Survival variability and population density in fish populations.

To understand the processes that regulate the abundance and persistence of wild populations is a fundamental goal of ecology and a prerequisite for the management of living resources. Variable abundance data, however, make the demonstration of regulation processes challenging. A previously overlooked aspect in understanding how populations are regulated is the possibility that the pattern of variability--its strength as a function of population size--may be more than 'noise', thus revealing much about the characteristics of population regulation. Here we show that patterns in survival variability do provide evidence of regulation through density. Using a large, global compilation of marine, anadromous and freshwater fisheries data, we examine the relationship between the variability of survival and population abundance. The interannual variability in progeny survival increases at low adult abundance in an inversely density-dependent fashion. This pattern is consistent with models in which density dependence enters after the larval stage. The findings are compatible with very simple forms of density dependence: even a linear increase of juvenile mortality with adult density adequately explains the results. The model predictions explain why populations with strong regulation may experience large increases in variability at low densities. Furthermore, the inverse relationship between survival variability and the strength of density dependence has important consequences for fisheries management and recovery, and population persistence or extinction.

Management effectiveness of the world's marine fisheries.

Ongoing declines in production of the world's fisheries may have serious ecological and socioeconomic consequences. As a result, a number of international efforts have sought to improve management and prevent overexploitation, while helping to maintain biodiversity and a sustainable food supply. Although these initiatives have received broad acceptance, the extent to which corrective measures have been implemented and are effective remains largely unknown. We used a survey approach, validated with empirical data, and enquiries to over 13,000 fisheries experts (of which 1,188 responded) to assess the current effectiveness of fisheries management regimes worldwide; for each of those regimes, we also calculated the probable sustainability of reported catches to determine how management affects fisheries sustainability. Our survey shows that 7% of all coastal states undergo rigorous scientific assessment for the generation of management policies, 1.4% also have a participatory and transparent processes to convert scientific recommendations into policy, and 0.95% also provide for robust mechanisms to ensure the compliance with regulations; none is also free of the effects of excess fishing capacity, subsidies, or access to foreign fishing. A comparison of fisheries management attributes with the sustainability of reported fisheries catches indicated that the conversion of scientific advice into policy, through a participatory and transparent process, is at the core of achieving fisheries sustainability, regardless of other attributes of the fisheries. Our results illustrate the great vulnerability of the world's fisheries and the urgent need to meet well-identified guidelines for sustainable management; they also provide a baseline against which future changes can be quantified.

Life-history correlates of extinction risk and recovery potential.

Extinction risk is inversely associated with maximum per capita population growth rate (r(max)). However, this parameter is not known for most threatened species, underscoring the value in identifying correlates of r(max) that, in the absence of demographic data, would indirectly allow one to identify species and populations at elevated risk of extinction and their associated recovery potential. We undertook a comparative life-history analysis of 199 species from three taxonomic classes: Chondrichthyes (e.g., sharks; n = 82), Actinopterygii (teleost or bony fishes; n = 47), and Mammalia (n = 70, including 16 marine species). Median r(max) was highest for (and similar between) terrestrial mammals (0.71) and teleosts (0.43), significantly lower among chondrichthyans (0.26), and lower still in marine mammals (0.07). Age at maturity was the primary (and negative) correlate of r(max). In contrast, although body size was negatively correlated with r(max) in chondrichthyans and mammals, evidence of an association in teleosts was equivocal, and fecundity was not related to r(max) in fishes, despite recurring assertions to the contrary. Our analyses suggest that age at maturity can serve as a universal predictor of extinction risk in fishes and mammals when r(max) itself is unknown. Moreover, in contrast to what is generally expected, the recovery potential of teleost fishes does not differ from that of terrestrial mammals. Our findings are supportive of the application of extinction-risk criteria that are based on generation time and that are independent of taxonomic affinity.

A global assessment of salmon aquaculture impacts on wild salmonids.

Since the late 1980s, wild salmon catch and abundance have declined dramatically in the North Atlantic and in much of the northeastern Pacific south of Alaska. In these areas, there has been a concomitant increase in the production of farmed salmon. Previous studies have shown negative impacts on wild salmonids, but these results have been difficult to translate into predictions of change in wild population survival and abundance. We compared marine survival of salmonids in areas with salmon farming to adjacent areas without farms in Scotland, Ireland, Atlantic Canada, and Pacific Canada to estimate changes in marine survival concurrent with the growth of salmon aquaculture. Through a meta-analysis of existing data, we show a reduction in survival or abundance of Atlantic salmon; sea trout; and pink, chum, and coho salmon in association with increased production of farmed salmon. In many cases, these reductions in survival or abundance are greater than 50%. Meta-analytic estimates of the mean effect are significant and negative, suggesting that salmon farming has reduced survival of wild salmon and trout in many populations and countries.

Trade-offs between efficiency and robustness in bacterial metabolic networks are associated with niche breadth.

The relation between structure and function in biologic networks is a central point of systems biology research. Key functional features--notably, efficiency and robustness--are linked to the topologic structure of a network, and there appears to be a degree of trade-off between these features, i.e., simulation studies indicate that more efficient networks tend to be less robust. Here, we investigate this issue in metabolic networks from 105 lineages of bacteria having a wide range of ecologies. We take quantitative measurements on each network and integrate this network data with ecologic data using a phylogenetic comparative model. In this setting, we find that biologic conclusions obtained with classical phylogenetic comparative methods are sensitive to correlations between model covariates and phylogenetic branch length. To avoid this problem, we propose a revised statistical framework--hierarchical mixed-effect regression--to accommodate phylogenetic nonindependence. Using this approach, we show that the cartography of metabolic networks does indeed reflect a trade-off between efficiency and robustness. Furthermore, ecologic characteristics related to niche breadth are strong predictors of network shape. Given the broad variation in niche breadth seen among species, we predict that there is no universally optimal balance between efficiency and robustness in bacterial metabolic networks and, thus, no universally optimal network structure. These results highlight the biologic relevance of variation in network structure and the potential role of niche breadth in shaping metabolic strategies of efficiency and robustness.

Sex-specific, seasonal foraging tactics of adult grey seals (Halichoerus grypus) revealed by state-space analysis.

In many large pelagic animals, observing behavior is limited to observation by radio or satellite telemetry. In many cases, discriminating different behaviors from telemetry data has been a key, but often elusive, goal. Here we use state-space models (SSMs) to fit a correlated random walk (CRW) model that switches between two unobserved behavioral states (nominally foraging and traveling) to 41 male and 43 female adult grey seal (Halichoerus grypus) satellite telemetry tracks. The SSM results reveal markedly different spatial behavior between the sexes, fitting well with sexual size dimorphism and known dietary differences, suggesting that the sexes deal with seasonal prey availability and reproductive costs differently. From these results we were also able to produce behaviorally informed habitat use maps, showing a complex and dynamic network of small, intensely used foraging areas. Our flexible SSM approach clearly demonstrates sex-related behavioral differences, fine scale spatial and temporal foraging patterns, and a clearer picture of grey seal ecology and role in the Scotian Shelf ecosystem.

Assessing threats to species at risk using stage-structured state-space models: mortality trends in skate populations.

Population models are needed to assess the threats to species at risk and to evaluate alternative management actions. Data to support modeling is limited for many species at risk, and commonly used approaches generally assume stationary vital rates, a questionable assumption given widespread ecosystem change. We describe a modeling approach that can be applied to time series of length composition data to estimate vital rates and test for changes in these rates. Our approach uses stage-structured population models fit within a Bayesian state-space model. This approach simultaneously allows for both process and observation uncertainty, and it facilitates incorporating prior information on population dynamics and on the monitoring process. We apply these models to populations of winter skate (Leucoraja ocellata) that have been designated as "endangered" or "threatened." These models indicate that natural mortality has decreased for juveniles and increased for adults in these populations. The declines observed in these populations had been attributed to unsustainable rates of bycatch in fisheries for other groundfishes; our analyses indicate that increased natural mortality of adults is also an important factor contributing to these declines. Adult natural mortality was positively related to grey seal (Halichoerus grypus) abundance, suggesting the hypothesis that increased adult mortality reflected increased predation by expanding grey seal herds. Population projections indicated that the threatened population would be expected to stabilize at a low level of abundance if all fishery removals were eliminated, but that the endangered population would likely continue to decline even in the absence of fishery removals. We note that time series of size distributions are available for most marine fish populations monitored by research surveys, and we suggest that a similar approach could be used to extract information from these time series in order to estimate mortality rates and changes in these rates.

The importance of habitat and life history to extinction risk in sharks, skates, rays and chimaeras.

We compared life-history traits and extinction risk of chondrichthyans (sharks, rays and chimaeras), a group of high conservation concern, from the three major marine habitats (continental shelves, open ocean and deep sea), controlling for phylogenetic correlation. Deep-water chondrichthyans had a higher age at maturity and longevity, and a lower growth completion rate than shallow-water species. The average fishing mortality needed to drive a deep-water chondrichthyan species to extinction (Fextinct) was 38-58% of that estimated for oceanic and continental shelf species, respectively. Mean values of Fextinct were 0.149, 0.250 and 0.368 for deep-water, oceanic and continental shelf species, respectively. Reproductive mode was an important determinant of extinction risk, while body size had a weak effect on extinction risk. As extinction risk was highly correlated with phylogeny, the loss of species will be accompanied by a loss of phylogenetic diversity. Conservation priority should not be restricted to large species, as is usually suggested, since many small species, like those inhabiting the deep ocean, are also highly vulnerable to extinction. Fishing mortality of deep-water chondrichthyans already exploited should be minimized, and new deep-water fisheries affecting chondrichthyans should be prevented.

The completeness of taxonomic inventories for describing the global diversity and distribution of marine fishes.

Taxonomic inventories (or species censuses) are the most elementary data in biogeography, macroecology and conservation biology. They play fundamental roles in the construction of species richness patterns, delineation of species ranges, quantification of extinction risk and prioritization of conservation efforts in hot spot areas. Given their importance, any issue related to the completeness of taxonomic inventories can have far-reaching consequences. Here, we used the largest publicly available database of georeferenced marine fish records to determine its usefulness in depicting the diversity and distribution of this taxonomic group. All records were grouped at multiple spatial resolutions to generate accumulation curves, from which the expected number of species were extrapolated using a variety of nonlinear models. Comparison of the inventoried number of species with that expected from the models was used to calculate the completeness of the taxonomic inventory at each resolution. In terms of the global number of fish species, we found that approximately 21% of the species remain to be described. In terms of spatial distribution, we found that the completeness of taxonomic data was highly scale dependent, with completeness being lower at finer spatial resolutions. At a 3 degrees (approx. 350km2) spatial resolution, less than 1.8% of the world's oceans have above 80% of their fish fauna currently described. Censuses of species were particularly incomplete in tropical areas and across the entire range of countries' gross domestic product (GDP), although the few censuses nearing completion were all along the coasts of a few developed countries or territories. Our findings highlight that failure to quantify the completeness of taxonomic inventories can introduce substantial flaws in the description of diversity patterns, and raise concerns over the effectiveness of conservation strategies based upon data that remain largely precarious.

Loss of large predatory sharks from the Mediterranean Sea.

Evidence for severe declines in large predatory fishes is increasing around the world. Because of its long history of intense fishing, the Mediterranean Sea offers a unique perspective on fish population declines over historical timescales. We used a diverse set of records dating back to the early 19th and mid 20th century to reconstruct long-term population trends of large predatory sharks in the northwestern Mediterranean Sea. We compiled 9 time series of abundance indices from commercial and recreational fishery landings, scientific surveys, and sighting records. Generalized linear models were used to extract instantaneous rates of change from each data set, and a meta-analysis was conducted to compare population trends. Only 5 of the 20 species we considered had sufficient records for analysis. Hammerhead (Sphyrna spp.), blue (Prionace glauca), mackerel (Isurus oxyrinchus and Lamna nasus), and thresher sharks (Alopias vulpinus) declined between 96 and 99.99% relative to their former abundance. According to World Conservation Union (IUCN) criteria, these species would be considered critically endangered. So far, the lack of quantitative population assessments has impeded shark conservation in the Mediterranean Sea. Our study fills this critical information gap, suggesting that current levels of exploitation put large sharks at risk of extinction in the Mediterranean Sea. Possible ecosystem effects of these losses involve a disruption of top-down control and a release of midlevel consumers.

Experimental simulations about the effects of overexploitation and habitat fragmentation on populations facing environmental warming.

Populations of many species are dramatically declining worldwide, but the causal mechanism remains debated among different human-related threats. Coping with this uncertainty is critical to several issues about the conservation and future of biodiversity, but remains challenging due to difficulties associated with the experimental manipulation and/or isolation of the effects of such threats under field conditions. Using controlled microcosm populations, we quantified the individual and combined effects of environmental warming, overexploitation and habitat fragmentation on population persistence. Individually, each of these threats produced similar and significant population declines, which were accelerated to different degrees depending upon particular interactions. The interaction between habitat fragmentation and harvesting generated an additive decline in population size. However, both of these threats reduced population resistance causing synergistic declines in populations also facing environmental warming. Declines in population size were up to 50 times faster when all threats acted together. These results indicate that species may be facing risks of extinction higher than those anticipated from single threat analyses and suggest that all threats should be mitigated simultaneously, if current biodiversity declines are to be reversed.

Behaviour of leatherback sea turtles, Dermochelys coriacea, during the migratory cycle.

Leatherback sea turtles, Dermochelys coriacea, undertake broad oceanic movements. While satellite telemetry has been used to investigate the post-nesting behaviour of female turtles tagged on tropical nesting beaches, long-term behavioural patterns of turtles of different sexes and sizes have not been described. Here we investigate behaviour for 25 subadult and adult male and female turtles satellite-tagged in temperate waters off Nova Scotia, Canada. Although sex and reproductive condition contributed to variation in migratory patterns, the migratory cycle of all turtles included movement between temperate and tropical waters. Marked changes in rates of travel, and diving and surfacing behaviour, accompanied southward movement away from northern foraging areas. As turtles approached higher latitudes the following spring and summer, they assumed behaviours consistent with regular foraging activity and eventually settled in coastal areas off Canada and the northeastern USA. Behavioural patterns corresponding to various phases of the migratory cycle were consistent across multiple animals and were repeated within individuals that completed return movements to northern waters. We consider the potential biological significance of these patterns, including how turtle behaviour relates to predator avoidance, thermoregulation and prey distribution.

A Spurious Correlation in an Interpopulation Comparison of Atlantic Salmon Life Histories.

We tested two hypotheses concerning geographical variation in Atlantic salmon (Salmo salar) life histories: (1) mean age at first reproduction is positively correlated with growth rate at sea and (2) within-population variation in age at first reproduction first increases and then decreases with latitude. Data on growth and age at first reproduction were compiled from 41 populations in eastern North America. Data reliability was checked by a redetermination of ages based on scale examination. The proportion of fish that were incorrectly aged was small (°0.7%); however, aging errors were primarily of one kind; salmon that had previously spawned were misclassified as virgin fish of an older age class. Growth rate at sea was found not to be positively correlated with age at maturation. Schaffer and Elson's (1975) positive correlation between growth and age at first reproduction can be attributed to a subtle statistical artifact caused by aging errors. We also found that within-population variation of age at maturation was not related to latitude. We conclude that tests of life history theories should not assume constancy in life history traits, such as mortality, among populations.

Indicators of AEI applied to the Delaware Estuary.

We evaluated the impacts of entrainment and impingement at the Salem Generating Station on fish populations and communities in the Delaware Estuary. In the absence of an agreed-upon regulatory definition of "adverse environmental impact" (AEI), we developed three independent benchmarks of AEI based on observed or predicted changes that could threaten the sustainability of a population or the integrity of a community. Our benchmarks of AEI included: (1) disruption of the balanced indigenous community of fish in the vicinity of Salem (the "BIC" analysis); (2) a continued downward trend in the abundance of one or more susceptible fish species (the "Trends" analysis); and (3) occurrence of entrainment/impingement mortality sufficient, in combination with fishing mortality, to jeopardize the future sustainability of one or more populations (the "Stock Jeopardy" analysis). The BIC analysis utilized nearly 30 years of species presence/absence data collected in the immediate vicinity of Salem. The Trends analysis examined three independent data sets that document trends in the abundance of juvenile fish throughout the estuary over the past 20 years. The Stock Jeopardy analysis used two different assessment models to quantify potential long-term impacts of entrainment and impingement on susceptible fish populations. For one of these models, the compensatory capacities of the modeled species were quantified through meta-analysis of spawner-recruit data available for several hundred fish stocks. All three analyses indicated that the fish populations and communities of the Delaware Estuary are healthy and show no evidence of an adverse impact due to Salem. Although the specific models and analyses used at Salem are not applicable to every facility, we believe that a weight of evidence approach that evaluates multiple benchmarks of AEI using both retrospective and predictive methods is the best approach for assessing entrainment and impingement impacts at existing facilities.

Hierarchical state-space estimation of leatherback turtle navigation ability.

Remotely sensed tracking technology has revealed remarkable migration patterns that were previously unknown; however, models to optimally use such data have developed more slowly. Here, we present a hierarchical Bayes state-space framework that allows us to combine tracking data from a collection of animals and make inferences at both individual and broader levels. We formulate models that allow the navigation ability of animals to be estimated and demonstrate how information can be combined over many animals to allow improved estimation. We also show how formal hypothesis testing regarding navigation ability can easily be accomplished in this framework. Using Argos satellite tracking data from 14 leatherback turtles, 7 males and 7 females, during their southward migration from Nova Scotia, Canada, we find that the circle of confusion (the radius around an animal's location within which it is unable to determine its location precisely) is approximately 96 km. This estimate suggests that the turtles' navigation does not need to be highly accurate, especially if they are able to use more reliable cues as they near their destination. Moreover, for the 14 turtles examined, there is little evidence to suggest that male and female navigation abilities differ. Because of the minimal assumptions made about the movement process, our approach can be used to estimate and compare navigation ability for many migratory species that are able to carry electronic tracking devices.

Large-scale absence of sharks on reefs in the greater-Caribbean: a footprint of human pressures.

BACKGROUND: In recent decades, large pelagic and coastal shark populations have declined dramatically with increased fishing; however, the status of sharks in other systems such as coral reefs remains largely unassessed despite a long history of exploitation. Here we explore the contemporary distribution and sighting frequency of sharks on reefs in the greater-Caribbean and assess the possible role of human pressures on observed patterns. METHODOLOGY/PRINCIPAL FINDINGS: We analyzed 76,340 underwater surveys carried out by trained volunteer divers between 1993 and 2008. Surveys were grouped within one km2 cells, which allowed us to determine the contemporary geographical distribution and sighting frequency of sharks. Sighting frequency was calculated as the ratio of surveys with sharks to the total number of surveys in each cell. We compared sighting frequency to the number of people in the cell vicinity and used population viability analyses to assess the effects of exploitation on population trends. Sharks, with the exception of nurse sharks occurred mainly in areas with very low human population or strong fishing regulations and marine conservation. Population viability analysis suggests that exploitation alone could explain the large-scale absence; however, this pattern is likely to be exacerbated by additional anthropogenic stressors, such as pollution and habitat degradation, that also correlate with human population. CONCLUSIONS/SIGNIFICANCE: Human pressures in coastal zones have lead to the broad-scale absence of sharks on reefs in the greater-Caribbean. Preventing further loss of sharks requires urgent management measures to curb fishing mortality and to mitigate other anthropogenic stressors to protect sites where sharks still exist. The fact that sharks still occur in some densely populated areas where strong fishing regulations are in place indicates the possibility of success and encourages the implementation of conservation measures.

Declining wild salmon populations in relation to parasites from farm salmon.

Rather than benefiting wild fish, industrial aquaculture may contribute to declines in ocean fisheries and ecosystems. Farm salmon are commonly infected with salmon lice (Lepeophtheirus salmonis), which are native ectoparasitic copepods. We show that recurrent louse infestations of wild juvenile pink salmon (Oncorhynchus gorbuscha), all associated with salmon farms, have depressed wild pink salmon populations and placed them on a trajectory toward rapid local extinction. The louse-induced mortality of pink salmon is commonly over 80% and exceeds previous fishing mortality. If outbreaks continue, then local extinction is certain, and a 99% collapse in pink salmon population abundance is expected in four salmon generations. These results suggest that salmon farms can cause parasite outbreaks that erode the capacity of a coastal ecosystem to support wild salmon populations.