Hostname: page-component-78c5997874-j824f Total loading time: 0 Render date: 2024-11-12T02:11:05.535Z Has data issue: false hasContentIssue false
  • English
  • Français

Integrating parasite assemblages and host genetics for population discrimination in the black grouper (Mycteroperca bonaci) in natural protected areas of the northern Yucatan peninsula

Published online by Cambridge University Press:  27 April 2022

Harold Villegas-Hernández Open the ORCID record for Harold Villegas-Hernández [Opens in a new window] ,
Sergio Guillén-Hernández Open the ORCID record for Sergio Guillén-Hernández [Opens in a new window] ,
Carlos González-Salas ,
Dawrin Pech-Puch  and
Juan F. Espínola-Novelo
Harold Villegas-Hernández
Affiliation:
Departamento de Biología Marina, Universidad Autónoma de Yucatán, Km. 15.5, carretera Mérida-Xmatkuil, A.P. 4-116 Itzimná, C.P. 97100, Mérida, Yucatán, México
Sergio Guillén-Hernández*
Affiliation:
Departamento de Biología Marina, Universidad Autónoma de Yucatán, Km. 15.5, carretera Mérida-Xmatkuil, A.P. 4-116 Itzimná, C.P. 97100, Mérida, Yucatán, México
Carlos González-Salas
Affiliation:
Departamento de Biología Marina, Universidad Autónoma de Yucatán, Km. 15.5, carretera Mérida-Xmatkuil, A.P. 4-116 Itzimná, C.P. 97100, Mérida, Yucatán, México
Dawrin Pech-Puch
Affiliation:
Departamento de Biología Marina, Universidad Autónoma de Yucatán, Km. 15.5, carretera Mérida-Xmatkuil, A.P. 4-116 Itzimná, C.P. 97100, Mérida, Yucatán, México
Juan F. Espínola-Novelo
Affiliation:
Departamento de Biología Marina, Universidad Autónoma de Yucatán, Km. 15.5, carretera Mérida-Xmatkuil, A.P. 4-116 Itzimná, C.P. 97100, Mérida, Yucatán, México
*
Author for correspondence: Sergio Guillén-Hernández, E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

The population structure of the black grouper (Mycteroperca bonaci) from the northern Yucatan Peninsula was evaluated with a two-fold emphasis on the spatial scales (whether island or coastal localities), as well as the effects of protection based on three natural protected areas (NPA) with different categories. To this end, specimens were collected at each NPA: Celestun (Biosphere Reserve) and Dzilam (State NPA) which are coastal and Alacranes (National Park) which is an island. Population discrimination was carried out by means of intestinal helminth parasite infracommunities and the hosts’ genetic similarities, highlighting the contradictions or coincidences between approaches. The intestinal parasitic fauna was examined in 161 specimens, of which 150 were genetically characterized using microsatellite DNA markers. Three distinct parasite communities were observed, in which taxa mainly responsible for the differences were the digeneans Prosorhynchus atlanticus, Prosorhynchus sp., Lepidapedoides epinepheli and Hamacreadium mutabile as well as the acanthocephalan Gorgorhynchus sp. The hosts’ genotypes indicated three genetically separated subunits that deviated significantly from Hardy–Weinberg equilibrium, and genetic differences evidenced a structured population. Despite the expectation that island NPAs would be distinctive, the coastal locality of Dzilam was the most differentiated. The present recognition of population subunits would indicate the beneficial effects of preserving the gene pool variability of the coastal Dzilam subunit since it is, at present, the least restrictive NPA where unregulated fishing is still allowed. Thus, this study indicates fishing regulations should be strengthened (e.g. determine catch quotas or reduce fishing effort) to prevent diversity loss (whether biological or genetic) in these NPAs, particularly in Dzilam, which is probably the most threatened area.

Keywords

Black grouperDNA microsatellitesMycteroperca bonacinatural protected areasparasitespopulation discrimination
Type
Research Article
Information
Journal of the Marine Biological Association of the United Kingdom , Volume 101 , Issue 8 , December 2021 , pp. 1185 - 1195
Copyright
Copyright © Universidad Autónoma de Yucatán, 2022. Published by Cambridge University Press on behalf of Marine Biological Association of the United Kingdom

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Abaunza, P, Murta, AG, Campbell, N, Cimmaruta, R, Comesaña, AS, Dahle, G, Gallo, E, García Santamaría, MT, Gordo, LS, Iversen, SA, MacKenzie, K, Magoulas, A, Mattiucci, S, Molloy, J, Nascetti, G, Pinto, AL, Quinta, R, Ramos, P, Ruggi, A, Sanjuan, A, Santos, AT, Stransky, C and Zimmermann, C (2008) Considerations on sampling strategies for an holistic approach to stock identification: the example of the HOMSIR project. Fisheries Research 89, 104–113.CrossRefGoogle Scholar
Ablan, MCA (2006) Genetics and the study of fisheries connectivity in Asian developing countries. Fisheries Research 78, 158–168.CrossRefGoogle Scholar
Anderson, MJ (2001) A new method for non-parametric multivariate analysis of variance. Austral Ecology 26, 32–46.Google Scholar
Anderson, MJ, Gorley, RN and Clarke, RK (2005) PERMANOVA: Permutational Multivariate Analysis of Variance: A Computer Program. New Zeland: Department of Statistics, University of Auckland, 24 p.Google Scholar
Baldwin, RE, Banks, MA and Jacobson, KC (2012) Integrating fish and parasite data as a holistic solution for identifying the elusive stock structure of Pacific sardines (Sardinops sagax). Reviews in Fish Biology and Fisheries 22, 137–156.CrossRefGoogle Scholar
Balloux, F, Amos, W and Coulson, T (2004) Does heterozygosity estimate inbreeding in real populations? Molecular Ecology 13, 3021–3031.CrossRefGoogle ScholarPubMed
Beacham, TD, Pollard, S and Le, KD (2000) Microsatellite DNA population structure and stock identification of steelhead trout (Oncorhynchus mykiss) in the Nass and Skeena Rivers in northern British Columbia. Marine Biotechnology 2, 587–600.CrossRefGoogle ScholarPubMed
Beacham, TD, Wood, CC, Withler, RE, Le, KD and Miller, KM (1999) Application of microsatellite DNA variation to estimation of stock composition and escapement of Nass River sockeye salmon (Oncorhynchus nerka). Canadian Journal of Fisheries and Aquatic Sciences 56, 297–310.CrossRefGoogle Scholar
Begg, G and Waldman, J (1999) An holistic approach to fish stock identification. Fisheries Research 43, 35–44.CrossRefGoogle Scholar
Bergenius, MAJ, Mapstone, BD, Begg, GA and Murchie, CD (2005) The use of otolith chemistry to determine stock structure of three epinepheline serranid coral reef fishes on the Great Barrier Reef, Australia. Fisheries Research 72, 253–270.CrossRefGoogle Scholar
Bergh, MO and Getz, WM (1989) Stability and harvesting of competing populations with genetic variation in life history strategy. Theoretical Population Biology 36, 77–124.CrossRefGoogle Scholar
Berryman, AA (2002) Population: a central concept for ecology? Oikos 97, 439–442.CrossRefGoogle Scholar
Braicovich, PE, Irigoitia, MM, Bovcon, ND and Timi, JT (2021) Parasites of Percophis brasiliensis (Percophidae) benefited from fishery regulations: indicators of success for marine protected areas? Aquatic Conservation: Marine and Freshwater Ecosystems 31, 139–152.CrossRefGoogle Scholar
Brulé, T, Renán, X, Colés-Marrufo, T, Hauyon, Y, Tuz-Sulub, AN and Déniel, C (2003) Reproduction in the protogynous black grouper (Mycteroperca bonaci (Poey)) from the southern Gulf of Mexico. Fishery Bulletin 101, 463–475.Google Scholar
Bush, AO, Lafferty, KD, Lotz, JM and Shostak, AW (1997) Parasitology meets ecology on its own terms: Margolis et al. revisited. Journal of Parasitology 83, 575–583.Google Scholar
Cadrin, SX (2020) Defining spatial structure for fishery stock assessment. Fisheries Research 221, 105397.CrossRefGoogle Scholar
Cadrin, SX, Kerr, LA and Mariani, S (eds) (2014) Stock Identification Methods: Applications in Fishery Science, 2nd edn. Academic Press, ISBN: 9780123970039. 566 p.CrossRefGoogle Scholar
Campana, SE (1999) Chemistry and composition of fish otoliths: pathways, mechanisms and applications. Marine Ecology Progress Series 188, 263–297.CrossRefGoogle Scholar
Christie, MR, Johnson, DW, Stallings, CD and Hixon, MA (2010) Self-recruitment and sweepstakes reproduction amid extensive gene flow in a coral-reef fish. Molecular Ecology 19, 1042–1057.CrossRefGoogle Scholar
Clarke, KR and Gorley, RN (2015) Plymouth Routines in Multivariate Ecological Research (PRIMER-E) v7: User Manual/Tutorial. Plymouth: PRIMER-E.Google Scholar
Corander, J, Marttinen, P and Mäntyniemi, S (2006) A Bayesian method for identification of stock mixtures from molecular marker data. Fishery Bulletin 104, 550–558.Google Scholar
Coscia, I, Chopelet, J, Waples, RS, Mann, BQ and Mariani, S (2016) Sex change and effective population size: implications for population genetic studies in marine fish. Heredity 117, 251–258.CrossRefGoogle ScholarPubMed
Cowen, RK, Lwiza, KMMM, Sponaugle, S, Paris, CB and Olson, DB (2000) Connectivity of marine populations: open or closed? Science (New York, N.Y.) 287, 857–859.CrossRefGoogle ScholarPubMed
Cowen, RK, Paris, CB and Srinivasan, A (2006) Scaling of connectivity in marine populations. Science (New York, N.Y.) 311, 522 LP–522527.CrossRefGoogle ScholarPubMed
Crabtree, RE and Bullock, LH (1998) Age, growth and reproduction of black grouper, Mycteroperca bonaci, in Florida waters. Fishery Bulletin 96, 735–753.Google Scholar
de Buron, I and Nickol, BB (1994) Histopathological effects of the acanthocephalan Leptorhynchoides thecatus in the ceca of the green sunfish, Lepomis cyanellus. Transactions of the American Microscopical Society 113, 161.CrossRefGoogle Scholar
Díaz, F and George-Nascimento, M (2002) Estabilidad temporal de las infracomunidades de parásitos en la borrachilla Scartichthys viridis (Valenciennes, 1836) (Pisces: Blenniidae) en la costa central de Chile. Revista Chilena de Historia Natural 75, 641–664.CrossRefGoogle Scholar
DOF DOdelaF (2006) Actualización de la Carta Nacional Pesquera. México, DF: DOF.Google Scholar
DOF DOdelaF (2014) Plan de Manejo Pesquero de Mero (Epinephelus morio) y especies asociadas en la Península de Yucatán. Available at https://www.inapesca.gob.mx/portal/documentos/Planes-de-Manejo-Pesquero/Golfo/2014_11_25_MAT_sagarpa-PLAN-DE-MERO.pdf.Google Scholar
Doherty, PJ, Planes, S and Mather, P (1995) Gene flow and larval duration in seven species of fish from the Great Barrier Reef. Ecology 76, 2373–2391.CrossRefGoogle Scholar
Ellis, C and Williams, IC (1973) The longevity of some species of helminth parasites in naturally acquired infections of the lesser Black-backed Gull, Larus fuscus L., in Britain. Journal of Helminthology 47, 329–338.CrossRefGoogle ScholarPubMed
Enriquez, C, Mariño-Tapia, IJ and Herrera-Silveira, JA (2010) Dispersion in the Yucatan coastal zone: implications for red tide events. Continental Shelf Research 30, 127–137.CrossRefGoogle Scholar
Espínola-Novelo, JF, González-Salas, C, Guillén-Hernández, S and MacKenzie, K (2015) Metazoan parasite infracommunities of Mycteroperca bonaci (Poey, 1960) (Pisces: Epinephelidae) in reef and coastal environments off the coast of Yucatán, México. Acta Parasitologica 60(3), 476–484.CrossRefGoogle ScholarPubMed
Farmer, NA (2009) Reef fish movements and marine reserve designs. PhD dissertation, Rosenstiel School: University of Miami, 217 p.Google Scholar
Favoretto, F, Mascareñas-Osorio, I, León-Deniz, L, González-Salas, C, Pérez-España, H, Rivera-Higueras, M, Ruiz-Zárate, MÁ, Vega-Zepeda, A, Villegas-Hernández, H and Aburto-Oropeza, O (2020) Being isolated and protected is better than just being isolated: a case study from the Alacranes Reef, Mexico. Frontiers in Marine Science 7, 1–13.CrossRefGoogle Scholar
Flores, K and George-Nascimento, M (2009) Las infracomunidades de parásitos de dos especies de Scartichthys (Pisces: Blenniidae) en localidades cercanas del norte de Chile. Revista Chilena de Historia Natural 82, 63–71.CrossRefGoogle Scholar
Froese, R (2004) Keep it simple: three indicators to deal with overfishing. Fish and Fisheries 5, 86–91.CrossRefGoogle Scholar
Galindo, HM, Olson, DB and Palumbi, SR (2006) Seascape genetics: a coupled oceanographic-genetic model predicts population structure of Caribbean corals. Current Biology 16, 1622–1626.CrossRefGoogle ScholarPubMed
George-Nascimento, M (2000) Geographical variations in the jack mackerel Trachurus symmetricus murphyi populations in the southeastern Pacific Ocean as evidenced from the associated parasite communities. Journal of Parasitology 86, 929–932.CrossRefGoogle ScholarPubMed
González-Salas, C, Villegas-Hernández, H, Poot-López, GR, Pech-Puch, D, Guillén-Hernández, S and Barrera-Guzmán, A (2020) Genetic population structure of black grouper (Mycteroperca bonaci) in the northern coast of Yucatan. Regional Studies in Marine Science 37, 101327.CrossRefGoogle Scholar
Green, AL, Maypa, AP, Almany, GR, Rhodes, KL, Weeks, R, Abesamis, RA, Gleason, MG, Mumby, PJ and White, AT (2015) Larval dispersal and movement patterns of coral reef fishes, and implications for marine reserve network design. Biological Reviews 90, 1215–1247.CrossRefGoogle ScholarPubMed
Hellberg, ME, Burton, RS, Neigel, JE and Palumbi, SR (2002) Genetic assessment of connectivity among marine populations. Bulletin of Marine Science 70, 273–290.Google Scholar
Hemmer-Hansen, J, Nielsen, EEG, Grønkjær, P and Loeschcke, V (2007) Evolutionary mechanisms shaping the genetic population structure of marine fishes; lessons from the European flounder (Platichthys flesus L.). Molecular Ecology 16, 3104–3118.CrossRefGoogle Scholar
Ihssen, PE, Booke, HE, Casselman, JM, McGlade, JM, Payne, NR and Utter, FM (1981) Stock identification: materials and methods. Canadian Journal of Fisheries and Aquatic Sciences 38, 1838–1855.CrossRefGoogle Scholar
Jennings, S, Reynolds, JD and Polunin, NVC (1999) Predicting the vulnerability of tropical reef fishes to exploitation with phylogenies and life histories. Conservation Biology 13, 1466–1475.CrossRefGoogle Scholar
Johnston, MW and Bernard, AM (2017) A bank divided: quantifying a spatial and temporal connectivity break between the Campeche Bank and the northeastern Gulf of Mexico. Marine Biology 164(1), 1–15.CrossRefGoogle Scholar
Jones, P (2002) Marine protected area strategies: issues, divergences and the search for middle ground. Reviews in Fish Biology and Fisheries 11, 197–216.CrossRefGoogle Scholar
Jónsdóttir, IG, Campana, SE and Marteinsdottir, G (2006) Stock structure of Icelandic cod Gadus morhua L. based on otolith chemistry. Journal of Fish Biology 69, 136–150.CrossRefGoogle Scholar
Keener, P, Johnson, GD, Stender, BW, Brothers, EB and Beatty, HR (1988) Ingress of postlarval gag, Mycteroperca microlepis (Pisces: Serranidae), through a South Carolina barrier island inlet. Bulletin of Marine Science 42, 376–396.Google Scholar
Kennedy, CR (2006) Ecology of the Acanthocephala. Cambridge: Cambridge University Press.CrossRefGoogle Scholar
Lamothe-Argumedo, R (1997) Manual de técnicas para preparar y estudiar los parásitos de animales silvestres. Mexico, DF: AGT Editores, 43 p.Google Scholar
Lester, R and MacKenzie, K (2009) The use and abuse of parasites as stock markers for fish. Fisheries Research 97, 1–2.CrossRefGoogle Scholar
Lester, R and Moore, B (2015) Parasites as valuable stock markers for fisheries in Australasia, East Asia and the Pacific Islands. Parasitology 142, 36–53.CrossRefGoogle ScholarPubMed
MacKenzie, K (2002) Parasites as biological tags in population studies of marine organisms: an update. Parasitology 124, 153–163.CrossRefGoogle ScholarPubMed
MacKenzie, K and Abaunza, P (1998) Parasites as biological tags for stock discrimination of marine fish: a guide to procedures and methods. Fisheries Research 38, 45–56.CrossRefGoogle Scholar
MacKenzie, K and Abaunza, P (2014). Parasites as biological tags. In Cadrin, SX, Kerr, LA and Mariani, S (eds), Stock Identification Methods: Applications in Fishery Science, 2nd Edn. San Diego, CA: Elsevier Academic Press, pp. 185–203.CrossRefGoogle Scholar
MacKenzie, K, Campbell, N, Mattiucci, S, Ramos, P, Pinto, AL and Abaunza, P (2008) Parasites as biological tags for stock identification of Atlantic horse mackerel Trachurus trachurus L. Fisheries Research 89, 136–145.CrossRefGoogle Scholar
Marchal, P, Ulrich, C, Korsbrekke, K, Pastoors, M and Rackham, BD (2003) Annual trends in catchability and fish stock assessments. Scientia Marina 67, 63–73.Google Scholar
Marcogliese, DJ (2004) Parasites: small players with crucial roles in the ecological theater. EcoHealth 1, 151–164.CrossRefGoogle Scholar
Marcogliese, DJ, Albert, E, Gagnon, P and Sévigny, JM (2003) Use of parasites in stock identification of the deepwater redfish (Sebastes mentella) in the Northwest Atlantic. Fishery Bulletin 101, 183–188.Google Scholar
Merino, M (1997) Upwelling on the Yucatan Shelf: hydrographic evidence. Journal of Marine Systems 13, 101–121.CrossRefGoogle Scholar
Molinari, R and Morrison, J (1988) The separation of the Yucatan Current from the Campeche Bank and the intrusion of the loop current into the Gulf of Mexico. Journal of Geophysical Research 93, 10645–10654.CrossRefGoogle Scholar
Moore, B, Buckworth, R, Moss, H and Lester, R (2003) Stock discrimination and movements of narrow-barred Spanish mackerel across northern Australia as indicated by parasites. Journal of Fish Biology 63, 765–779.CrossRefGoogle Scholar
Muñoz-Muga, P and Muñoz, G (2010) Parasite communities of Scartichthys viridis (Pisces: Blenniidae) from Central Chile: locality vs. host length. Revista de Biología Marina y Oceanografía 45, 165–169.CrossRefGoogle Scholar
Murta, AG (2000) Morphological variation of horse mackerel (Trachurus trachurus) in the Iberian and North African Atlantic: implications for stock identification. ICES Journal of Marine Science 57, 1240–1248.CrossRefGoogle Scholar
Nei, M (1978) Estimation of average heterozygosity and genetic distance from a small number of individuals. Genetics 89(3), 583–590.CrossRefGoogle ScholarPubMed
Palumbi, SR (2003) Population genetics, demographic connectivity, and the design of marine reserves. Ecological Applications 13, 146–158.CrossRefGoogle Scholar
Pérez-Ruzafa, Á, González-Wangüemert, M, Lenfant, P, Marcos, C and García-Charton, JA (2006) Effects of fishing protection on the genetic structure of fish populations. Biological Conservation 129, 244–255.CrossRefGoogle Scholar
Pita, A, Casey, J, Hawkins, SJ, Villarreal, MR, Gutiérrez, MJ, Cabral, H, Carocci, F, Abaunza, P, Pascual, S and Presa, P (2016) Conceptual and practical advances in fish stock delineation. Fisheries Research 173, 185–193.CrossRefGoogle Scholar
Planes, S, Parroni, M and Chauvet, C (1998) Evidence of limited gene flow in three species of coral reef fishes in the lagoon of New Caledonia. Marine Biology 130, 361–368.Google Scholar
Poulin, R (2003) The decay of similarity with geographical distance in parasite communities of vertebrate hosts. Journal of Biogeography 30, 1609–1615.CrossRefGoogle Scholar
Poulin, R and Mouillot, D (2004) The evolution of taxonomic diversity in helminth assemblages of mammalian hosts. Evolutionary Ecology 18, 231–247.CrossRefGoogle Scholar
Pudovkin, AI, Zaykin, DV and Hedgecock, D (1996) On the potential for estimating the effective number of breeders from heterozygote-excess in progeny. Genetics 144, 383–387.CrossRefGoogle ScholarPubMed
Purcell, JF, Cowen, RK, Hughes, CR and Williams, DA (2006) Weak genetic structure indicates strong dispersal limits: a tale of two coral reef fish. Proceedings of the Royal Society B: Biological Sciences 273, 1483–1490.CrossRefGoogle ScholarPubMed
Quiroz-Martínez, B and Salgado-Maldonado, G (2013) Taxonomic distinctness and richness of helminth parasite assemblages of freshwater fishes in Mexican hydrological basins. PLoS ONE 8(9), e74419.CrossRefGoogle ScholarPubMed
Riginos, C and Victor, BC (2001) Larval spatial distribution and other early life-history characteristics predict genetic differentiation in eastern Pacific blennoid fishes. Proceedings of the Royal Society B: Biological Sciences 268, 1931–1936.CrossRefGoogle Scholar
Roques, S, Sévigny, JM and Bernatchez, L (2002) Genetic structure of deep-water redfish, Sebastes mentella, populations across the North Atlantic. Marine Biology 140, 297–307.Google Scholar
Ruiz-Castillo, E, Gomez-Valdes, J, Sheinbaum, J and Rioja-Nieto, R (2016) Wind-driven coastal upwelling and westward circulation in the Yucatan shelf. Continental Shelf Research 118, 63–76.CrossRefGoogle Scholar
Ruzzante, DE, Taggart, CT, Cook, D and Goddard, SV (1997) Genetic differentiation between inshore and offshore Atlantic cod (Gadus morhua) off Newfoundland: a test and evidence of temporal stability. Canadian Journal of Fisheries and Aquatic Sciences 54, 2700–2708.CrossRefGoogle Scholar
Salles, OC, Maynard, JA, Joannides, M, Barbu, CM, Saenz-Agudelo, P, Almany, GR, Berumen, ML, Thorrold, SR, Jones, GP and Planes, S (2015) Coral reef fish populations can persist without immigration. Proceedings of the Royal Society B: Biological Sciences 282, 1–9.Google ScholarPubMed
Sardella, N and Timi, JT (2004) Parasites of Argentine hake in the Argentine Sea: population and infracommunity structure as evidences for host stock discrimination. Journal of Fish Biology 65, 1472–1488.CrossRefGoogle Scholar
Shaklee, JB and Currens, KP (2003) Genetic stock identification and risk assessment. In Hallerman, EM (ed.), Population Genetics: Principles and Applications for Fisheries Scientists. Bethesda, MD: American Fisheries Society, pp. 291–328.Google Scholar
Slatkin, M (1995) A measure of population subdivision based on microsatellite allele frequencies. Genetics 139, 457–462.CrossRefGoogle ScholarPubMed
Stoeckel, S, Grange, J, Fernández-Manjarres, JF, Bilger, I, Frascaria-Lacoste, N and Mariette, S (2006) Heterozygote excess in a self-incompatible and partially clonal forest tree species – Prunus avium L. Molecular Ecology 15, 2109–2118.CrossRefGoogle Scholar
Stransky, C, Baumann, H, Fevolden, SE, Harbitz, A, Høie, H, Nedreaas, KH, Salberg, AB and Skarstein, TH (2008 a) Separation of Norwegian coastal cod and Northeast Arctic cod by outer otolith shape analysis. Fisheries Research 90, 26–35.CrossRefGoogle Scholar
Stransky, C, Murta, AG, Schlickeisen, J and Zimmermann, C (2008 b) Otolith shape analysis as a tool for stock separation of horse mackerel (Trachurus trachurus) in the Northeast Atlantic and Mediterranean. Fisheries Research 89, 159–166.CrossRefGoogle Scholar
Taylor, MS and Hellberg, ME (2003) Genetic evidence for local retention of pelagic larval in a Caribbean reef fish. Science (New York, N.Y.) 299, 107–109.Google Scholar
Thieltges, DW, Dolch, T, Krakau, M and Poulin, R (2010) Salinity gradient shapes distance decay of similarity among parasite communities in three marine fishes. Journal of Fish Biology 76, 1806–1814.CrossRefGoogle ScholarPubMed
Timi, JT and Lanfranchi, AL (2009) The metazoan parasite communities of the Argentinean sandperch Pseudopercis semifasciata (Pisces: Perciformes) and their use to elucidate the stock structure of the host. Parasitology 136, 1209–1219.CrossRefGoogle ScholarPubMed
Tracey, SR, Lyle, JM and Duhamel, G (2006) Application of elliptical Fourier analysis of otolith form as a tool for stock identification. Fisheries Research 77, 138–147.CrossRefGoogle Scholar
Turan, C, Oral, M, Ozturk, B and Duzgunes, E (2006) Morphometric and meristic variation between stocks of bluefish (Pomatomus saltatrix) in the Black, Marmara, Aegean and northeastern Mediterranean Seas. Fisheries Research 79, 139–147.CrossRefGoogle Scholar
Vasconcelos, J, Hermida, M, Saraiva, A, González, JA and Gordo, LS (2017) The use of parasites as biological tags for stock identification of blue jack mackerel, Trachurus picturatus, in the North-eastern Atlantic. Fisheries Research 193, 1–6.CrossRefGoogle Scholar
Williams, HH, MacKenzie, K and McCarthy, AM (1992) Parasites as biological indicators of the population biology, migrations, diet, and phylogenetics of fish. Reviews in Fish Biology and Fisheries 2(2), 144–176.CrossRefGoogle Scholar
Wood, CL and Lafferty, KD (2015) How have fisheries affected parasite communities? Parasitology 142, 134–144.CrossRefGoogle ScholarPubMed
Zatcoff, M, Ball, AO and Chapman, RW (2002) Characterization of polymorphic microsatellite loci from black grouper, Mycteroperca bonaci (Teleostei: Serranidae). Molecular Ecology Notes 2, 211–219.Google Scholar