J. Wilson White

Decision analysis for designing marine protected areas for multiple species with uncertain fishery status

Marine protected areas (MPAs) are growing in popularity as a conservation tool, and there are increasing calls for additional MPAs. Meta-analyses indicate that most MPAs successfully meet the minimal goal of increasing biomass inside the MPA, while some do not, leaving open the important question of what makes MPAs successful. An often-overlooked aspect of this problem is that the success of fishery management outside MPA boundaries (i.e., whether a population is overfished) affects how well MPAs meet both conservation goals (e.g., increased biomass) and economic goals (e.g., minimal negative effects on fishery yield). Using a simple example of a system with homogeneous habitat and periodically spaced MPAs, we show that, as area in MPAs increases, (1) conservation value (biomass) may initially be zero, implying no benefit, then at some point increases monotonically; and (2) fishery yield may be zero, then increases monotonically to a maximum beyond which further increase in MPA area causes yield to decline. Importantly, the points at which these changes in slope occur vary among species and depend on management outside MPAs. Decision makers considering the effects of a potential system of MPAs on multiple species are confronted by a number of such cost-benefit curves, and it is usually impossible to maximize benefits and minimize costs for all species. Moreover, the precise shape of each curve is unknown due to uncertainty regarding the fishery status of each species. Here we describe a decision-analytic approach that incorporates existing information on fishery stock status to present decision makers with the range of likely outcomes of MPA implementation. To summarize results from many species whose overfishing status is uncertain, our decision-analysis approach involves weighted averages over both overfishing uncertainty and species. In an example from an MPA decision process in California, USA, an optimistic projection of future fishery management success led to recommendation of fewer and smaller MPAs than that derived from a more pessimistic projection of future management success. This example illustrates how information on fishery status can be used to project potential outcomes of MPA implementation within a decision analysis framework and highlights the need for better population information.

Linking models with monitoring data for assessing performance of no-take marine reserves

No-take marine reserves are an increasingly popular conservation and management tool. Assessing reserve performance in an adaptive management framework ideally involves predicting the response of populations and communities to reserves (typically in the design process) and testing predicted outcomes against observations. Here we compare existing modeling and empirical studies on no-take marine reserves, and provide a prospectus for their future integration. Numerical models of ecological responses to reserves typically project longterm, steady-state interactions over the relatively broad spatial scales of larval dispersal, reserve configuration, fishing effort, and fish movement. Existing empirical studies focus on short-term outcomes over small scales, typically aggregated over many explanatory factors. Linking models and empirical data together for the adaptive management of marine reserves requires adjusting the spatial and temporal scales of models to match empirically feasible tests, and adjusting the metrics and scale of empirical studies to account for the interacting biological and human factors affecting reserve outcomes.

Synthesizing mechanisms of density dependence in reef fishes: behavior, habitat configuration, and observational scale

Coral and rocky reef fish populations are widely used as model systems for the experimental exploration of density-dependent vital rates, but patterns of density-dependent mortality in these systems are not yet fully understood. In particular, the paradigm for strong, directly density-dependent (DDD) postsettlement mortality stands in contrast to recent evidence for inversely density-dependent (IDD) mortality. We review the processes responsible for DDD and IDD per capita mortality in reef fishes, noting that the pattern observed depends on predator and prey behavior, the spatial configuration of the reef habitat, and the spatial and temporal scales of observation. Specifically, predators tend to produce DDD prey mortality at their characteristic spatial scale of foraging, but prey mortality is IDD at smaller spatial scales due to attack-abatement effects (e.g., risk dilution). As a result, DDD mortality may be more common than IDD mortality on patch reefs, which tend to constrain predator foraging to the same scale as prey aggregation, eliminating attack-abatement effects. Additionally, adjacent groups of prey on continuous reefs may share a subset of refuges, increasing per capita refuge availability and relaxing DDD mortality relative to prey on patch reefs, where the patch edge could prevent such refuge sharing. These hypotheses lead to a synthetic framework to predict expected mortality patterns for a variety of scenarios. For nonsocial, nonaggregating species and species that aggregate in order to take advantage of spatially clumped refuges, IDD mortality is possible but likely superseded by DDD refuge competition, especially on patch reefs. By contrast, for species that aggregate socially, mortality should be IDD at the scale of individual aggregations but DDD at larger scales. The results of nearly all prior reef fish studies fit within this framework, although additional work is needed to test many of the predicted outcomes. This synthesis reconciles some apparent contradictions in the recent reef fish literature and suggests the importance of accounting for the scale-sensitive details of predator and prey behavior in any study system.

Behavioral and energetic costs of group membership in a coral reef fish

Animals in social aggregations often spend more time foraging than solitary conspecifics. This may be a product of the relative safety afforded by aggregations: group members can devote more time to foraging and less time to antipredator behaviors than solitary animals (the “risk reduction” effect). All else being equal, risk reduction should result in higher food intake for grouped animals. However, intragroup competition may force group members to spend more time foraging in order to obtain the same food ration as solitary individuals (the “resource competition” effect). We compared these opposing explanations of foraging time allocation in a coral reef fish, bluehead wrasse (Thalassoma bifasciatum). Aggregations of juvenile bluehead wrasse experience safety-in-numbers, and preliminary observations suggested that juveniles in aggregations spent more time foraging for copepods in the water column than solitary juveniles. However, the risk reduction and resource competition hypotheses are indistinguishable on the basis of behavioral observations alone. Therefore, we collected behavioral, dietary, and growth data (using otolith growth rings) for bluehead wrasse at multiple reefs around a Caribbean island. Despite spending more time foraging in the water column, grouped fish did not capture more prey items and had slower growth rates than solitary fish. Thus, the increased foraging time of grouped fish appears to reflect resource competition, not risk reduction. This competition may limit the size and frequency of aggregations among juvenile bluehead wrasse, which have been shown to experience reduced mortality rates in larger groups. Bluehead wrasse recruits also spent less time foraging but grew faster at sites where planktonic copepod prey were more abundant. This suggests the possibility that large-scale spatiotemporal variability in the abundance of planktonic copepods over coral reefs may produce corresponding variability in the dynamics of reef fish populations.

Toxicity of a dissolved pyrethroid mixture to Hyalella azteca at environmentally relevant concentrations.

Use of pyrethroid pesticides, which are highly toxic to aquatic organisms, has increased substantially over the past decade. In 2006, the pyrethroid pesticides cyfluthrin and permethrin were measured in Sacramento-San Joaquin (SSJ) Delta (CA, USA) water at 5 and 24 ng/L (pptr), respectively. To elucidate any interactions between the two pyrethroids, a 10-d laboratory exposure was performed with 7- to 14-d-old amphipods (Hyalella azteca). Cyfluthrin and permethrin were tested singly and in combination at detected levels and also at half and twice the detected levels, both with and without the addition of 25 ppb of piperonyl butoxide (PBO). Mortality in all treatments was significantly higher than in controls, with the median lethal concentration (LC50) for permethrin with PBO (13.9 ng/L) and the LC50s with and without PBO for cyfluthrin (5.7 and 2.9 ng/L, respectively) at or below levels measured in SSJ Delta water samples. The LC50 for permethrin alone was estimated to be 48.9 ng/L. To evaluate combined toxicity, logistic regression models containing terms for concentrations of cyfluthrin, permethrin, and PBO, as well as models containing all possible combinations of these terms and interactions, were run and compared using Akaikes information criterion. The most parsimonious set of models indicated slight antagonism between cyfluthrin and permethrin. Results indicate that a dissolved mixture of cyfluthrin and permethrin is toxic at environmentally relevant concentrations in the water column.

Marine Population Connectivity: Reconciling Large-Scale Dispersal and High Self-Retention

Predicting connectivity patterns in systems with fluid transport requires descriptions of the spatial distribution of propagules. In contrast to research on terrestrial seed dispersal, where much attention has focused on localized physical factors affecting dispersal, studies of oceanic propagule dispersal have often emphasized the role of large-scale factors. We link these two perspectives by exploring how propagule dispersal in the ocean is influenced by the “coastal boundary layer” (CBL), a region of reduced velocities near the shoreline that might substantially modify local-scale dispersal. We used a simple simulation model to demonstrate that accounting for the CBL markedly alters transport distances, the widths of dispersal distributions, and the fraction of larvae retained near their sites of origin (self-retention). Median dispersal distances were up to 59% shorter in simulations with a CBL than in those without. Self-retention of larvae increased by up to 3 orders of magnitude in the presence of CBLs, but only minor changes arose in the long-distance tails of the distributions, resulting in asymmetric, non-Gaussian kernels analogous to those quantified for terrestrial seed dispersal. Because successfully settling larvae are commonly those that remain close to shore and interact with the CBL, ignoring this pervasive oceanographic feature will substantially alter predictions of population self-persistence, estimates of connectivity, and outcomes of metapopulation analyses.

From ‘Omics to Otoliths: Responses of an Estuarine Fish to Endocrine Disrupting Compounds across Biological Scales

Endocrine disrupting chemicals (EDCs) cause physiological abnormalities and population decline in fishes. However, few studies have linked environmental EDC exposures with responses at multiple tiers of the biological hierarchy, including population-level effects. To this end, we undertook a four-tiered investigation in the impacted San Francisco Bay estuary with the Mississippi silverside (Menidia audens), a small pelagic fish. This approach demonstrated links between different EDC sources and fish responses at different levels of biological organization. First we determined that water from a study site primarily impacted by ranch run-off had only estrogenic activity in vitro, while water sampled from a site receiving a combination of urban, limited ranch run-off, and treated wastewater effluent had both estrogenic and androgenic activity. Secondly, at the molecular level we found that fish had higher mRNA levels for estrogen-responsive genes at the site where only estrogenic activity was detected but relatively lower expression levels where both estrogenic and androgenic EDCs were detected. Thirdly, at the organism level, males at the site exposed to both estrogens and androgens had significantly lower mean gonadal somatic indices, significantly higher incidence of severe testicular necrosis and altered somatic growth relative to the site where only estrogens were detected. Finally, at the population level, the sex ratio was significantly skewed towards males at the site with measured androgenic and estrogenic activity. Our results suggest that mixtures of androgenic and estrogenic EDCs have antagonistic and potentially additive effects depending on the biological scale being assessed, and that mixtures containing androgens and estrogens may produce unexpected effects. In summary, evaluating EDC response at multiple tiers is necessary to determine the source of disruption (lowest scale, i.e. cell line) and what the ecological impact will be (largest scale, i.e. sex ratio).

MARKOV CHAIN MONTE CARLO METHODS FOR ASSIGNING LARVAE TO NATAL SITES USING NATURAL GEOCHEMICAL TAGS

Geochemical signatures deposited in otoliths are a potentially powerful means of identifying the origin and dispersal history of fish. However, current analytical methods for assigning natal origins of fish in mixed-stock analyses require knowledge of the number of potential sources and their characteristic geochemical signatures. Such baseline data are difficult or impossible to obtain for many species. A new approach to this problem can be found in iterative Markov Chain Monte Carlo (MCMC) algorithms that simultaneously estimate population parameters and assign individuals to groups. MCMC procedures only require an estimate of the number of source populations, and post hoc model selection based on the deviance information criterion can be used to infer the correct number of chemically distinct sources. We describe the basics of the MCMC approach and outline the specific decisions required when implementing the technique with otolith geochemical data. We also illustrate the use of the MCMC approach on simulated data and empirical geochemical signatures in otoliths from young-of-the-year and adult weakfish, Cynoscion regalis, from the U.S. Atlantic coast. While we describe how investigators can use MCMC to complement existing analytical tools for use with otolith geochemical data, the MCMC approach is suitable for any mixed-stock problem with a continuous, multivariate data.

Planktonic larval mortality rates are lower than widely expected

Fundamental knowledge of mortality during the planktonic phase of the typical marine life cycle is essential to understanding population dynamics and managing marine resources. However, estimating larval mortality is extremely challenging, because the fate of microscopic larvae cannot be tracked as they develop for weeks in ocean currents. We used a two-pronged approach to provide reliable estimates of larval mortality: (1) frequent, long-term sampling where the combination of larval behaviors and recirculation greatly reduces larval transport to and from the study area, and (2) an improved method of calculating larval mortality that consists of a vertical life table with a negative binomial distribution to account for the notorious patchiness of plankton. Larval mortality rates of our study species (barnacles and crabs) were ≤0.14 larvae/d, which produce survivorships over an order of magnitude higher than commonly determined for marine larvae. These estimates are reliable because they were similar for s...

Spatially Coupled Larval Supply of Marine Predators and Their Prey Alters the Predictions of Metapopulation Models

Oceanographic forces can strongly affect the movement of planktonic marine larvae, often producing predictable spatial patterns of larval delivery. In particular, recent empirical evidence suggests that in some coastal systems, certain locations consistently receive higher (or lower) larval supplies of both predators and their prey. As a consequence, rates of settlement and predation may be coupled spatially, a phenomenon I term the “coupled settlement effect.” To investigate the metapopulation consequences of this phenomenon, I created discrete‐time, patch‐based analytical and simulation models with a common larval pool and uneven larval supply among patches. Using two complementary measures of subpopulation value as a basis of comparison, I found that models with and without the coupled settlement effect yielded strikingly different predictions. When prey and predator larval supplies were not coupled, patches supplied with a larger proportion of the larval pool made a greater contribution to the metapopulation. When settlement of prey and predator was strongly coupled, however, the opposite was true: subpopulations with lower rates of larval supply (above some minimum) were more essential to metapopulation persistence. These considerations could facilitate more effective selection of sites for protection in marine reserves.