Population connectivity of the highly migratory shortfin mako (Isurus oxyrinchus Rafinesque 1810) and implications for management in the Southern Hemisphere

Published: 20 November 2018In this paper we combine analyses of satellite telemetry and molecular data to investigate spatial connectivity and genetic structure among populations of shortfin mako (Isurus oxyrinchus) in and around Australian waters, where this species is taken in recreational and commercial fisheries. Mitochondrial DNA data suggest matrilineal substructure across hemispheres, while nuclear DNA data indicate shortfin mako may constitute a globally panmictic population. There was generally high genetic connectivity within Australian waters. Assessing genetic connectivity across the Indian Ocean basin, as well as the extent that shortfin mako exhibit sex biases in dispersal patterns would benefit from future improved sampling of adult size classes, particularly of individuals from the eastern Indian Ocean. Telemetry data indicated that Australasian mako are indeed highly migratory and frequently make long-distance movements. However, individuals also exhibit fidelity to relatively small geographic areas for extended periods. Together these patterns suggest that shortfin mako populations may be genetically homogenous across large geographical areas as a consequence of few reproductively active migrants, although spatial partitioning exists. Given that connectivity appears to occur at different scales, management at both the national and regional levels seems most appropriate.Shannon Corrigan, Andrew D. Lowther, Luciano B. Beheregaray, Barry D. Bruce, Geremy Cliff, Clinton A. Duffy, Alan Foulis, Malcolm P. Francis, Simon D. Goldsworthy, John R. Hyde, Rima W. Jabado, Dovi Kacev, Lindsay Marshall, Gonzalo R. Mucientes, Gavin J. P. Naylor, Julian G. Pepperell, Nuno Queiroz, William T. White, Sabine P. Wintner and Paul J. Roger

Population Connectivity of the Highly Migratory Shortfin Mako (Isurus oxyrinchus Rafinesque 1810) and Implications for Management in the Southern Hemisphere

Copyright © 2018 Corrigan, Lowther, Beheregaray, Bruce, Cliff, Duffy, Foulis, Francis, Goldsworthy, Hyde, Jabado, Kacev, Marshall, Mucientes, Naylor, Pepperell, Queiroz, White, Wintner and Rogers. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.In this paper we combine analyses of satellite telemetry and molecular data to investigate spatial connectivity and genetic structure among populations of shortfin mako (Isurus oxyrinchus) in and around Australian waters, where this species is taken in recreational and commercial fisheries. Mitochondrial DNA data suggest matrilineal substructure across hemispheres, while nuclear DNA data indicate shortfin mako may constitute a globally panmictic population. There was generally high genetic connectivity within Australian waters. Assessing genetic connectivity across the Indian Ocean basin, as well as the extent that shortfin mako exhibit sex biases in dispersal patterns would benefit from future improved sampling of adult size classes, particularly of individuals from the eastern Indian Ocean. Telemetry data indicated that Australasian mako are indeed highly migratory and frequently make long-distance movements. However, individuals also exhibit fidelity to relatively small geographic areas for extended periods. Together these patterns suggest that shortfin mako populations may be genetically homogenous across large geographical areas as a consequence of few reproductively active migrants, although spatial partitioning exists. Given that connectivity appears to occur at different scales, management at both the national and regional levels seems most appropriate

Insights into the life history and ecology of a large shortfin mako shark Isurus oxyrinchus captured in southern California

In June 2013, a record-breaking female Isurus oxyrinchus (total length 373 cm, mass 600 kg) was captured by rod and reel off Huntington Beach, California, where it was subsequently donated to research and provided a rare opportunity to collect the first data for a female I. oxyrinchus of this size. Counts of vertebral band pairs estimate the shark to have been c. 22 years old, depending upon assumptions of band-pair deposition rates, and the distended uteri and spent ovaries indicated that this shark had recently given birth. The stomach contained a c. 4 year-old female California sea lion Zalophus californianus that confirmed the high trophic position of this large I. oxyrinchus, which was corroborated with the high levels of measured contaminants and tissue isotope analyses

Accounting for unobserved population dynamics and aging error in close‐kin mark‐recapture assessments

Abstract Obtaining robust estimates of population abundance is a central challenge hindering the conservation and management of many threatened and exploited species. Close‐kin mark‐recapture (CKMR) is a genetics‐based approach that has strong potential to improve the monitoring of data‐limited species by enabling estimates of abundance, survival, and other parameters for populations that are challenging to assess. However, CKMR models have received limited sensitivity testing under realistic population dynamics and sampling scenarios, impeding the application of the method in population monitoring programs and stock assessments. Here, we use individual‐based simulation to examine how unmodeled population dynamics and aging uncertainty affect the accuracy and precision of CKMR parameter estimates under different sampling strategies. We then present adapted models that correct the biases that arise from model misspecification. Our results demonstrate that a simple base‐case CKMR model produces robust estimates of population abundance with stable populations that breed annually; however, if a population trend or non‐annual breeding dynamics are present, or if year‐specific estimates of abundance are desired, a more complex CKMR model must be constructed. In addition, we show that CKMR can generate reliable abundance estimates for adults from a variety of sampling strategies, including juvenile‐focused sampling where adults are never directly observed (and aging error is minimal). Finally, we apply a CKMR model that has been adapted for population growth and intermittent breeding to two decades of genetic data from juvenile lemon sharks (Negaprion brevirostris) in Bimini, Bahamas, to demonstrate how application of CKMR to samples drawn solely from juveniles can contribute to monitoring efforts for highly mobile populations. Overall, this study expands our understanding of the biological factors and sampling decisions that cause bias in CKMR models, identifies key areas for future inquiry, and provides recommendations that can aid biologists in planning and implementing an effective CKMR study, particularly for long‐lived data‐limited species

Improving metabarcoding taxonomic assignment: A case study of fishes in a large marine ecosystem.

DNA metabarcoding is an important tool for molecular ecology. However, its effectiveness hinges on the quality of reference sequence databases and classification parameters employed. Here we evaluate the performance of MiFish 12S taxonomic assignments using a case study of California Current Large Marine Ecosystem fishes to determine best practices for metabarcoding. Specifically, we use a taxonomy cross-validation by identity framework to compare classification performance between a global database comprised of all available sequences and a curated database that only includes sequences of fishes from the California Current Large Marine Ecosystem. We demonstrate that the regional database provides higher assignment accuracy than the comprehensive global database. We also document a tradeoff between accuracy and misclassification across a range of taxonomic cutoff scores, highlighting the importance of parameter selection for taxonomic classification. Furthermore, we compared assignment accuracy with and without the inclusion of additionally generated reference sequences. To this end, we sequenced tissue from 597 species using the MiFish 12S primers, adding 252 species to GenBank's existing 550 California Current Large Marine Ecosystem fish sequences. We then compared species and reads identified from seawater environmental DNA samples using global databases with and without our generated references, and the regional database. The addition of new references allowed for the identification of 16 additional native taxa representing 17.0% of total reads from eDNA samples, including species with vast ecological and economic value. Together these results demonstrate the importance of comprehensive and curated reference databases for effective metabarcoding and the need for locus-specific validation efforts

Archived DNA reveals marine heatwave‐associated shifts in fish assemblages

Abstract Marine heatwaves can drive large‐scale shifts in marine ecosystems, but studying their impacts on whole species assemblages is difficult. Analysis combining microscopic observations with environmental DNA (eDNA) metabarcoding of the ethanol preservative of an ichthyoplankton biorepository spanning a 23 years time series captures major and sometimes unexpected changes to fish assemblages in the California Current Large Marine Ecosystem during and after the 2014–2016 Pacific Marine Heatwave. Joint modeling efforts reveal patterns of tropicalization with increases in southern, mesopelagic species and associated declines in commercially important temperate fish species (e.g., North Pacific Hake [Merluccius productus] and Pacific Sardine [Sardinops sagax]). Data show shifts in fisheries assemblages (e.g., Northern Anchovy, Engraulis mordax) even after the return to average water temperatures, corroborating ecosystem impacts found through multiple traditional surveys of this study area. Our innovative approach of metabarcoding preservative eDNA coupled with quantitative modeling leverages the taxonomic breadth and resolution of DNA sequences combined with microscopy‐derived ichthyoplankton identification to yield higher‐resolution, species‐specific quantitative abundance estimates. This work opens the door to economically reconstruct the historical dynamics of assemblages from modern and archived samples worldwide