The passage of California’s Marine Life Protection Act (1999) established what has become a global model, with 124 conserved areas (16% of state waters) and predicted network-level ecological benefits to California’s nearshore ecosystems. The designations explicitly called out the intended benefits from the network function of these marine protected areas (MPAs). Establishing the “network” benefits of marine conservation areas (e.g. replenishing fish populations both within the reserves and areas outside reserves that are open to fishing) has presented a difficult empirical challenge, primarily due to our limited ability to observe and document the movement of fish offspring within an MPA to populations beyond the boundaries of that MPA. This is especially true along the open coasts of California (some of the most productive marine ecosystems on earth), where currents can disperse young (larvae) vast distances. The development of new approaches to understand population connectivity (i.e. the movement of individuals between populations), their dynamics and the influence of oceanographic features is critically needed to evaluate the existing network and potentially to guide the design and siting of new MPAs, especially in the face of climate change.

Understanding connectivity between MPAs and adjacent fished areas is critical to the design of MPA networks and their ongoing management. The challenge of evaluating the function of MPA networks is one of scale. Because young (larvae) can be dispersed vast distances by ocean currents, it is very difficult to determine the spatial patterns of dispersal. Emerging methods that utilize relatively low-cost, next-generation DNA sequencing technologies, coupled with advanced analytical techniques, now allow us to identify larvae delivered along the coast back to the population where it originated. The significant gene sequencing advances and rapidly dropping costs have the potential to transform our ability to empirically evaluate the benefits of California’s MPA network and lay the groundwork for new tools in the siting and evaluation of MPAs globally.

The specific emerging approach that overcomes this limitation is large-scale genetic pedigree reconstruction, also known as close-kin mark and recapture (CKMR) or inter-generational tagging. Genetic profiles are a perfect tag, since every organism has an innate and individually specific genetic signature that can be ‘read’ with a non-lethally collected tissue sample. Moreover, they pass these ‘tags’ to their offspring, who can be identified in the same way and linked definitively together in pedigrees. Thus, if parents and young are sampled, the young can be traced back to where its parents reside.

Since many fishes can produce millions of offspring during their lifetime, this method expands the scope of a tagging effort by orders of magnitude. A single genotyped parent effectively provides tags for all of its offspring that are recovered through a genetic-based, large-scale parentage analysis. Since many fishes and other species that inhabit MPAs do not move very much during their adult lives, the distance between parents and offspring is an accurate and direct measure of lifetime movement or dispersal. The CKMR approach can also be applied to siblings, which can deepen our understanding of the extent of dispersal because full siblings originate in the same location. Any siblings that are recovered in a new area represent individual dispersal data points that paint the distribution of larval dispersal from a single parental source.

The combination of these new conceptual approaches with the emergence of rapid and low-cost DNA sequencing methods provides an unprecedented and novel opportunity to improve our knowledge of population connectivity in marine systems. The CKMR approach has been applied to refining stock assessments, notably in southern bluefin tuna, and shows tremendous promise for studying MPAs as well.

This Big Idea capitalizes on the emergence of these genetic methods and analytical techniques to study family relationships in the coastal ocean, a previously intractable undertaking, and uses that information to evaluate the efficacy of California’s MPA network. Demonstration of this family-level ability to monitor dispersal and connectivity will be a game-changing advance in our ability to understand MPA function. In fact, the California Department of Fish & Wildlife is required to report back to the State Legislature on the efficacy and functions of the MPA system in 2022. This study ideally timed to inform that report.

This effort is uniquely timed to leverage and significantly expand a prior investigation of population connectivity within Monterey Bay National Marine Sanctuary that received over $1 million from the National Science Foundation (NSF) and the National Oceanic and Atmospheric Administration (NOAA). That study genetically profiled over 6,000 kelp rockfish using novel genetic markers, termed microhaplotypes, that leverage the awesome power of high-throughput DNA sequencing and act as inter-generational genetic “tags.” These “tagged” offspring represent a tremendous leap in the capacity to document dispersal of larval kelp rockfish within and outside of MPAs. Rockfishes are ideal study species due to restricted distribution of adults to shallow kelp forests, their sedentary lifestyle following settlement, high abundance in the study area, high fecundity, and ease of sampling of adults and juveniles.

Geographic distribution of parent-offspring pairs revealed through pedigree reconstruction reflect patterns of larval dispersal and magnitude of connectivity among populations of these and other rocky reef fishes that have sedentary adults. The proposed study will significantly expand the extent of sampling to hopefully demonstrate the fisheries benefits from the Monterey Peninsula to Big Creek State Marine Conservation Area to the south and Natural Bridges State Marine Reserve to the north (roughly 120 kilometers of coastline in each direction). Estimates of dispersal will be used to validate predictions of larval dispersal from ocean circulation models specific to this region.

The investigators will evaluate how coastal ocean currents influence patterns of larval dispersal and population connectivity along the coast. They will analyze potential oceanographic conditions that enhance or restrict dispersal of juvenile kelp rockfish along the coast in the expanded study area. The anticipated documentation of the wider network effects of the MPA network represents an amazing leap forward in science of marine protection strategies like MPAs and exclusion zones. Furthermore, the deeper insights afforded by the massive increase in “tagged” individuals may inform our understanding of the reliance of populations for their replenishment from other populations and how those patterns may change with climate induced changing ocean conditions.

Mark Carr – Department of Ecology and Evolutionary Biology, University of California, Santa Cruz, CA USA

John Carlos Garza & Eric Anderson – Southwest Fisheries Science Center, NMFS and University of California, Santa Cruz, CA USA

• Accurately identifying closely related species as larvae and obtaining sufficiently large sample sizes continue to impede the study of dispersal in marine ecosystems. Many species of rockfishes will be trapped and sampled as part of the project and because of evolutionary and phenotypic similarity, visually discriminating them as juveniles is difficult. As mentioned above, microhaplotypes overcome this obstacle by simultaneously identifying multiple species of rockfish and matching parents with offspring, and other kin members, using large-scale parentage analysis.
• Despite the huge number of “marked” individuals from the genetic tags, given the significant expansion in the study area, sampling effort is still rather limited. The conclusiveness of unsuccessful sampling is difficult to evaluate.
• High front end costs for this work in other settings. While this type of close-kin mark and recapture work could guide siting of MPAs in other marine regions, the costs and time associated with sampling and genotyping at a high enough resolution may be prohibitive.