Identifying Whitemouth Croaker (Micropogonias furnieri) Populations along the Rio de Janeiro Coast, Brazil, through Microsatellite and Otolith Analyses

Simple Summary The whitemouth croaker Micropogonias furnieri is an important fishery resource on the southwest Atlantic coast. Despite being heavily exploited, there are a few uncertainties regarding the population structure in the transition area between the tropical and warm temperate zones (South Brazilian Bight). In the State of Rio de Janeiro (the northern part of this area), local environmental conditions, such as an upwelling phenomena and large estuarine bays, together with contributions of continental drainage and anthropogenic activities, could determine different croaker populations. The aim of this study was to assess the fine-scale population structure of this species in three localities in Rio de Janeiro State (Brazil) and to compare it with previous studies that used different approaches. Through the combined use of genetic markers (nuclear microsatellites) and otolith signatures (morphometry and chemistry), two genotypic (North + Center/South) and three phenotypic (North + Center + South) populations were found. These results could contribute to a better understanding of the M. furnieri population dynamics and allow a rational management of this important fishing resource. Abstract The inshore area of the Southwestern Atlantic between 22 °S and 29 °S (South Brazilian Bight) is a transitional climatic zone, where the tropical and warm temperate provinces mix. In its northern part, i.e., in the coastal waters of Rio de Janeiro, Brazil, local oceanographic conditions, such as upwelling in the north, and great bays with different degrees of anthropogenic influences in the center and south can determine the population structure of several fish stocks. The Whitemouth croaker (Micropogonias furnieri) is one the most heavily exploited fishing resources in this area, but there are still some doubts about its population structure. In this study, through combined analyses using nuclear genetic markers and morphological and geochemical signatures of otoliths, a divergence of individuals between two populations was identified using microsatellites, while a finer spatial structure with three populations (north, center and south, respectively) was found based on otolith shapes and elemental signatures. This regional population structure may have direct implications for rational fisheries management and conservation of the species.

[1]  E. Avigliano Optimizing the Methodological Design in Fish Stock Delineation from Otolith Chemistry: Review of Spatio-Temporal Analysis Scales , 2021, Reviews in Fisheries Science & Aquaculture.

[2]  N. Miller,et al.  Population structure and habitat connectivity of Genidens genidens (Siluriformes) in tropical and subtropical coasts from Southwestern Atlantic , 2020 .

[3]  K. Hüssy,et al.  Trace Element Patterns in Otoliths: The Role of Biomineralization , 2020, Reviews in Fisheries Science & Aquaculture.

[4]  E. Froufe,et al.  Spatio-temporal microsatellite data suggest a multidirectional connectivity pattern in the Trachurus picturatus metapopulation from the Northeast Atlantic , 2020 .

[5]  E. Froufe,et al.  Genetic diversity and population structure of the blue jack mackerel Trachurus picturatus across its western distribution. , 2019, Journal of fish biology.

[6]  A. Correia,et al.  Stock structure of Atlantic spadefish Chaetodipterus faber from Southwest Atlantic Ocean inferred from otolith elemental and shape signatures , 2019, Fisheries Research.

[7]  K. Glover,et al.  Genetic management of mixed-stock fisheries “real-time”: The case of the largest remaining cod fishery operating in the Atlantic in 2007–2017 , 2018, Fisheries Research.

[8]  J. Vieira,et al.  Regional patterns in species richness and taxonomic diversity of the nearshore fish community in the Brazilian coast , 2018, Estuarine, Coastal and Shelf Science.

[9]  S. Sánchez,et al.  Spatial segregation and connectivity in young and adult stages of Megaleporinus obtusidens inferred from otolith elemental signatures: Implications for management , 2018, Fisheries Research.

[10]  H. W. van der Veer,et al.  Movement, connectivity and population structure of the intertidal fish Lipophrys pholis as revealed by otolith oxygen and carbon stable isotopes , 2017 .

[11]  H. Cabral,et al.  Stock identification of tainha (Mugil liza) by analyzing stable carbon and oxygen isotopes in otoliths , 2017 .

[12]  M. Haimovici,et al.  Stocks and management units of Micropogonias furnieri (Desmarest, 1823) in southwestern Atlantic , 2016 .

[13]  P. Shaw,et al.  Molecular genetic, life‐history and morphological variation in a coastal warm‐temperate sciaenid fish: evidence for an upwelling‐driven speciation event , 2016 .

[14]  A. Correia,et al.  Habitat residency and movement patterns of Centropomus parallelus juveniles in a subtropical estuarine complex. , 2016, Journal of fish biology.

[15]  F. Bonhomme,et al.  Genetic population structure of the commercially most important demersal fish in the Southwest Atlantic: The whitemouth croaker (Micropogonias furnieri) , 2015 .

[16]  P. Shaw,et al.  Incipient genetic isolation of a temperate migratory coastal sciaenid fish (Argyrosomus inodorus) within the Benguela Cold Current system , 2015 .

[17]  Lísa Anne Libungan,et al.  ShapeR: An R Package to Study Otolith Shape Variation among Fish Populations , 2015, PloS one.

[18]  G. Velasco,et al.  Use of lapillus otolith microchemistry as an indicator of the habitat of Genidens barbus from different estuarine environments in the southwestern Atlantic Ocean , 2015, Environmental Biology of Fishes.

[19]  J. Vieira,et al.  Microsatellite variation and genetic structuring in Mugil liza (Teleostei: Mugilidae) populations from Argentina and Brazil , 2014 .

[20]  H. Cabral,et al.  Integrating microsatellite DNA markers and otolith geochemistry to assess population structure of European hake (Merluccius merluccius) , 2014 .

[21]  P. Shaw,et al.  Population Connectivity and Phylogeography of a Coastal Fish, Atractoscion aequidens (Sciaenidae), across the Benguela Current Region: Evidence of an Ancient Vicariant Event , 2014, PloS one.

[22]  J. Santora,et al.  Water and otolith chemistry identify exposure of juvenile rockfish to upwelled waters in an open coastal system , 2013 .

[23]  B. vonHoldt,et al.  STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method , 2012, Conservation Genetics Resources.

[24]  Rod Peakall,et al.  GenAlEx 6.5: genetic analysis in Excel. Population genetic software for teaching and research—an update , 2012, Bioinform..

[25]  M. Vignon Ontogenetic trajectories of otolith shape during shift in habitat use: Interaction between otolith growth and environment , 2012 .

[26]  R. Castilho,et al.  Population structure and connectivity of the European conger eel (Conger conger) across the north-eastern Atlantic and western Mediterranean: integrating molecular and otolith elemental approaches , 2012 .

[27]  L. Beheregaray,et al.  Climate‐driven genetic divergence of limpets with different life histories across a southeast African marine biogeographic disjunction: different processes, same outcome , 2011, Molecular ecology.

[28]  K. Limburg,et al.  Tracking Baltic hypoxia and cod migration over millennia with natural tags , 2011, Proceedings of the National Academy of Sciences.

[29]  Alfredo N. Pereira,et al.  Genetic structure of the white croaker, Micropogonias furnieri Desmarest 1823 (Perciformes: Sciaenidae) along Uruguayan coasts: contrasting marine, estuarine, and lacustrine populations , 2011, Environmental Biology of Fishes.

[30]  A. Piola,et al.  The influence of the Brazil and Malvinas Currents on the Southwestern Atlantic Shelf circulation , 2010 .

[31]  S. Campana,et al.  Integrated stock mixture analysis for continous and categorical data, with application to genetic- otolith combinations , 2010 .

[32]  M. Vignon,et al.  Environmental and genetic determinant of otolith shape revealed by a non-indigenous tropical fish. , 2010 .

[33]  S. Mariani,et al.  A comparison of otolith microchemistry and otolith shape analysis for the study of spatial variation in a deep-sea teleost, Coryphaenoides rupestris , 2010, Environmental Biology of Fishes.

[34]  I. Sampaio,et al.  Macrodon atricauda (Günther, 1880) (Perciformes: Sciaenidae), a valid species from the southwestern Atlantic, with comments on its conservation , 2010 .

[35]  K. Severin,et al.  Otolith chemistry analyses indicate that water Sr:Ca is the primary factor influencing otolith Sr:Ca for freshwater and diadromous fish but not for marine fish. , 2009 .

[36]  S. Campana,et al.  OTOLITH CHEMISTRY TO DESCRIBE MOVEMENTS AND LIFE-HISTORY PARAMETERS OF FISHES : HYPOTHESES, ASSUMPTIONS, LIMITATIONS AND INFERENCES , 2008 .

[37]  D. Günther,et al.  Interspecific variations of otolith chemistry in estuarine fish nurseries , 2008 .

[38]  H. Kubota,et al.  Multi-species regime shifts reflected in spawning temperature optima of small pelagic fish in the western North Pacific , 2008 .

[39]  B. Letcher,et al.  create: a software to create input files from diploid genotypic data for 52 genetic software programs , 2008, Molecular ecology resources.

[40]  S. Campana,et al.  Estimating contemporary early life‐history dispersal in an estuarine fish: integrating molecular and otolith elemental approaches , 2008, Molecular ecology.

[41]  Christophe Lett,et al.  Assessment of an environmental barrier to transport of ichthyoplankton from the southern to the northern Benguela ecosystems , 2007 .

[42]  Noah A. Rosenberg,et al.  CLUMPP: a cluster matching and permutation program for dealing with label switching and multimodality in analysis of population structure , 2007, Bioinform..

[43]  T. Hrbek,et al.  Population genetic structuring of the king weakfish, Macrodon ancylodon (Sciaenidae), in Atlantic coastal waters of South America: deep genetic divergence without morphological change , 2006, Molecular ecology.

[44]  M. Haimovici,et al.  Status of white croaker Micropogonias furnieri exploited in southern Brazil according to alternative hypotheses of stock discreetness , 2006 .

[45]  A. Cirelli,et al.  Otolith chemical composition as a useful tool for sciaenid stock discrimination in the south-western Atlantic , 2006 .

[46]  Aaron P. Wagner,et al.  ml‐relate: a computer program for maximum likelihood estimation of relatedness and relationship , 2006 .

[47]  J. A. Levy,et al.  Genetic structure of Brazilian populations of white mouth croaker Micropogonias furnieri (Perciformes : Sciaenidae) , 2006 .

[48]  P. Smouse,et al.  genalex 6: genetic analysis in Excel. Population genetic software for teaching and research , 2006 .

[49]  Peter Beerli,et al.  Comparison of Bayesian and maximum-likelihood inference of population genetic parameters , 2006, Bioinform..

[50]  R. Sturgeon,et al.  Certification of a fish otolith reference material in support of quality assurance for trace element analysis , 2005 .

[51]  G. Evanno,et al.  Detecting the number of clusters of individuals using the software structure: a simulation study , 2005, Molecular ecology.

[52]  Laurent Excoffier,et al.  Arlequin (version 3.0): An integrated software package for population genetics data analysis , 2005, Evolutionary bioinformatics online.

[53]  C. Oosterhout,et al.  Micro-Checker: Software for identifying and correcting genotyping errors in microsatellite data , 2004 .

[54]  J. Waters,et al.  Phylogeography of a high‐dispersal New Zealand sea‐star: does upwelling block gene‐flow? , 2004, Molecular ecology.

[55]  N. Rosenberg distruct: a program for the graphical display of population structure , 2003 .

[56]  Peter Beerli,et al.  Maximum likelihood estimation of a migration matrix and effective population sizes in n subpopulations by using a coalescent approach , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[57]  P. Donnelly,et al.  Inference of population structure using multilocus genotype data. , 2000, Genetics.

[58]  B. Morales-Nin Review of the growth regulation processes of otolith daily increment formation , 2000 .

[59]  Cynthia M. Jones,et al.  Strontium and barium uptake in aragonitic otoliths of marine fish , 2000 .

[60]  Markus Schuelke,et al.  An economic method for the fluorescent labeling of PCR fragments , 2000, Nature Biotechnology.

[61]  J. Largier,et al.  Demonstration of the onshore transport of larval invertebrates by the shoreward movement of an upwelling front , 2000 .

[62]  A. Soares-Gomes,et al.  Biogeographic and species richness patterns of gastropoda on the southwestern Atlantic. , 1999, Revista brasileira de biologia.

[63]  S. Thorrold,et al.  Analysis of otolith chemistry in Nassau grouper (Epinephelus striatus) from the Bahamas and Belize using solution-based ICP-MS , 1999, Coral Reefs.

[64]  R. Maggioni,et al.  Close genetic similarity among populations of the white croaker (Micropogonias furnieri) in the south and south-eastern Brazilian coast. I. Allozyme studies , 1998 .

[65]  S. Campana,et al.  Experimental assessment of the effect of temperature and salinity on elemental composition of otoliths using laser ablation ICPMS , 1995 .

[66]  François Rousset,et al.  GENEPOP (version 1.2): population genetic software for exact tests and ecumenicism , 1995 .

[67]  D. M. Ware,et al.  Biological Basis of Maturation and Spawning Waves in Pacific Herring (Clupea harengus pallasi) , 1989 .

[68]  Shirley A. Miller,et al.  A simple salting out procedure for extracting DNA from human nucleated cells. , 1988, Nucleic acids research.

[69]  A. Vazzoler Diversificação fisiológica e morfológica de Micropogon furnieri (Desmarest, 1822) ao sul de Cabo Frio, Brasil , 1971 .

[70]  Sven Ekman,et al.  Zoogeography of the sea , 1953 .

[71]  E. Pinto,et al.  Stock structure of the Brazilian sardine Sardinella brasiliensis from Southwest Atlantic Ocean inferred from otolith elemental signatures , 2022, Fisheries Research.

[72]  A. Correia,et al.  Population structure of the blue jack mackerel (Trachurus picturatus) in the NE Atlantic inferred from otolith microchemistry , 2018 .

[73]  P. Reis-Santos,et al.  Otolith chemistry in stock delineation: A brief overview, current challenges and future prospects , 2016 .

[74]  Alves Johnatas,et al.  Otoliths as a tool to study reef fish population structure from coastal islands of south Brazil , 2016 .

[75]  K. Limburg,et al.  In search of the dead zone: Use of otoliths for tracking fish exposure to hypoxia , 2015 .

[76]  S. Thorrold,et al.  Population differences in otolith chemistry have a genetic basis in Menidia menidia , 2011 .

[77]  A. Correia,et al.  Discrimination of Trisopterus luscus stocks in northern Portugal using otolith elemental fingerprints , 2011 .

[78]  E.,et al.  Chemistry and composition of fish otoliths : pathways , mechanisms and applications , 2006 .

[79]  F. G. Araújo,et al.  Use of a tropical bay in southeastern Brazil by juvenile and subadult Micropogonias furnieri (Perciformes, Sciaenidae) , 2003 .

[80]  K. Friedland,et al.  Use of Otolith Morphology in Stock Discriminations of Atlantic Salmon (Salmo salar) , 1994 .

[81]  E. Gonzalez-Rodriguez,et al.  Upwelling and downwelling at Cabo Frio (Brazil): comparison of biomass and primary production responses , 1992 .

[82]  Phan Van Ngan,et al.  Padrões eletroforéticos de proteínas gerais de cristalino de Micropogonias furnieri (Desmarest, 1823) da costa sudeste-sul do Brasil: estudo populacional , 1989 .

[83]  D. Secor,et al.  Somatic Growth Effects on the Otolith–Fish Size Relationship in Young Pond-reared Striped Bass, Morone saxatilis , 1989 .

[84]  V. Isaac Synopsis of biological data on the whitemouth croaker Micropogonias furnieri (Desmarest, 1823) , 1988 .

[85]  F. J. Palacio Revisión zoogeográfica marina del sur del Brasil , 1982 .