Award Abstract # 1260693
Integrative evaluation of larval dispersal and delivery in kelp rockfish using inter-generational genetic tagging, demography and oceanography

NSF Org: OCE
Division Of Ocean Sciences
Recipient: UNIVERSITY OF CALIFORNIA SANTA CRUZ
Initial Amendment Date: January 14, 2013
Latest Amendment Date: April 6, 2015
Award Number: 1260693
Award Instrument: Standard Grant
Program Manager: David Garrison
OCE
 Division Of Ocean Sciences
GEO
 Directorate for Geosciences
Start Date: March 1, 2013
End Date: June 30, 2017 (Estimated)
Total Intended Award Amount: $878,770.00
Total Awarded Amount to Date: $922,480.00
Funds Obligated to Date: FY 2013 = $878,770.00
FY 2014 = $21,990.00

FY 2015 = $21,720.00
History of Investigator:
  • Mark Carr (Principal Investigator)
    mhcarr@ucsc.edu
  • John Garza (Co-Principal Investigator)
  • Christopher Edwards (Co-Principal Investigator)
  • Eric Anderson (Co-Principal Investigator)
Recipient Sponsored Research Office: University of California-Santa Cruz
1156 HIGH ST
SANTA CRUZ
CA  US  95064-1077
(831)459-5278
Sponsor Congressional District: 19
Primary Place of Performance: Southwest Fisheries Science Center Santa Cruz
110 Shaffer Rd
Santa Cruz
CA  US  95060-5730
Primary Place of Performance
Congressional District:
19
Unique Entity Identifier (UEI): VXUFPE4MCZH5
Parent UEI:
NSF Program(s): BIOLOGICAL OCEANOGRAPHY
Primary Program Source: 01001314DB NSF RESEARCH & RELATED ACTIVIT
01001415DB NSF RESEARCH & RELATED ACTIVIT

01001516DB NSF RESEARCH & RELATED ACTIVIT
Program Reference Code(s): 9169, 9117, 9251
Program Element Code(s): 165000
Award Agency Code: 4900
Fund Agency Code: 4900
Assistance Listing Number(s): 47.050

ABSTRACT

The spatial structure and dynamics of coastal marine fish populations are strongly influenced by the transport and recruitment of larvae. However, the scale and patterns of larval dispersal are among the most difficult demographic parameters to quantify in marine systems, due to the inability to tag and track the movement of larvae. In particular, the extent of local retention of larvae versus regional dispersal to other locations and populations is currently a hotly debated topic in the field of marine ecology and has profound implications for the design and effectiveness of Marine Protected Areas (MPAs). The research will identify patterns of larval dispersal and use those patterns to test predictions of dispersal generated by state-of-the-art circulation models.

The PI team brings together ecologists, geneticists, statisticians, and oceanographers with expertise in population demography and field sampling, mark/recapture data from genetic tags, and empirical and model-based evaluation of oceanographic processes to answer the following questions. 1. Do observed patterns of dispersal and connectivity of larval kelp rockfish correspond to patterns predicted by high spatial resolution regional ocean circulation models? Model predictions will be tested empirically using larval settlement samples. Parentage analysis will be used to verify the occurrence of larvae derived from genetically tagged source populations. 2. Is there evidence for local retention of larval kelp rockfish within the study area? To test the hypothesis that local retention of juvenile kelp rockfish from source populations is greater than expected by existing larval transport models, the PIs will compare the proportion of recruits that are genetically identified to have been produced from within three focal sites with the proportion of larval production that was tagged in those sites. 3. Is the relative recruitment of recently settled kelp rockfish to focal sites in the study region proportionate to the relative larval production of those focal sites? The PIs will compare the proportion of tagged recruits with the proportion of larval production generated from tagged adults at varying spatial scales. They will use goodness of fit models to compare expected and observed connectivity matrices under varying hypotheses of larval dispersal. Alternatively, if the relative contribution of focal sites to larval replenishment of themselves, one another, and more distant populations is disproportionate to their relative production, can this discrepancy be explained by oceanographic processes that could facilitate particular trajectories of larval dispersal? To determine if differences in self recruitment and connectivity can be attributed to local oceanographic features, the PIs will examine spatial and temporal correlations between these features and the spatial distribution and timing of recruitment.

Broader Impacts: These include three elements: graduate and undergraduate interdisciplinary training, public outreach, and informing fisheries and conservation managers and policy makers. Graduate training in interdisciplinary science will be achieved through co-mentoring by PIs with expertise in population genetics, ecology and oceanography. Undergraduates will assist graduate students and faculty in all aspects of the study. Results will be disseminated to the general public through collaboration with the local University outreach center. Outreach to the fishing community will be through their involvement in the sampling program and through workshops facilitated by the Sea Grant advisor and the state collaborative fisheries program. Based on the PI's relationships with state and federal agencies, managers and policy makers will be directly informed of the results and their implications for management decisions.

PUBLICATIONS PRODUCED AS A RESULT OF THIS RESEARCH

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Anderson, EC, Ng, TC "Bayesian pedigree inference with small numbers of single nucleotide polymorphisms via a factor-graph representation." Theoretical Population Biology , v.107 , 2016 , p.39
Baetscher, D.S., A.J. Clemento, T.C. Ng, E.C. Anderson, and J.C. Garza "Microhaplotypes provide increased power from short-read DNA sequences for relationship inference." Molecular Ecology Resources , 2017 10.1111/1755-0998.12737
Bravington, Mark V.; Skaug, Hans J.; Anderson, Eric C. "Close-Kin Mark-Recapture." Statistical Science. , v.31 , 2016 , p.259 10.1214/16-STS552.
Carr, M.H., S.P. Robinson, C. Wahle, G. Davis, S. Kroll, S. Murray, E.J. Schumacker, and M. Williams "The central importance of ecological spatial connectivity to effective marine protected areas and to meeting the challenges of climate change in the marine environment." Aquatic Conservation , 2017
Hughes, B.B., R. Beas-Luna, A. Barner, K. Brewitt, D.R. Brumbaugh, E. Cerny-Chipman, S.L. Close, K.E. Coblentz, K. L. de Nesnera, S.T. Drobnitch, J.D. Figurski, B. Focht, J. Freiwald, M. Friedman, K.K. Heady, W.N. Heady, K.A. Karr, A. Hettinger, A. Johnso "Long-term ecological studies contribute disproportionately to advancing the science and informing policy." BioScience , v.67 , 2017 , p.271
Liebowitz, D.M., K.J. Nielsen,, J.E. Dugan, S.G. Morgan, D.P. Malone, J.L. Largier, D.M. Hubbard, M.H. Carr. "Ecosystem connectivity and trophic subsidies of sandy beach ecosystems." Ecosphere , v.7 , 2016 10.1002/ecs2.1503
White, J.W., K.J. Nickols, D.P.Malone, M.H. Carr, R.M. Starr, F. Cordoleani, M.L. Baskett, A. Hastings, L.W. Botsford. "Models for adaptive management: Methods for fitting state-space integral projection models to time series data." Ecological Applications. , v.26 , 2016 , p.2675

PROJECT OUTCOMES REPORT

Disclaimer

This Project Outcomes Report for the General Public is displayed verbatim as submitted by the Principal Investigator (PI) for this award. Any opinions, findings, and conclusions or recommendations expressed in this Report are those of the PI and do not necessarily reflect the views of the National Science Foundation; NSF has not approved or endorsed its content.

The vast majority of marine species produce young that are dispersed by ocean currents. Therefore, replenishment of local populations is dependent on both the transport of young produced elsewhere, and the retention of young in their native location. The relative contribution of these sources of young to replenishment of local populations has profound consequences for the ecology, evolution and management of marine species. Nonetheless it remains one of the most challenging questions in marine ecology and evolution. We explored this question with the kelp rockfish, Sebastes atrovirens, which is one of the most common fishes in kelp forests along the central coast of California. This is the first study to our knowledge that has identified and measured realized dispersal of a species with a substantial larval duration (two months) along the open coast of North America. As such, the study provides a critical proof-of-concept for our approach to measuring dispersal patterns for coastal marine fishes along continental coastlines. 

We sampled recruiting offspring (4,269) and reproductive adults (1,887) and, because kelp rockfish are largely sedentary following larval settlement, the distance between a reproductive adult and its settled offspring is a close approximation of its larval dispersal distance. We sampled in four areas (“local populations”) in southern Monterey Bay and Carmel Bay. We estimated the density of adults at each population from visual diver surveys each year and multiplied those densities by the area of rocky reef from high resolution seafloor maps to estimate the size of each adult population.  The resulting estimates of adult population size relative to the numbers of adults and young sampled, and parent-offspring matches detected in each year and each population allowed us to determine the contribution each population made to replenishing itself and other populations.

We identified a total of nine parent-offspring pairs, which were distributed throughout the study area. Dispersal trajectories included north to south, south to north and short distance events. Across the four-year study, we estimated that 8% of larvae recruiting within the study were produced by populations within the study region. However, this contribution varied markedly among the four years (0 to 13%). At the scale of subregions, approximating local populations, we detected self-replenishment at only one population (North Carmel Bay) in only one year (2014); however, the level of self-replenishment (8%) was surprisingly high for a species of such long larval duration along the open coast.

We also found 31 pairs of recently settled full siblings that were similarly spread throughout the study area. As with parent-offspring pairs, frequency of these sibling matches varied interannually with a corresponding pattern among the four years of the study. In addition, we identified a pair of adult siblings, and two pairs of siblings born in consecutive years, indicating either monogamy or long term sperm storage.

Together, the parent offspring matches and distribution of siblings indicate that kelp rockfish populations can be self-replenishing at a scale corresponding to an individual marine protected area (MPA), while simultaneously contributing to the replenishment of other MPAs and populations outside the MPA.  

The high dispersal potential and gene flow of the study species made highly accurate pedigree reconstruction more difficult and therefore required us to develop of an entirely novel set of genetic markers, methods and analytical framework. We leveraged the power of next generation DNA sequencing to develop a novel type of population genetic marker, the ‘microhaplotype’, that utilizes the same short read sequence data as traditional single nucleotide polymorphism (SNP) analyses, but has orders of magnitude more power for pedigree reconstruction. Our set of 96 microhaplotypes not only allowed us to identify parents and offspring and full siblings with high accuracy, but also to distinguish kelp rockfish from 48 other common co-occuring rockfish species. Many juvenile rockfish are visually indistinguishable, so this allowed us to identify the ~45% of sampled juveniles that were kelp rockfish and not other closely related species. This microhaplotype method is already being widely adopted in molecular ecology.

The project also required development of a high resolution nearshore ocean circulation model across the study region, achieved through grid nests from coarse resolution models resolving the California Current System coast-wide down to the Carmel and Monterey Bay regions, all using Regional Ocean Modeling System. The model allowed us to evaluate whether circulation patterns might explain the patterns of larval dispersal revealed by genetic sampling including higher levels of larval retention and sibling cohesion seen in one year of our study (2014). Highly variable ocean circulation enabled both local retention within and transient two-way exchange between Carmel Bay and southern Monterey Bay, consistent with genetic results. The nesting approach used in this study is now being applied to other projects examining nearshore coastal processes at very high resolution.


Last Modified: 03/05/2018
Modified by: Mark H Carr

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