Harnessing island-ocean connections to maximize marine benefits of island conservation.

Islands support unique plants, animals, and human societies found nowhere else on the Earth. Local and global stressors threaten the persistence of island ecosystems, with invasive species being among the most damaging, yet solvable, stressors. While the threat of invasive terrestrial mammals on island flora and fauna is well recognized, recent studies have begun to illustrate their extended and destructive impacts on adjacent marine environments. Eradication of invasive mammals and restoration of native biota are promising tools to address both island and ocean management goals. The magnitude of the marine benefits of island restoration, however, is unlikely to be consistent across the globe. We propose a list of six environmental characteristics most likely to affect the strength of land-sea linkages: precipitation, elevation, vegetation cover, soil hydrology, oceanographic productivity, and wave energy. Global databases allow for the calculation of comparable metrics describing each environmental character across islands. Such metrics can be used today to evaluate relative potential for coupled land-sea conservation efforts and, with sustained investment in monitoring on land and sea, can be used in the future to refine science-based planning tools for integrated land-sea management. As conservation practitioners work to address the effects of climate change, ocean stressors, and biodiversity crises, it is essential that we maximize returns from our management investments. Linking efforts on land, including eradication of island invasive mammals, with marine restoration and protection should offer multiplied benefits to achieve concurrent global conservation goals.

Protected fish spawning aggregations as self-replenishing reservoirs for regional recovery.

Dispersal of eggs and larvae from spawning sites is critical to the population dynamics and conservation of marine fishes. For overfished species like critically endangered Nassau grouper (Epinephelus striatus), recovery depends on the fate of eggs spawned at the few remaining aggregation sites. Biophysical models can predict larval dispersal, yet these rely on assumed values of key parameters, such as diffusion and mortality rates, which have historically been difficult or impossible to estimate. We used in situ imaging to record three-dimensional positions of individual eggs and larvae in proximity to oceanographic drifters released into egg plumes from the largest known Nassau grouper spawning aggregation. We then estimated a diffusion-mortality model and applied it to previous years' drifter tracks to evaluate the possibility of retention versus export to nearby sites within 5 days of spawning. Results indicate that larvae were retained locally in 2011 and 2017, with 2011 recruitment being a substantial driver of population recovery on Little Cayman. Export to a nearby island with a depleted population occurred in 2016. After two decades of protection, the population appears to be self-replenishing but also capable of seeding recruitment in the region, supporting calls to incorporate spawning aggregation protections into fisheries management.

Recovery of critically endangered Nassau grouper (Epinephelus striatus) in the Cayman Islands following targeted conservation actions.

Many large-bodied marine fishes that form spawning aggregations, such as the Nassau grouper (Epinephelus striatus), have suffered regional overfishing due to exploitation during spawning. In response, marine resource managers in many locations have established marine protected areas or seasonal closures to recover these overfished stocks. The challenge in assessing management effectiveness lies largely in the development of accurate estimates to track stock size through time. For the past 15 y, the Cayman Islands government has taken a series of management actions aimed at recovering collapsed stocks of Nassau grouper. Importantly, the government also partnered with academic and nonprofit organizations to establish a research and monitoring program (Grouper Moon) aimed at documenting the impacts of conservation action. Here, we develop an integrated population model of 2 Cayman Nassau grouper stocks based on both diver-collected mark-resight observations and video censuses. Using both data types across multiple years, we fit parameters for a state-space model for population growth. We show that over the last 15 y the Nassau grouper population on Little Cayman has more than tripled in response to conservation efforts. Census data from Cayman Brac, while more sparse, show a similar pattern. These findings demonstrate that spatial and seasonal closures aimed at rebuilding aggregation-based fisheries can foster conservation success.

Grouper source levels and aggregation dynamics inferred from passive acoustic localization at a multispecies spawning site.

Four species of grouper (family Epinephlidae), Red Hind (Epinephelus guttatus), Nassau (Epinephelus striatus), Black (Mycteroperca bonaci), and Yellowfin Grouper (Mycteroperca venenosa) share an aggregation site in Little Cayman, Cayman Islands and produce sounds while aggregating. Continuous observation of these aggregations is challenging because traditional diver or ship-based methods are limited in time and space. Passive acoustic localization can overcome this challenge for sound-producing species, allowing observations over long durations and at fine spatial scales. A hydrophone array was deployed in February 2017 over a 9-day period that included Nassau Grouper spawning. Passive acoustic localization was used to find positions of the grouper-produced calls recorded during this time, which enabled the measurement of call source levels and evaluation of spatiotemporal aspects of calling. Yellowfin Grouper had the lowest mean peak-to-peak (PP) call source level, and Nassau Grouper had the highest mean PP call source level (143.7 and 155.2 dB re: 1 µPa at 1 m for 70-170 Hz, respectively). During the days that Nassau Grouper spawned, calling peaked after sunset. Similarly, when Red Hind calls were abundant, calls were highest in the afternoon and evening. The measured source levels can be used to estimate communication and detection ranges and implement passive acoustic density estimation for these fishes.

A Bayesian nested patch occupancy model to estimate steelhead movement and abundance.

Anthropogenic impacts on riverine systems have, in part, led to management concerns regarding the population status of species using these systems. In an effort to assess the efficacy of restoration actions, and in order to improve monitoring of species of concern, managers have turned to PIT (passive integrated transponder) tag studies with in-stream detectors to monitor movements of tagged individuals throughout river networks. However, quantifying movements in a river network using PIT tag data with incomplete coverage and imperfect detections presents a challenge. We propose a flexible Bayesian analytic framework that models the imperfectly detected movements of tagged individuals in a nested PIT tag array river network. This model structure provides probabilistic estimates of up-stream migration routes for each tagged individual based on a set of underlying nested state variables. These movement estimates can be converted into abundance estimates when an estimate of abundance is available for a location within the river network. We apply the model framework to data from steelhead (Oncorhynchus mykiss) in the Upper Columbia River basin and evaluate model performance (precision/variance of simulated population sizes) as a function of population tagging rates and PIT tag array detection probability densities within the river system using a simulation framework. This simulation framework provides both model validation (precision) and the ability to evaluate expected performance improvements (variance) due to changes in tagging rates or PIT receiver array configuration. We also investigate the impact of different network configurations on model estimates. Results from such investigations can help inform decisions regarding future monitoring and management.

Allele-Specific Expression and Evolution of Gene Regulation Underlying Acute Heat Stress Response and Local Adaptation in the Copepod Tigriopus californicus.

Geographic variation in environmental temperature can select for local adaptation among conspecific populations. Divergence in gene expression across the transcriptome is a key mechanism for evolution of local thermal adaptation in many systems, yet the genetic mechanisms underlying this regulatory evolution remain poorly understood. Here we examine gene expression in 2 locally adapted Tigriopus californicus populations (heat tolerant San Diego, SD, and less tolerant Santa Cruz, SC) and their F1 hybrids during acute heat stress response. Allele-specific expression (ASE) in F1 hybrids was used to determine cis-regulatory divergence. We found that the number of genes showing significant allelic imbalance increased under heat stress compared to unstressed controls. This suggests that there is significant population divergence in cis-regulatory elements underlying heat stress response. Specifically, the number of genes showing an excess of transcripts from the more thermal tolerant (SD) population increased with heat stress while that number of genes with an SC excess was similar in both treatments. Inheritance patterns of gene expression also revealed that genes displaying SD-dominant expression phenotypes increase in number in response to heat stress; that is, across loci, gene expression in F1's following heat stress showed more similarity to SD than SC, a pattern that was absent in the control treatment. The observed patterns of ASE and inheritance of gene expression provide insight into the complex processes underlying local adaptation and thermal stress response.

Unifying error structures in commonly used biotracer mixing models.

Mixing models are statistical tools that use biotracers to probabilistically estimate the contribution of multiple sources to a mixture. These biotracers may include contaminants, fatty acids, or stable isotopes, the latter of which are widely used in trophic ecology to estimate the mixed diet of consumers. Bayesian implementations of mixing models using stable isotopes (e.g., MixSIR, SIAR) are regularly used by ecologists for this purpose, but basic questions remain about when each is most appropriate. In this study, we describe the structural differences between common mixing model error formulations in terms of their assumptions about the predation process. We then introduce a new parameterization that unifies these mixing model error structures, as well as implicitly estimates the rate at which consumers sample from source populations (i.e., consumption rate). Using simulations and previously published mixing model datasets, we demonstrate that the new error parameterization outperforms existing models and provides an estimate of consumption. Our results suggest that the error structure introduced here will improve future mixing model estimates of animal diet.

Phenotypic variation and selective mortality as major drivers of recruitment variability in fishes.

An individual's phenotype will usually influence its probability of survival. However, when evaluating the dynamics of populations, the role of selective mortality is not always clear. Not all mortality is selective, patterns of selective mortality may vary, and it is often unknown how selective mortality compares or interacts with other sources of mortality. As a result, there is seldom a clear expectation for how changes in the phenotypic composition of populations will translate into differences in average survival. We address these issues by evaluating how selective mortality affects recruitment of fish populations. First, we provide a quantitative review of selective mortality. Our results show that most of the mortality during early life is selective, and that variation in phenotypes can have large effects on survival. Next, we describe an analytical framework that accounts for variation in selection, while also describing the amount of selective mortality experienced by different cohorts recruiting to a single population. This framework is based on reconstructing fitness surfaces from phenotypic selection measurements, and can be employed for either single or multiple traits. Finally, we show how this framework can be integrated with models of density-dependent survival to improve our understanding of recruitment variability and population dynamics.

Using low volume eDNA methods to sample pelagic marine animal assemblages.

Environmental DNA (eDNA) is an increasingly useful method for detecting pelagic animals in the ocean but typically requires large water volumes to sample diverse assemblages. Ship-based pelagic sampling programs that could implement eDNA methods generally have restrictive water budgets. Studies that quantify how eDNA methods perform on low water volumes in the ocean are limited, especially in deep-sea habitats with low animal biomass and poorly described species assemblages. Using 12S rRNA and COI gene primers, we quantified assemblages comprised of micronekton, coastal forage fishes, and zooplankton from low volume eDNA seawater samples (n = 436, 380-1800 mL) collected at depths of 0-2200 m in the southern California Current. We compared diversity in eDNA samples to concurrently collected pelagic trawl samples (n = 27), detecting a higher diversity of vertebrate and invertebrate groups in the eDNA samples. Differences in assemblage composition could be explained by variability in size-selectivity among methods and DNA primer suitability across taxonomic groups. The number of reads and amplicon sequences variants (ASVs) did not vary substantially among shallow (<200 m) and deep samples (>600 m), but the proportion of invertebrate ASVs that could be assigned a species-level identification decreased with sampling depth. Using hierarchical clustering, we resolved horizontal and vertical variability in marine animal assemblages from samples characterized by a relatively low diversity of ecologically important species. Low volume eDNA samples will quantify greater taxonomic diversity as reference libraries, especially for deep-dwelling invertebrate species, continue to expand.

Anchovy boom and bust linked to trophic shifts in larval diet.

Although massive biomass fluctuations of coastal-pelagic fishes are an iconic example of the impacts of climate variability on marine ecosystems, the mechanisms governing these dynamics are often elusive. We construct a 45-year record of nitrogen stable isotopes measured in larvae of Northern Anchovy (Engraulis mordax) in the California Current Ecosystem to assess patterns in food chain length. Larval trophic efficiency associated with a shortened food chain increased larval survival and produced boom periods of high adult biomass. In contrast, when larval food chain length increased, and energy transfer efficiency decreased, the population crashed. We propose the Trophic Efficiency in Early Life (TEEL) hypothesis, which states that larval fishes must consume prey that confer sufficient energy for survival, to help explain natural boom-bust dynamics of coastal pelagic fishes. Our findings illustrate a potential for trophic indicators to generally inform larval survival and adult population dynamics of coastal-pelagic fishes.

Spatial ecology of the Giant Sea Bass, Stereolepis gigas, in a southern California kelp forest as determined by acoustic telemetry.

The fisheries history of the Giant Sea Bass, Stereolepis gigas (Telostei: Polyprionidae), is closely linked to its spatial ecology. Its overharvest is directly associated with formation of spatially distinct spawning aggregations during summer, while its subsequent recovery is hypothesized to be the result of spatially explicit gear restrictions. Understanding the spatial ecology of Giant Sea Bass is a key part of efforts to assess contemporary threats such as commercial harvest and incidental catch by recreational fisheries. In this study, we used acoustic telemetry to characterize Giant Sea Bass space use in the La Jolla kelp forest using an acoustic array that encompasses two marine protected areas (MPAs) and heavily trafficked recreational fishing grounds. Five of the seven fish we tagged remained in the La Jolla array for at least 6 months. Two fish were resident across multiple years, with one fish consistently detected for 4 years. Only one fish was detected in the broader network of regional acoustic receivers, moving north approximately 8 km to Del Mar. Most tagged fish had home ranges and core use areas indicating they spend considerable time outside MPAs, particularly in areas with high recreational fishing activity. During spawning season we detected fish less frequently in the La Jolla array and recorded higher movement rates. While the current MPA network in La Jolla by no means offers complete protection to this fish, it does appear to support long-term persistence of some individuals in a region of exceptionally high recreational fishing pressure.

Assessing the effects of large mobile predators on ecosystem connectivity.

Large predators are often highly mobile and can traverse and use multiple habitats. We know surprisingly little about how predator mobility determines important processes of ecosystem connectivity. Here we used a variety of data sources drawn from Palmyra Atoll, a remote tropical marine ecosystem where large predators remain in high abundance, to investigate how these animals foster connectivity. Our results indicate that three of Palmyra's most abundant large predators (e.g., two reef sharks and one snapper) use resources from different habitats creating important linkages across ecosystems. Observations of cross-system foraging such as this have important implications for the understanding of ecosystem functioning, the management of large-predator populations, and the design of conservation measures intended to protect whole ecosystems. In the face of widespread declines of large, mobile predators, it is important that resource managers, policy makers, and ecologists work to understand how these predators create connectivity and to determine the impact that their depletions may be having on the integrity of these linkages.

Habitat structure determines resource use by zooplankton in temperate lakes.

While the importance of terrestrial linkages to aquatic ecosystems is well appreciated, the degree of terrestrial support of aquatic consumers remains debated. Estimates of terrestrial contributions to lake zooplankton have omitted a key food source, phytoplankton produced below the mixed layer. We used carbon and nitrogen stable isotope data from 25 Pacific Northwest lakes to assess the relative importance of particulate organic matter (POM) from the mixed layer, below the mixed layer and terrestrial detritus to zooplankton. Zooplankton and deep POM were depleted in ¹³C relative to mixed layer POM in lakes that can support deep primary production. A Bayesian stable isotope mixing model estimated that terrestrial detritus contributed <5% to zooplankton production, and confirms the role of lake optical and thermal properties; deep POM accounted for up to 80% of zooplankton production in the clearest lakes. These results suggest terrestrial support of lake zooplankton production is trivial.

Effects of multiple levels of social organization on survival and abundance.

Identifying how social organization shapes individual behavior, survival, and fecundity of animals that live in groups can inform conservation efforts and improve forecasts of population abundance, even when the mechanism responsible for group-level differences is unknown. We constructed a hierarchical Bayesian model to quantify the relative variability in survival rates among different levels of social organization (matrilines and pods) of an endangered population of killer whales (Orcinus orca). Individual killer whales often participate in group activities such as prey sharing and cooperative hunting. The estimated age-specific survival probabilities and survivorship curves differed considerably among pods and to a lesser extent among matrilines (within pods). Across all pods, males had lower life expectancy than females. Differences in survival between pods may be caused by a combination of factors that vary across the population's range, including reduced prey availability, contaminants in prey, and human activity. Our modeling approach could be applied to demographic rates for other species and for parameters other than survival, including reproduction, prey selection, movement, and detection probabilities.

Modeling the past, present, and future distributions of endangered white abalone (Haliotis sorenseni) to inform recovery efforts in California.

White abalone (Haliotis sorenseni) was once commonly found in coastal waters of the Southern California Bight (SCB) and south to Punta Abreojos, Baja California, Mexico. During the 1970s, white abalone supported a commercial fishery, which reduced the population and resulted in the closure of the fishery in 1996. When population levels continued to decline, National Marine Fisheries Service (NMFS) listed the species as endangered under the Endangered Species Act. The California Department of Fish and Wildlife and NMFS began surveying the wild populations, propagating specimens in captivity, and protecting its seabed habitat. We modeled coarse-scale (17 x 17 km) historical (using fishery-dependent data [1955-1996]) and contemporary (using fishery-independent data [1996-2017]) distributions of white abalone throughout its historical domain using random forests and maximum entropy (MaxEnt), respectively, and its fine-scale (10 x 10 m) contemporary distribution (fishery-independent data) using MaxEnt. We also investigated potential outplanting habitat farther north under two scenarios of future climate conditions. The coarse-scale models identified potential regions to focus outplanting efforts within SCB while fine-scale models can inform population monitoring and outplanting activities in these particular areas. These models predict that areas north of Point Conception may become candidate outplant sites as seawater temperatures continue to rise in the future due to climate change. Collectively, these results provide guidance on the design and potential locations for experimental outplanting at such locations to ultimately improve methods and success of recovery efforts.

The rise in climate change-induced federal fishery disasters in the United States.

Commercial, recreational, and indigenous fisheries are critical to coastal economies and communities in the United States. For over three decades, the federal government has formally recognized the impact of fishery disasters via federal declarations. Despite these impacts, national syntheses of the dynamics, impacts, and causes of fishery disasters are lacking. We developed a nationwide Federal Fishery Disaster database using National Oceanic and Atmospheric Administration (NOAA) fishery disaster declarations and fishery revenue data. From 1989-2020, there were 71 federally approved fishery disasters (eleven are pending), which spanned every federal fisheries management region and coastal state in the country. To date, we estimate fishery disasters resulted in $2B (2019 USD) in Congressional allocations, and an additional, conservative estimate of $3.2B (2019 USD) in direct revenue loss. Despite this scale of impact, the disaster assistance process is largely ad hoc and lacks sufficient detail to properly assess allocation fairness and benefit. Nonetheless, fishery disasters increased in frequency over time, and the causes of disasters included a broad range of anthropogenic and environmental factors, with a recent shift to disasters now almost exclusively caused by extreme environmental events (e.g., marine heatwaves, hurricanes, and harmful algal blooms). Nationwide, 84.5% of fishery disasters were either partially or entirely attributed to extreme environmental events. As climate change drives higher rates of such extreme events, and as natural disaster assistance requests reach an all-time high, the federal system for fisheries disaster declaration and mitigation must evolve in order to effectively protect both fisheries sustainability and societal benefit.

Long-term participation in collaborative fisheries research improves angler opinions on marine protected areas.

Recent marine spatial planning efforts, including the management and monitoring of marine protected areas (MPAs), increasingly focus on the importance of stakeholder engagement. For nearly 15 years, the California Collaborative Fisheries Research Program (CCFRP) has partnered volunteer anglers with researchers, the fishing industry, and resource managers to monitor groundfishes in California's network of MPAs. While the program has succeeded in generating sustained biological observations, we know little about volunteer angler demography or the impact of participation on their perceptions and opinions on fisheries data or MPAs. In this study we surveyed CCFRP volunteers to learn about (a) volunteer angler demographics and attitudes toward groundfish management and stock health, (b) volunteer angler motivations for joining and staying in the program, and (c) whether participation in the program influenced volunteer angler opinions on the quality of fisheries data used in resource management and the establishment of MPAs in California. CCFRP volunteers were older and had higher fishing avidity than average within the California recreational angling community. Many self-identified as more conservation-minded than their peers in the recreational fishing community and had positive views of California groundfish management and stock health. Participation in science and giving back to fisheries resources were major motivating factors in their decision to become and remain CCFRP volunteers. Angler opinions toward MPAs were more positive after volunteering with CCFRP. Those who had volunteered for seven or more years with CCFRP were more likely than not to gain a positive opinion of MPAs. Our survey results provide evidence that long-term engagement of stakeholders in collaborative research positively influences stakeholder opinions regarding marine resource management, and highlights CCFRP's success in engaging citizen science stakeholders in collaborative fisheries research.

Improving Bayesian isotope mixing models: a response to Jackson et al. (2009).

We recently described a Bayesian framework for stable isotope mixing models and provided a software tool, MixSIR, for conducting such analyses (Ecol. Lett., 2008; 11:470). Jackson et al. (Ecol. Lett., 2009; 12:E1) criticized the performance of our software based on tests using simulated data. However, their simulation data were flawed, rendering claims of erroneous behaviour inaccurate. A re-evaluation of the MixSIR source code did, however, uncover two minor coding errors, which we have fixed. When data are correctly simulated according to eqns (1)-(4) in Jackson et al. (2009), MixSIR consistently and accurately estimated the proportional contribution of prey to a predator diet, and was surprisingly robust to additional unquantified error. Jackson et al. (2009) also suggested we use a Dirichlet prior on the source proportion parameters, which we agree with. Finally, Jackson et al. (2009) propose adding additional error parameters to our mixing model framework. We caution that such increases in model complexity should be evaluated based on data support.

Incorporating uncertainty and prior information into stable isotope mixing models.

Stable isotopes are a powerful tool for ecologists, often used to assess contributions of different sources to a mixture (e.g. prey to a consumer). Mixing models use stable isotope data to estimate the contribution of sources to a mixture. Uncertainty associated with mixing models is often substantial, but has not yet been fully incorporated in models. We developed a Bayesian-mixing model that estimates probability distributions of source contributions to a mixture while explicitly accounting for uncertainty associated with multiple sources, fractionation and isotope signatures. This model also allows for optional incorporation of informative prior information in analyses. We demonstrate our model using a predator-prey case study. Accounting for uncertainty in mixing model inputs can change the variability, magnitude and rank order of estimates of prey (source) contributions to the predator (mixture). Isotope mixing models need to fully account for uncertainty in order to accurately estimate source contributions.

Analyzing mixing systems using a new generation of Bayesian tracer mixing models.

The ongoing evolution of tracer mixing models has resulted in a confusing array of software tools that differ in terms of data inputs, model assumptions, and associated analytic products. Here we introduce MixSIAR, an inclusive, rich, and flexible Bayesian tracer (e.g., stable isotope) mixing model framework implemented as an open-source R package. Using MixSIAR as a foundation, we provide guidance for the implementation of mixing model analyses. We begin by outlining the practical differences between mixture data error structure formulations and relate these error structures to common mixing model study designs in ecology. Because Bayesian mixing models afford the option to specify informative priors on source proportion contributions, we outline methods for establishing prior distributions and discuss the influence of prior specification on model outputs. We also discuss the options available for source data inputs (raw data versus summary statistics) and provide guidance for combining sources. We then describe a key advantage of MixSIAR over previous mixing model software-the ability to include fixed and random effects as covariates explaining variability in mixture proportions and calculate relative support for multiple models via information criteria. We present a case study of Alligator mississippiensis diet partitioning to demonstrate the power of this approach. Finally, we conclude with a discussion of limitations to mixing model applications. Through MixSIAR, we have consolidated the disparate array of mixing model tools into a single platform, diversified the set of available parameterizations, and provided developers a platform upon which to continue improving mixing model analyses in the future.