{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2025,11,11]],"date-time":"2025-11-11T22:24:33Z","timestamp":1762899873057,"version":"3.37.3"},"reference-count":65,"publisher":"Springer Science and Business Media LLC","issue":"1","license":[{"start":{"date-parts":[[2020,1,28]],"date-time":"2020-01-28T00:00:00Z","timestamp":1580169600000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"},{"start":{"date-parts":[[2020,1,28]],"date-time":"2020-01-28T00:00:00Z","timestamp":1580169600000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"}],"content-domain":{"domain":["link.springer.com"],"crossmark-restriction":false},"short-container-title":["Sci Rep"],"abstract":"<jats:title>Abstract<\/jats:title><jats:p>The Northern spot shrimp,<jats:italic>Pandalus platyceros<\/jats:italic>, a protandric hermaphrodite of commercial importance in North America, is the primary target species for shrimp fisheries within Southeast Alaska. Fishery data obtained from the Alaska Department of Fish and Game indicate that spot shrimp populations have been declining significantly over the past 25 years. We collected spot shrimps in Southeast Alaska and measured reproductive-related morphological, gonadal and molecular changes during the entire life history. The<jats:italic>appendix masculina<\/jats:italic>, a major sexual morphological indicator, is indicative of the reproductive phase of the animal, lengthening during maturation from juvenile to the male phase and then gradually shortening throughout the transitional stages until its complete disappearance upon transformation to a female. This morphological change occurs in parallel with the degeneration of testicular tissue in the ovotestis and enhanced ovarian vitellogenesis. Moreover, we obtained the entire mRNA sequence of the yolk protein precursor, vitellogenin, and monitored its transcript levels throughout the entire shrimp life-cycle. Vitellogenin transcript levels in the hepatopancreas increased in the early transitional stage until reaching a peak prior to extruding eggs. Such transcriptomic analyses, coupled with a comprehensive description of the gonad, external sex characters and timing of the reproductive life history of spot shrimps contribute to a better understanding of the hermaphroditic reproduction process in the cold Southeast Alaskan waters. This knowledge can contribute to a revision of current conservation efforts to maintain wild populations sustainable for both commercial and ecological considerations.<\/jats:p>","DOI":"10.1038\/s41598-020-58262-6","type":"journal-article","created":{"date-parts":[[2020,1,28]],"date-time":"2020-01-28T11:03:18Z","timestamp":1580209398000},"update-policy":"https:\/\/doi.org\/10.1007\/springer_crossmark_policy","source":"Crossref","is-referenced-by-count":10,"title":["The protandric life history of the Northern spot shrimp Pandalus platyceros: molecular insights and implications for fishery management"],"prefix":"10.1038","volume":"10","author":[{"ORCID":"https:\/\/orcid.org\/0000-0003-1484-0310","authenticated-orcid":false,"given":"Tom","family":"Levy","sequence":"first","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Sherry L.","family":"Tamone","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Rivka","family":"Manor","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Esther D.","family":"Bower","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-4229-1059","authenticated-orcid":false,"given":"Amir","family":"Sagi","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"297","published-online":{"date-parts":[[2020,1,28]]},"reference":[{"key":"58262_CR1","doi-asserted-by":"publisher","first-page":"108","DOI":"10.1016\/j.fishres.2011.12.014","volume":"119","author":"AW Stoner","year":"2012","unstructured":"Stoner, A. W. Evaluating vitality and predicting mortality in spot prawn, Pandalus platyceros, using reflex behaviors. Fisheries Research 119, 108\u2013114 (2012).","journal-title":"Fisheries Research"},{"issue":"6","key":"58262_CR2","doi-asserted-by":"publisher","first-page":"1403","DOI":"10.1139\/f64-121","volume":"21","author":"THG Butler","year":"1964","unstructured":"Butler, T. H. G. Reproduction, and distribution of pandalid shrimps in British Columbia. Journal of the Fisheries Board of Canada 21(6), 1403\u20131452 (1964).","journal-title":"Journal of the Fisheries Board of Canada"},{"key":"58262_CR3","unstructured":"Smith, Q. T. & Gray, D. 2018 Report to the Board of Fisheries on Region 1 Shrimp Fisheries. Alaska Department of Fish and Game, Division of Sport Fish, Research and Technical Services; (2017)."},{"issue":"6","key":"58262_CR4","doi-asserted-by":"publisher","first-page":"889","DOI":"10.1071\/MF04256","volume":"56","author":"WG Macbeth","year":"2005","unstructured":"Macbeth, W. G., Broadhurst, M. K., Millar, R. B. & Smith, S. D. A. Increasing codend mesh openings: an appropriate strategy for improving the selectivity of penaeid fishing gears in an Australian estuary? Marine and Freshwater Research 56(6), 889\u2013900 (2005).","journal-title":"Marine and Freshwater Research"},{"issue":"6","key":"58262_CR5","doi-asserted-by":"publisher","first-page":"1519","DOI":"10.1111\/j.1523-1739.2010.01530.x","volume":"24","author":"TR McClanahan","year":"2010","unstructured":"McClanahan, T. R. Effects of fisheries closures and gear restrictions on fishing income in a Kenyan coral reef. Conservation Biology 24(6), 1519\u20131528 (2010).","journal-title":"Conservation Biology"},{"issue":"2\u20134","key":"58262_CR6","doi-asserted-by":"publisher","first-page":"403","DOI":"10.1016\/j.ecolmodel.2003.09.020","volume":"172","author":"D Zeller","year":"2004","unstructured":"Zeller, D. & Reinert, J. Modelling spatial closures and fishing effort restrictions in the Faroe Islands marine ecosystem. Ecological Modelling 172(2\u20134), 403\u2013420 (2004).","journal-title":"Ecological Modelling"},{"issue":"5548","key":"58262_CR7","doi-asserted-by":"publisher","first-page":"1920","DOI":"10.1126\/science.294.5548.1920","volume":"294","author":"CM Roberts","year":"2001","unstructured":"Roberts, C. M., Bohnsack, J. A., Gell, F., Hawkins, J. P. & Goodridge, R. Effects of marine reserves on adjacent fisheries. Science 294(5548), 1920\u20131923 (2001).","journal-title":"Science"},{"issue":"5682","key":"58262_CR8","doi-asserted-by":"publisher","first-page":"346","DOI":"10.1126\/science.1098222","volume":"305","author":"EK Pikitch","year":"2004","unstructured":"Pikitch, E. K. et al. Ecosystem-based fishery management. Science 305(5682), 346\u2013347 (2004).","journal-title":"Science"},{"issue":"1","key":"58262_CR9","doi-asserted-by":"publisher","first-page":"79","DOI":"10.1139\/f31-006","volume":"6","author":"AA Berkeley","year":"1930","unstructured":"Berkeley, A. A. The post-embryonic development of the common pandalids of British Columbia. Contributions to Canadian biology and fisheries 6(1), 79\u2013163 (1930).","journal-title":"Contributions to Canadian biology and fisheries"},{"issue":"2","key":"58262_CR10","doi-asserted-by":"publisher","first-page":"286","DOI":"10.2307\/1540101","volume":"137","author":"DL Hoffman","year":"1969","unstructured":"Hoffman, D. L. Development of androgenic glands of a protandric shrimp. Biological Bulletin 137(2), 286\u2013296 (1969).","journal-title":"Biological Bulletin"},{"issue":"1","key":"58262_CR11","first-page":"1","volume":"3","author":"A Kimker","year":"1996","unstructured":"Kimker, A., Donaldson, W. & Bechtol, W. R. Spot shrimp growth in Unakwik Inlet, Prince William Sound, Alaska. Alaska Fishery Research Bulletin 3(1), 1\u20138 (1996).","journal-title":"Alaska Fishery Research Bulletin"},{"issue":"38","key":"58262_CR12","doi-asserted-by":"publisher","first-page":"55","DOI":"10.1016\/S0065-2881(00)38003-8","volume":"38","author":"BI Bergstrom","year":"2000","unstructured":"Bergstrom, B. I. The biology of Pandalus. Advances in Marine Biology 38(38), 55\u2013245 (2000).","journal-title":"Advances in Marine Biology"},{"issue":"3\u20134","key":"58262_CR13","first-page":"65","volume":"35","author":"L Barr","year":"1973","unstructured":"Barr, L. Studies of spot shrimp, Pandalus platyceros, at Little Port Walter, Alaska. Marine Fisheries Review 35(3\u20134), 65\u201366 (1973).","journal-title":"Marine Fisheries Review"},{"key":"58262_CR14","unstructured":"Butler, T. H. Synopsis of biological data on the prawn Pandalus platyceros Brandt, 1851. Food and Agriculture Organization of the United Nations; (1965)."},{"key":"58262_CR15","volume-title":"Shrimp capture and culture fisheries of the United States.","author":"ES Iversen","year":"1993","unstructured":"Iversen, E. S., Allen, D. M. & Higman, J. B. Shrimp capture and culture fisheries of the United States. (Halsted Press, New York, 1993)."},{"issue":"4","key":"58262_CR16","doi-asserted-by":"publisher","first-page":"567","DOI":"10.2307\/1548071","volume":"4","author":"MG King","year":"1984","unstructured":"King, M. G. & Moffitt, R. B. The sexuality of tropical deep-water shrimps (Decapoda: Pandalidae). Journal of Crustacean Biology 4(4), 567\u2013571 (1984).","journal-title":"Journal of Crustacean Biology"},{"issue":"4","key":"58262_CR17","doi-asserted-by":"publisher","first-page":"442","DOI":"10.1016\/0016-6480(80)90049-0","volume":"41","author":"C Nagamine","year":"1980","unstructured":"Nagamine, C., Knight, A. W., Maggenti, A. & Paxman, G. Masculinization of female Macrobrachium rosenbergii (de Man) (Decapoda, Palaemonidae) by androgenic gland implantation. General and Comparative Endocrinology 41(4), 442\u2013457 (1980).","journal-title":"General and Comparative Endocrinology"},{"key":"58262_CR18","doi-asserted-by":"crossref","unstructured":"Tombes, A. S. & Foster, M. W. Growth of appendix masculina and appendix interna in juvenile Macrobrachium rosenbergii (De Man)(Decapoda, Caridea). Crustaceana Supplement, 179\u2013184 (1979).","DOI":"10.1163\/9789004629349_026"},{"issue":"5","key":"58262_CR19","doi-asserted-by":"publisher","first-page":"554","DOI":"10.1007\/s10126-016-9717-5","volume":"18","author":"T Levy","year":"2016","unstructured":"Levy, T. et al. A single injection of hypertrophied androgenic gland cells produces all-female aquaculture. Marine Biotechnology 18(5), 554\u2013563 (2016).","journal-title":"Marine Biotechnology"},{"issue":"3","key":"58262_CR20","doi-asserted-by":"publisher","first-page":"1278","DOI":"10.1210\/en.2008-0906","volume":"150","author":"T Ventura","year":"2009","unstructured":"Ventura, T. et al. Temporal silencing of an androgenic gland-specific insulin-like gene affecting phenotypical gender differences and spermatogenesis. Endocrinology 150(3), 1278\u20131286 (2009).","journal-title":"Endocrinology"},{"issue":"2","key":"58262_CR21","doi-asserted-by":"publisher","first-page":"251","DOI":"10.2307\/1540229","volume":"142","author":"DL Hoffman","year":"1972","unstructured":"Hoffman, D. L. Development of ovotestis and copulatory organs in a population of protandric shrimp, Pandalus platyceros Brandt from Lopez Sound, Washington. Biological Bulletin 142(2), 251\u2013& (1972).","journal-title":"Biological Bulletin"},{"issue":"5","key":"58262_CR22","doi-asserted-by":"publisher","first-page":"417","DOI":"10.1002\/jez.10083","volume":"292","author":"A Okuno","year":"2002","unstructured":"Okuno, A. et al. Deduced primary structure of vitellogenin in the giant freshwater prawn, Macrobrachium rosenbergii, and yolk processing during ovarian maturation. Journal of Experimental Zoology 292(5), 417\u2013429 (2002).","journal-title":"Journal of Experimental Zoology"},{"issue":"9","key":"58262_CR23","doi-asserted-by":"publisher","first-page":"1116","DOI":"10.1002\/cbic.201300152","volume":"14","author":"Z Roth","year":"2013","unstructured":"Roth, Z. et al. Identification of receptor-interacting regions of vitellogenin within evolutionarily conserved beta-sheet structures by using a peptide array. Chembiochem 14(9), 1116\u20131122 (2013).","journal-title":"Chembiochem"},{"issue":"1","key":"58262_CR24","doi-asserted-by":"publisher","first-page":"66","DOI":"10.1095\/biolreprod.107.066258","volume":"79","author":"SHK Tiu","year":"2008","unstructured":"Tiu, S. H. K., Benzie, J. & Chan, S. M. From hepatopancreas to ovary: molecular characterization of a shrimp vitellogenin receptor involved in the processing of vitellogenin. Biology of Reproduction 79(1), 66\u201374 (2008).","journal-title":"Biology of Reproduction"},{"issue":"10","key":"58262_CR25","doi-asserted-by":"publisher","first-page":"1037","DOI":"10.2108\/zsj.21.1037","volume":"21","author":"T Okumura","year":"2004","unstructured":"Okumura, T., Yoshida, K. & Nikaido, H. Ovarian development and hemolymph vitellogenin levels in laboratory-maintained protandric shrimp, Pandalus hypsinotus: measurement by a newly developed time-resolved fluoroimmunoassay (TR-FIA). Zoological Science 21(10), 1037\u20131047 (2004).","journal-title":"Zoological Science"},{"issue":"3","key":"58262_CR26","first-page":"465","volume":"41","author":"B Tsukimura","year":"2001","unstructured":"Tsukimura, B. Crustacean vitellogenesis: Its role in oocyte development. American Zoologist 41(3), 465\u2013476 (2001).","journal-title":"American Zoologist"},{"issue":"4","key":"58262_CR27","doi-asserted-by":"publisher","first-page":"1028","DOI":"10.1016\/j.cbpa.2007.03.011","volume":"147","author":"T Okumura","year":"2007","unstructured":"Okumura, T., Yamano, K. & Sakiyama, K. Vitellogenin gene expression and hemolymph vitellogenin during vitellogenesis, final maturation, and oviposition in female kuruma prawn, Marsupenaeus japonicus. Comparative Biochemistry and Physiology a-Molecular & Integrative Physiology 147(4), 1028\u20131037 (2007).","journal-title":"Comparative Biochemistry and Physiology a-Molecular & Integrative Physiology"},{"issue":"4","key":"58262_CR28","doi-asserted-by":"publisher","first-page":"678","DOI":"10.1046\/j.1444-2906.2000.00108.x","volume":"66","author":"T Okumura","year":"2000","unstructured":"Okumura, T. & Aida, K. Hemolymph vitellogenin levels and ovarian development during the reproductive and non reproductive molt cycles in the giant freshwater prawn Macrobrachium rosenbergii. Fisheries Science 66(4), 678\u2013685 (2000).","journal-title":"Fisheries Science"},{"issue":"3","key":"58262_CR29","doi-asserted-by":"publisher","first-page":"453","DOI":"10.1016\/0305-0491(94)90211-9","volume":"107","author":"CC Chen","year":"1994","unstructured":"Chen, C. C. & Chen, S. N. Vitellogenesis in the Giant Tiger Prawn, Penaeus monodon Fabricius, 1789. Comparative Biochemistry and Physiology B-Biochemistry & Molecular Biology 107(3), 453\u2013460 (1994).","journal-title":"Comparative Biochemistry and Physiology B-Biochemistry & Molecular Biology"},{"issue":"1","key":"58262_CR30","doi-asserted-by":"publisher","first-page":"39","DOI":"10.1016\/j.ygcen.2005.06.009","volume":"145","author":"S Raviv","year":"2006","unstructured":"Raviv, S., Parnes, S., Segall, C., Davis, C. & Sagi, A. Complete sequence of Litopenaeus vannamei (Crustacea: Decapoda) vitellogenin cDNA and its expression in endocrinologically induced sub-adult females. General and Comparative Endocrinology 145(1), 39\u201350 (2006).","journal-title":"General and Comparative Endocrinology"},{"issue":"1","key":"58262_CR31","doi-asserted-by":"publisher","first-page":"22","DOI":"10.1016\/j.gene.2014.12.008","volume":"562","author":"HK Bai","year":"2015","unstructured":"Bai, H. K. et al. Molecular characterization and developmental expression of vitellogenin in the oriental river prawn Macrobrachium nipponense and the effects of RNA interference and eyestalk ablation on ovarian maturation. Gene 562(1), 22\u201331 (2015).","journal-title":"Gene"},{"issue":"1","key":"58262_CR32","doi-asserted-by":"publisher","first-page":"138","DOI":"10.1095\/biolreprod.106.055483","volume":"77","author":"N Zmora","year":"2007","unstructured":"Zmora, N., Trant, J., Chan, S. M. & Chung, J. S. Vitellogenin and its messenger RNA during ovarian development in the female blue crab, Callinectes sapidus: gene expression, synthesis, transport, and cleavage. Biology of Reproduction 77(1), 138\u2013146 (2007).","journal-title":"Biology of Reproduction"},{"issue":"4","key":"58262_CR33","doi-asserted-by":"publisher","first-page":"459","DOI":"10.1016\/S0965-1748(03)00021-3","volume":"33","author":"MD Piulachs","year":"2003","unstructured":"Piulachs, M. D. et al. The vitellogenin of the honey bee, Apis mellifera: structural analysis of the cDNA and expression studies. Insect Biochemistry and Molecular Biology 33(4), 459\u2013465 (2003).","journal-title":"Insect Biochemistry and Molecular Biology"},{"issue":"1","key":"58262_CR34","doi-asserted-by":"publisher","first-page":"59","DOI":"10.1016\/0378-1119(96)00336-8","volume":"174","author":"N Mouchel","year":"1996","unstructured":"Mouchel, N., Trichet, V., Betz, A., LePennec, J. P. & Wolff, J. Characterization of vitellogenin from rainbow trout (Oncorhynchus mykiss). Gene 174(1), 59\u201364 (1996).","journal-title":"Gene"},{"issue":"3","key":"58262_CR35","doi-asserted-by":"publisher","first-page":"283","DOI":"10.1046\/j.1524-4725.2003.696.x","volume":"45","author":"S Yoshitome","year":"2003","unstructured":"Yoshitome, S. et al. Mr 25 000 protein, a substrate for protein serine\/threonine kinases, is identified as a part of Xenopus laevis vitellogenin B1. Development Growth & Differentiation 45(3), 283\u2013294 (2003).","journal-title":"Development Growth & Differentiation"},{"issue":"2","key":"58262_CR36","doi-asserted-by":"publisher","first-page":"245","DOI":"10.1016\/0022-2836(87)90688-7","volume":"196","author":"FD Vanhetschip","year":"1987","unstructured":"Vanhetschip, F. D. et al. Nucleotide sequence of a chicken vitellogenin gene and derived amino acid-sequence of the encoded yolk precursor protein. Journal of Molecular Biology 196(2), 245\u2013260 (1987).","journal-title":"Journal of Molecular Biology"},{"issue":"9","key":"58262_CR37","doi-asserted-by":"publisher","first-page":"1265","DOI":"10.1080\/002229399299914","volume":"33","author":"T Komai","year":"1999","unstructured":"Komai, T. A revision of the genus Pandalus (Crustacea: Decapoda: Caridea: Pandalidae). Journal of Natural History 33(9), 1265\u20131372 (1999).","journal-title":"Journal of Natural History"},{"issue":"2","key":"58262_CR38","doi-asserted-by":"publisher","first-page":"347","DOI":"10.1007\/s00227-005-0073-7","volume":"148","author":"T Okumura","year":"2005","unstructured":"Okumura, T. et al. Changes in gonadal development, androgenic gland cell structure, and hemolymph vitellogenin levels during male phase and sex change in laboratory-maintained protandric shrimp, Pandalus hypsinotus (Crustacea: Caridea: Pandalidae). Marine Biology 148(2), 347\u2013361 (2005).","journal-title":"Marine Biology"},{"key":"58262_CR39","doi-asserted-by":"publisher","first-page":"541","DOI":"10.1163\/156854006777584269","volume":"79","author":"DH Kim","year":"2006","unstructured":"Kim, D. H. et al. Gonad and androgenic gland development in relation to sexual morphology in Pandalopsis japonica Balss, 1914 (Decapoda, Pandalidae). Crustaceana 79, 541\u2013554 (2006).","journal-title":"Crustaceana"},{"issue":"4","key":"58262_CR40","doi-asserted-by":"publisher","first-page":"781","DOI":"10.1577\/1548-8659(1971)100<781:MOETAO>2.0.CO;2","volume":"100","author":"L Barr","year":"1971","unstructured":"Barr, L. Methods of estimating abundance of juvenile spot shrimp in a shallow nursery area. Transactions of the American Fisheries Society 100(4), 781\u2013+ (1971).","journal-title":"Transactions of the American Fisheries Society"},{"key":"58262_CR41","unstructured":"Mormorunni, C. L. The spot prawn fishery: a status report. Asia Pacific Environmental Exchange; (2001)."},{"key":"58262_CR42","unstructured":"Love, D. C. & Bishop, G. H. Pot shrimp stock assessment survey results from 1996\u20132003 in Districts 3, 7, 12, and 13 of Southeastern Alaska. Alaska Department of Fish and Game, Division of Sport Fish, Research and Technical Services; (2005)."},{"issue":"1\u20132","key":"58262_CR43","doi-asserted-by":"publisher","first-page":"8","DOI":"10.1016\/j.fishres.2008.02.003","volume":"93","author":"A Sala","year":"2008","unstructured":"Sala, A., Lucchetti, A., Piccinetti, C. & Ferretti, M. Size selection by diamond- and square-mesh codends in multi-species Mediterranean demersal trawl fisheries. Fisheries Research 93(1\u20132), 8\u201321 (2008).","journal-title":"Fisheries Research"},{"issue":"4","key":"58262_CR44","doi-asserted-by":"publisher","first-page":"413","DOI":"10.1139\/f72-068","volume":"29","author":"VA Price","year":"1972","unstructured":"Price, V. A. & Chew, K. K. Laboratory rearing of spot shrimp larvae (Pandalus platyceros) and descriptions of stages. Journal of the Fisheries Research Board of Canada 29(4), 413\u2013& (1972).","journal-title":"Journal of the Fisheries Research Board of Canada"},{"key":"58262_CR45","doi-asserted-by":"publisher","first-page":"193","DOI":"10.3354\/meps313193","volume":"313","author":"T Sato","year":"2006","unstructured":"Sato, T. & Goshima, S. Impacts of male-only fishing and sperm limitation in manipulated populations of an unfished crab, Hapalogaster dentata. Marine Ecology Progress Series 313, 193\u2013204 (2006).","journal-title":"Marine Ecology Progress Series"},{"issue":"5","key":"58262_CR46","doi-asserted-by":"publisher","first-page":"650","DOI":"10.1577\/1548-8659(1991)120<0650:NPCOIF>2.3.CO;2","volume":"120","author":"BD Smith","year":"1991","unstructured":"Smith, B. D. & Jamieson, G. S. Possible consequences of intensive fishing for males on the mating opportunities of Dungeness crabs. Transactions of the American Fisheries Society 120(5), 650\u2013653 (1991).","journal-title":"Transactions of the American Fisheries Society"},{"issue":"3","key":"58262_CR47","doi-asserted-by":"publisher","first-page":"655","DOI":"10.1139\/f96-308","volume":"54","author":"DG Hankin","year":"1997","unstructured":"Hankin, D. G., Butler, T. H., Wild, P. W. & Xue, Q. L. Does intense fishing on males impair mating success of female Dungeness crabs? Canadian Journal of Fisheries and Aquatic Sciences 54(3), 655\u2013669 (1997).","journal-title":"Canadian Journal of Fisheries and Aquatic Sciences"},{"issue":"1","key":"58262_CR48","doi-asserted-by":"publisher","first-page":"35","DOI":"10.1016\/S0169-5347(96)20109-0","volume":"12","author":"CM Roberts","year":"1997","unstructured":"Roberts, C. M. Ecological advice for the global fisheries crisis. Trends in Ecology & Evolution 12(1), 35\u201338 (1997).","journal-title":"Trends in Ecology & Evolution"},{"issue":"1\u20133","key":"58262_CR49","doi-asserted-by":"publisher","first-page":"1","DOI":"10.3354\/meps132001","volume":"132","author":"GR Russ","year":"1996","unstructured":"Russ, G. R. & Alcala, A. C. Do marine reserves export adult fish biomass? Evidence from Apo Island, central Philippines. Marine Ecology Progress Series 132(1\u20133), 1\u20139 (1996).","journal-title":"Marine Ecology Progress Series"},{"issue":"9","key":"58262_CR50","doi-asserted-by":"publisher","first-page":"2029","DOI":"10.1139\/f93-227","volume":"50","author":"JE Dugan","year":"1993","unstructured":"Dugan, J. E. & Davis, G. E. Applications of marine refugia to coastal fisheries management. Canadian Journal of Fisheries and Aquatic Sciences 50(9), 2029\u20132042 (1993).","journal-title":"Canadian Journal of Fisheries and Aquatic Sciences"},{"issue":"6","key":"58262_CR51","first-page":"363","volume":"22","author":"CM Roberts","year":"1993","unstructured":"Roberts, C. M. & Polunin, N. V. C. Marine reserves - simple solutions to managing complex fisheries. Ambio 22(6), 363\u2013368 (1993).","journal-title":"Ambio"},{"issue":"3","key":"58262_CR52","doi-asserted-by":"publisher","first-page":"205","DOI":"10.1002\/aqc.3270050305","volume":"5","author":"PK Dayton","year":"1995","unstructured":"Dayton, P. K., Thrush, S. F., Agardy, M. T. & Hofman, R. J. Environmental effects of marine fishing. Aquatic Conservation-Marine and Freshwater Ecosystems 5(3), 205\u2013232 (1995).","journal-title":"Aquatic Conservation-Marine and Freshwater Ecosystems"},{"key":"58262_CR53","doi-asserted-by":"crossref","unstructured":"Thurstan, R. H., Brockington, S. & Roberts, C. M. The effects of 118 years of industrial fishing on UK bottom trawl fisheries. Nature communications, 1 (2010).","DOI":"10.1038\/ncomms1013"},{"issue":"5352","key":"58262_CR54","doi-asserted-by":"publisher","first-page":"860","DOI":"10.1126\/science.279.5352.860","volume":"279","author":"D Pauly","year":"1998","unstructured":"Pauly, D., Christensen, V., Dalsgaard, J., Froese, R. & Torres, F. Fishing down marine food webs. Science 279(5352), 860\u2013863 (1998).","journal-title":"Science"},{"issue":"34","key":"58262_CR55","doi-asserted-by":"publisher","first-page":"201","DOI":"10.1016\/S0065-2881(08)60212-6","volume":"34","author":"S Jennings","year":"1998","unstructured":"Jennings, S. & Kaiser, M. J. The effects of fishing on marine ecosystems. Advances in Marine Biology 34(34), 201\u2013+ (1998).","journal-title":"Advances in Marine Biology"},{"issue":"2","key":"58262_CR56","doi-asserted-by":"publisher","first-page":"134","DOI":"10.1111\/j.1467-2979.2005.00183.x","volume":"6","author":"SJ Hall","year":"2005","unstructured":"Hall, S. J. & Mainprize, B. M. Managing by-catch and discards: how much progress are we making and how can we do better? Fish and Fisheries 6(2), 134\u2013155 (2005).","journal-title":"Fish and Fisheries"},{"key":"58262_CR57","doi-asserted-by":"publisher","first-page":"1","DOI":"10.2960\/J.v27.a1","volume":"27","author":"PJ Anderson","year":"2000","unstructured":"Anderson, P. J. Pandalid shrimp as indicators of ecosystem regime shift. Journal of Northwest Atlantic Fishery Science 27, 1\u201310 (2000).","journal-title":"Journal of Northwest Atlantic Fishery Science"},{"issue":"7","key":"58262_CR58","doi-asserted-by":"publisher","first-page":"671","DOI":"10.1038\/nmeth.2089","volume":"9","author":"CA Schneider","year":"2012","unstructured":"Schneider, C. A., Rasband, W. S. & Eliceiri, K. W. NIH Image to ImageJ: 25 years of image analysis. Nature Methods 9(7), 671\u2013675 (2012).","journal-title":"Nature Methods"},{"key":"58262_CR59","doi-asserted-by":"crossref","unstructured":"Levy, T., Rosen, O., Simons, O., Alkalay, A. S. & Sagi, A. The gene encoding the insulin-like androgenic gland hormone in an all-female parthenogenetic crayfish. Plos One, 12(12) (2017).","DOI":"10.1371\/journal.pone.0189982"},{"issue":"1","key":"58262_CR60","doi-asserted-by":"publisher","first-page":"231","DOI":"10.1093\/nar\/28.1.231","volume":"28","author":"J Schultz","year":"2000","unstructured":"Schultz, J., Copley, R. R., Doerks, T., Ponting, C. P. & Bork, P. SMART: a web-based tool for the study of genetically mobile domains. Nucleic Acids Research 28(1), 231\u2013234 (2000).","journal-title":"Nucleic Acids Research"},{"issue":"4","key":"58262_CR61","doi-asserted-by":"publisher","first-page":"772","DOI":"10.1093\/molbev\/mst010","volume":"30","author":"K Katoh","year":"2013","unstructured":"Katoh, K. & Standley, D. M. MAFFT multiple sequence alignment software version 7: Improvements in performance and usability. Molecular Biology and Evolution 30(4), 772\u2013780 (2013).","journal-title":"Molecular Biology and Evolution"},{"issue":"9","key":"58262_CR62","doi-asserted-by":"publisher","first-page":"2422","DOI":"10.1093\/molbev\/msx149","volume":"34","author":"V Lefort","year":"2017","unstructured":"Lefort, V., Longueville, J. E. & Gascuel, O. SMS: Smart model selection in PhyML. Molecular Biology and Evolution 34(9), 2422\u20132424 (2017).","journal-title":"Molecular Biology and Evolution"},{"issue":"3","key":"58262_CR63","first-page":"275","volume":"8","author":"DT Jones","year":"1992","unstructured":"Jones, D. T., Taylor, W. R. & Thornton, J. M. The rapid generation of mutation data matrices from protein sequences. Computer Applications in the Biosciences 8(3), 275\u2013282 (1992).","journal-title":"Computer Applications in the Biosciences"},{"issue":"6","key":"58262_CR64","doi-asserted-by":"publisher","first-page":"1547","DOI":"10.1093\/molbev\/msy096","volume":"35","author":"S Kumar","year":"2018","unstructured":"Kumar, S., Stecher, G., Li, M., Knyaz, C. & Tamura, K. MEGA X: molecular evolutionary genetics analysis across computing platforms. Molecular Biology and Evolution 35(6), 1547\u20131549 (2018).","journal-title":"Molecular Biology and Evolution"},{"issue":"1","key":"58262_CR65","doi-asserted-by":"publisher","first-page":"55","DOI":"10.1023\/B:EEST.0000011364.71236.f8","volume":"11","author":"M Liermann","year":"2004","unstructured":"Liermann, M., Steel, A., Rosing, M. & Guttorp, P. Random denominators and the analysis of ratio data. Environmental and Ecological Statistics 11(1), 55\u201371 (2004).","journal-title":"Environmental and Ecological Statistics"}],"container-title":["Scientific Reports"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.nature.com\/articles\/s41598-020-58262-6.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/www.nature.com\/articles\/s41598-020-58262-6","content-type":"text\/html","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/www.nature.com\/articles\/s41598-020-58262-6.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2024,7,30]],"date-time":"2024-07-30T19:59:17Z","timestamp":1722369557000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.nature.com\/articles\/s41598-020-58262-6"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2020,1,28]]},"references-count":65,"journal-issue":{"issue":"1","published-online":{"date-parts":[[2020,12]]}},"alternative-id":["58262"],"URL":"https:\/\/doi.org\/10.1038\/s41598-020-58262-6","relation":{},"ISSN":["2045-2322"],"issn-type":[{"type":"electronic","value":"2045-2322"}],"subject":[],"published":{"date-parts":[[2020,1,28]]},"assertion":[{"value":"18 September 2019","order":1,"name":"received","label":"Received","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"21 December 2019","order":2,"name":"accepted","label":"Accepted","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"28 January 2020","order":3,"name":"first_online","label":"First Online","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"The authors declare no competing interests.","order":1,"name":"Ethics","group":{"name":"EthicsHeading","label":"Competing interests"}}],"article-number":"1287"}}