepping stone populations with particular larval dispersal regimes shows that isolation by distance is most obvious when comparing populations separated by 2-5 times the mean larval dispersal distance. Available data on fish and invertebrates can be calibrated with this simulation approach and suggest mean dispersal distances of 25-150 km. Design of marine reserve systems requires an understanding of larval transport in and out of reserves, whether reserves will be self-seeding, whether they will accumulate recruits from surrounding exploited areas, and whether reserve networks can exchange recruits. Direct measurements of mean larval dispersal are needed to understand connectivity in a reserve system, but such measurements are extremely difficult. Genetic patterns of isolation by distance have the potential to add to direct measurement of larval dispersal distance and can help set the appropriate geographic scales on which marine reserve systems will function well.

Marine speciation on a small planet

The scale of population structure in many marine species is on the order of thousands to tens of thousands of kilometers. How does speciation take place in oceans that are only about this same size? Recent results suggest an important role for transient isolation, gamete ecology and molecular evolution at gamete recognition loci. These factors have long been appreciated by plant biologists, and are likely to be a fruitful area of research for marine biologists as well.

Designing marine reserve networks for both conservation and fisheries management

Marine protected areas (MPAs) that exclude fishing have been shown repeatedly to enhance the abundance, size, and diversity of species. These benefits, however, mean little to most marine species, because individual protected areas typically are small. To meet the larger-scale conservation challenges facing ocean ecosystems, several nations are expanding the benefits of individual protected areas by building networks of protected areas. Doing so successfully requires a detailed understanding of the ecological and physical characteristics of ocean ecosystems and the responses of humans to spatial closures. There has been enormous scientific interest in these topics, and frameworks for the design of MPA networks for meeting conservation and fishery management goals are emerging. Persistent in the literature is the perception of an inherent tradeoff between achieving conservation and fishery goals. Through a synthetic analysis across these conservation and bioeconomic studies, we construct guidelines for MPA network design that reduce or eliminate this tradeoff. We present size, spacing, location, and configuration guidelines for designing networks that simultaneously can enhance biological conservation and reduce fishery costs or even increase fishery yields and profits. Indeed, in some settings, a well-designed MPA network is critical to the optimal harvest strategy. When reserves benefit fisheries, the optimal area in reserves is moderately large (mode ≈30%). Assessing network design principals is limited currently by the absence of empirical data from large-scale networks. Emerging networks will soon rectify this constraint.

POPULATION MODELS FOR MARINE RESERVE DESIGN: A RETROSPECTIVE AND PROSPECTIVE SYNTHESIS

We synthesize results from existing models of marine reserves to identify key theoretical issues that appear to be well understood, as well as issues in need of further exploration. Models of marine reserves are relatively new in the scientific literature; 32 of the 34 theoretical papers we reviewed were published after 1990. These models have focused primarily on questions concerning fishery management at the expense of other objectives such as conservation, scientific understanding, recreation, education, and tourism. Roughly one-third of the models analyze effects on cohorts while the remaining models have some form of complete population dynamics. Few models explicitly include larval dispersal. In a fisheries context, the primary conclusion drawn by many of the complete population models is that reserves increase yield when populations would otherwise be overfished. A second conclusion, resulting primarily from single-cohort models, is that reserves will provide fewer benefits for species with greater adult rates of movement. Although some models are beginning to yield information on the spatial configurations of reserves required for populations with specific dispersal distances to persist, it remains an aspect of reserve design in need of further analysis. Other outstanding issues include the effects of (1) particular forms of density dependence, (2) multispecies interactions, (3) fisher behavior, and (4) effects of concentrated fishing on habitat. Model results indicate that marine reserves could play a beneficial role in the protection of marine systems against overfishing. Additional modeling and analysis will greatly improve prospects for a better understanding of the potential of marine reserves for conserving biodiversity.

Biogeography: A marine Wallace's line?

As most coral reef organisms with a pelagic larval phase are presumed to be readily dispersed between distant populations, sea-surface current patterns should be crucial for predicting ecological and genetic connections among threatened reef populations. Here we investigate this idea by examining variations in the genetic structuring of populations of the mantis shrimp Haptosquilla pulchella taken from 11 reef systems in Indonesia, in which a series of 36 protected areas are presumed to be connected by strong ocean currents. Our results reveal instead that there is a strong regional genetic differentiation that mirrors the separation of ocean basins during the Pleistocene low-sea-level stands, indicating that ecological connections are rare across distances as short as 300–400 km and that biogeographic history also influences contemporary connectivity between reef ecosystems.

Genomic basis for coral resilience to climate change

Recent advances in DNA-sequencing technologies now allow for in-depth characterization of the genomic stress responses of many organisms beyond model taxa. They are especially appropriate for organisms such as reef-building corals, for which dramatic declines in abundance are expected to worsen as anthropogenic climate change intensifies. Different corals differ substantially in physiological resilience to environmental stress, but the molecular mechanisms behind enhanced coral resilience remain unclear. Here, we compare transcriptome-wide gene expression (via RNA-Seq using Illumina sequencing) among conspecific thermally sensitive and thermally resilient corals to identify the molecular pathways contributing to coral resilience. Under simulated bleaching stress, sensitive and resilient corals change expression of hundreds of genes, but the resilient corals had higher expression under control conditions across 60 of these genes. These “frontloaded” transcripts were less up-regulated in resilient corals during heat stress and included thermal tolerance genes such as heat shock proteins and antioxidant enzymes, as well as a broad array of genes involved in apoptosis regulation, tumor suppression, innate immune response, and cell adhesion. We propose that constitutive frontloading enables an individual to maintain physiological resilience during frequently encountered environmental stress, an idea that has strong parallels in model systems such as yeast. Our study provides broad insight into the fundamental cellular processes responsible for enhanced stress tolerances that may enable some organisms to better persist into the future in an era of global climate change.

Marine defaunation: Animal loss in the global ocean

Marine animals are disappearing, too The loss of animal species in terrestrial environments has been well documented and is continuing. Loss of species in marine environments has been slower than in terrestrial systems, but appears to be increasing rapidly. McCauley et al. review the recent patterns of species decline and loss in marine environments. Though they note many worrying declines, they also highlight approaches that might allow us to prevent the type of massive defaunation that has occurred on land. Science, this issue 10.1126/science.1255641 BACKGROUND Comparing patterns of terrestrial and marine defaunation helps to place human impacts on marine fauna in context and to navigate toward recovery. Defaunation began in earnest tens of thousands of years later in the oceans than it did on land. Although defaunation has been less severe in the oceans than on land, our effects on marine animals are increasing in pace and impact. Humans have caused few complete extinctions in the sea, but we are responsible for many ecological, commercial, and local extinctions. Despite our late start, humans have already powerfully changed virtually all major marine ecosystems. ADVANCES Humans have profoundly decreased the abundance of both large (e.g., whales) and small (e.g., anchovies) marine fauna. Such declines can generate waves of ecological change that travel both up and down marine food webs and can alter ocean ecosystem functioning. Human harvesters have also been a major force of evolutionary change in the oceans and have reshaped the genetic structure of marine animal populations. Climate change threatens to accelerate marine defaunation over the next century. The high mobility of many marine animals offers some increased, though limited, capacity for marine species to respond to climate stress, but it also exposes many species to increased risk from other stressors. Because humans are intensely reliant on ocean ecosystems for food and other ecosystem services, we are deeply affected by all of these forecasted changes. Three lessons emerge when comparing the marine and terrestrial defaunation experiences: (i) today’s low rates of marine extinction may be the prelude to a major extinction pulse, similar to that observed on land during the industrial revolution, as the footprint of human ocean use widens; (ii) effectively slowing ocean defaunation requires both protected areas and careful management of the intervening ocean matrix; and (iii) the terrestrial experience and current trends in ocean use suggest that habitat destruction is likely to become an increasingly dominant threat to ocean wildlife over the next 150 years. OUTLOOK Wildlife populations in the oceans have been badly damaged by human activity. Nevertheless, marine fauna generally are in better condition than terrestrial fauna: Fewer marine animal extinctions have occurred; many geographic ranges have shrunk less; and numerous ocean ecosystems remain more wild than terrestrial ecosystems. Consequently, meaningful rehabilitation of affected marine animal populations remains within the reach of managers. Human dependency on marine wildlife and the linked fate of marine and terrestrial fauna necessitate that we act quickly to slow the advance of marine defaunation. Timeline (log scale) of marine and terrestrial defaunation. The marine defaunation experience is much less advanced, even though humans have been harvesting ocean wildlife for thousands of years. The recent industrialization of this harvest, however, initiated an era of intense marine wildlife declines. If left unmanaged, we predict that marine habitat alteration, along with climate change (colored bar: IPCC warming), will exacerbate marine defaunation. Marine defaunation, or human-caused animal loss in the oceans, emerged forcefully only hundreds of years ago, whereas terrestrial defaunation has been occurring far longer. Though humans have caused few global marine extinctions, we have profoundly affected marine wildlife, altering the functioning and provisioning of services in every ocean. Current ocean trends, coupled with terrestrial defaunation lessons, suggest that marine defaunation rates will rapidly intensify as human use of the oceans industrializes. Though protected areas are a powerful tool to harness ocean productivity, especially when designed with future climate in mind, additional management strategies will be required. Overall, habitat degradation is likely to intensify as a major driver of marine wildlife loss. Proactive intervention can avert a marine defaunation disaster of the magnitude observed on land.

Guiding ecological principles for marine spatial planning

The declining health of marine ecosystems around the world is evidence that current piecemeal governance is inadequate to successfully support healthy coastal and ocean ecosystems and sustain human uses of the ocean. One proposed solution to this problem is ecosystem-based marine spatial planning (MSP), which is a process that informs the spatial distribution of activities in the ocean so that existing and emerging uses can be maintained, use conflicts reduced, and ecosystem health and services protected and sustained for future generations. Because a key goal of ecosystem-based MSP is to maintain the delivery of ecosystem services that humans want and need, it must be based on ecological principles that articulate the scientifically recognized attributes of healthy, functioning ecosystems. These principles should be incorporated into a decision-making framework with clearly defined targets for these ecological attributes. This paper identifies ecological principles for MSP based on a synthesis of previously suggested and/or operationalized principles, along with recommendations generated by a group of twenty ecologists and marine scientists with diverse backgrounds and perspectives on MSP. The proposed four main ecological principles to guide MSP--maintaining or restoring: native species diversity, habitat diversity and heterogeneity, key species, and connectivity--and two additional guidelines, the need to account for context and uncertainty, must be explicitly taken into account in the planning process. When applied in concert with social, economic, and governance principles, these ecological principles can inform the designation and siting of ocean uses and the management of activities in the ocean to maintain or restore healthy ecosystems, allow delivery of marine ecosystem services, and ensure sustainable economic and social benefits.

SPECIATION AND POPULATION GENETIC STRUCTURE IN TROPICAL PACIFIC SEA URCHINS

Unlike populations of many terrestrial species, marine populations often are not separated by obvious, permanent barriers to gene flow. When species have high dispersal potential and few barriers to gene flow, allopatric divergence is slow. Nevertheless, many marine species are of recent origin, even in taxa with high dispersal potential. To understand the relationship between genetic structure and recent species formation in high dispersal taxa, we examined population genetic structure among four species of sea urchins in the tropical Indo‐West Pacific that have speciated within the past one to three million years. Despite high potential for gene flow, mtDNA sequence variation among 200 individuals of four species in the urchin genus Echinometra shows a signal of strong geographic effects. These effects include (1) substantial population heterogeneity; (2) lower genetic variation in peripheral populations; and (3) isolation by distance. These geographic patterns are especially strong across scales of 5000‐10,000 km, and are weaker over scales of 2500‐5000 km. As a result, strong geographic patterns would not have been readily visible except over the wide expanse of the tropical Pacific. Surface currents in the Pacific do not explain patterns of gene flow any better than do patterns of simple spatial proximity. Finally, populations of each species tend to group into large mtDNA regions with similar mtDNA haplotypes, but these regional boundaries are not concordant in different species. These results show that all four species have accumulated mtDNA differences over similar spatial and temporal scales but that the precise geographic pattern of genetic differentiation varies for each species. These geographic patterns appear much less deterministic than in other well‐known coastal marine systems and may be driven by chance and historical accident.