Long-term changes in population dynamics and life history contribute to explain the resilience of a stock of Micropogonias furnieri (Sciaenidae, Teleostei) in the SW Atlantic

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Abstract

We analysed the long-term changes in the population dynamics and life history of whitemouth croaker (Micropogonias furnieri) off Southern Brazil, to understand how four decades of heavy fishing (1976–2017) has affected its population dynamics. In the first three decades, size and age structure were eroded with the loss of the larger (> 60 cm total length) and older (>20 yrs. old) individuals. Individual growth increased sharply until the early 2000s and stabilized thereafter. The age at first maturity decreased by one year for females, the total mortality (Z) increased three-fold, and the stock size decreased approximately 90 %. Despite changes in the population structure due to intense fishing and high exploitation rates, the landings remained high until the late 2000s and in the last decade decreased less than expected by a former stock assessment. The resilience of the stock can be explained by its life history traits: (i) high fecundity, (ii) multiple spawning events during a protracted reproductive season in coastal waters, (iii) large estuarine nursery grounds unaffected by industrial fishing and (iv) faster growth and earlier sexual maturation due to the reduction in food competition and possibly evolution via gear selectivity. However, the stabilization of individual growth rates, the high rate of exploitation and the low spawning potential warn of the risk of further population decline and fishery collapse if intense fishing pressure continues.

Introduction

High fishing intensity across the world has altered the dynamics and underlying biological compositions of many marine fish populations (Myers et al., 1995; Audzijonyte et al., 2016). Understanding these changes in relation to life history variability is important when specifying stock assessment models that inform decisions supporting sustainable fisheries management (Longhurst, 2010).

Changes in the population structure due to high fishing intensity reduce fish population capacity to withstand environmental variability and increases the risk of fishery economic collapse (Marteinsdottir and Thorarinsson, 1998; Rouyer et al., 2012). By introducing additional mortality, many fisheries have truncated the age structure of marine fish populations and increased the relative abundance of younger age classes (Berkeley et al., 2004; Hsieh et al., 2010). Commonly, younger and smaller fish contribute less to overall recruitment than the older and larger ones (Palumbi, 2004; Hixon et al., 2014).

Evidence is accumulating that many marine fishes may undergo rapid changes in life-history traits, such as reproduction and growth. These changes have been attributed to fisheries-induced density-dependent factors, environmental drivers and/or evolutionary selective pressures (Audzijonyte et al., 2013; Morrongiello and Thresher, 2015). The relative importance of these drivers have been intensely debated (e.g., Olsen et al., 2004; Marshall and Browman, 2007; Kraak, 2007; Rogers et al., 2011; Therkildsen et al., 2013). However, regardless of the underlying mechanisms, the resulting trends have important implications for the assessment and management of individual species, as well as for ecosystem-based management (Audzijonyte et al., 2016). Understanding the relative importance of how genotypic (i.e., a set of genes an individual carries) and phenotypic (i.e., observable characteristics of an individual resulting from the interaction of its genotype with the environment) variability alters the population dynamics of intensely exploited marine fishes requires a long time series of data. Here we consider changes in expressed life history values of a sciaenid fish given its fishing history.

Marine sciaenid fishes are cosmopolitan (i.e., from tropical to temperate soft-bottom continental shelves) and widely important to fisheries worldwide. They are usually associated with large freshwater inputs, including the subtropical and warm temperate southwestern Atlantic Ocean (Longhurst and Pauly, 1987; Lowe-McConnell, 1987). Despite their importance and wide distribution, long-term studies on the population dynamics of sciaenid fishes are not frequent in the literature. For example, a comprehensive data set used by Keith and Hutchings (2012) to analyse fish population dynamics in low abundance included 204 stocks of 103 species, among which only one was a sciaenid (Micropogonias undulatus).

Along the extensive continental shelf of Southern Brazil (∼ width 100−200 km), sciaenids are dominant in the demersal fish communities and fisheries, among which M. furnieri (Desmarest, 1823) is the most common (Martins and Haimovici, 2016; Haimovici and Cardoso, 2017). This species is a euryhaline demersal sciaenid fish associated with soft bottoms in coastal and estuarine regions from the Yucatán Peninsula, in southeastern Mexico down to northern Patagonia (Chao, 1981). M. furnieri is an important component of the coastal fish community and the main target of the demersal coastal fisheries from Rio de Janeiro State in Brazil to Bahia Blanca in Argentina (23ᵒS - 40ᵒS) (Chiesa et al., 2006; Carozza, 2010; Haimovici et al., 2016). Annual landings in Argentina, Uruguay and Brazil have reached over 100,000 tons in recent years (FAO, 2018). In southern Brazil, the M. furnieri has been fished in the Patos Lagoon Estuary and in coastal waters since the 19th century by small-scale fishers with gillnets and beach seine nets (Odebrecht, 2003). Industrial fishing using otter and pair trawls began fishing on the continental shelf in the late 1940s in this region (Yesaki and Bager, 1975) and intensified from the mid-1970s when restrictions on economic exclusive zones excluded Brazilian fishing boats from fishing off Uruguay and Argentina continental shelves (Haimovici et al., 2014).

Although M. furnieri has a continuous distribution in the SW Atlantic, recent studies on the genetic population structure, spawning season, and growth suggest limited connectivity among the stocks fished in southern Brazil from those in southeastern Brazil to the north and in the Common Fishery Zone of Argentina and Uruguay to the south (Vasconcellos et al., 2015; Haimovici et al., 2016). In southern Brazil, the biology and population dynamics of M. furnieri have been studied since the 1970s (Vazzoler, 1991) because of its high abundance and economic importance, with industrial landings regularly monitored and sampled since 1976 in the town of Rio Grande (Haimovici, 1987). In this region, this species is considered to be overfished since the 1980s (Haimovici, 1998), with a fishing mortality (F) between 2–6 times higher than the calculated fishing mortality at maximum sustainable yield (FMSY) based on a surplus production model (Vasconcellos and Haimovici, 2006). However, despite low abundance compared to historical levels, this species still represents the main target of coastal demersal fishing in southern Brazil (Haimovici et al., 2016; Haimovici and Cardoso, 2017).

M. furnieri is a mid-sized (650 mm average maximum size) and long-lived (at least 38 years) fish (Schwingel and Castello, 1990; Haimovici and Unpierre, 1996). In the SW Atlantic, it is a seasonal spawner in coastal or estuarine waters (Weiss, 1981; Vazzoler, 1991; Macchi et al., 2003; Militelli et al., 2013). Pelagic eggs and larvae are carried into estuaries and coastal lagoons or retained in brackish waters where juveniles develop (Costa et al., 2013; Acha et al., 2018). Adults are opportunistic bottom-feeders that prey mainly on benthic infauna and epifauna such as polychaetas, mollusks, crustaceans and fish (Sánchez et al., 1991; Martins and Haimovici, 2020).

In this study, we aim to understand how four decades of heavy industrial fishing has affected life history values and population dynamics of M. furnieri and how this species has managed to stave off total collapse despite this intense removal pressure. In order to do so, we analyzed the long-term changes in growth, age and size at maturity, age and size structure, mortality and the reproductive potential of the stock of M. furnieri fished along southern Brazil between 1976 and 2017. Throughout this period, we observed that the truncation of age structure has decreased the reproductive potential for this stock. As a compensatory response to the reduction in density, growth increased and the age at first maturity of females decreased. In the last two decades, the age structure and growth have stabilized. We discuss the capacity of M. furnieri to withstand intense fishing into the future in the light of the realized changes in life history and subsequent population dynamics. The erosion of resilience due to the drastic decrease in the spawning potential highlights the potential risk of commercial collapse of the stock due to declining population size and recent technological improvements in fishing.

Section snippets

Material and methods

The primary dataset comes from a sampling program of the industrial fishing landings in Rio Grande from 1976 to 2019, and complemented by occasional bottom trawl surveys along southern Brazil (Haimovici, 1987; Haimovici et al., 1996). The periods used for each analysis were defined by data availability (Table 1).

In the multi-species coastal industrial bottom trawl and gillnet fisheries, fish are stored on board with ice in holds without previous size classification, therefore sampling for

Growth changes

The mean total length- and weight-at-age for both sexes of M. furnieri were calculated for the five periods with available data. Mean total length-at-age increased sharply between the first and the third period and stabilized during the following two periods (Fig. 2a). The changes become more evident when considering weight-at-age for ages greater than three (Fig. 2b):

The “multiple period” model (DIC = 36,982 for females and 27,117 for males) was better supported by the data than the “single

Discussion

Changes in the population structure and dynamics have been recorded for many fish stocks around the world as a response to heavy fishery exploitation (e.g., Bianchi et al., 2000; Sharpe and Hendry, 2009; Audzijonyte et al., 2013, 2016). The erosion of the size and age structure, the gradual increase in the total mortality and exploitation rates, and the low stock size in current years, as observed for M. furnieri in southern Brazil, are all indicators of population decline. These trends are

CRediT authorship contribution statement

Manuel Haimovici: Conceptualization, Methodology, Writing - original draft. Leticia Maria Cavole: Investigation, Formal analysis, Writing - original draft. Jason M. Cope: Formal analysis, Writing - original draft. Luís Gustavo Cardoso: Formal analysis, Writing - original draft, Software.

Declaration of Competing Interest

The authors report no declarations of interest.

Acknowledgements

The authors thank the Federal University of Rio Grande - FURG that provided continuous support, and the technicians and students who made possible the samplings and processing of the data along the years required in this long-term study. M.H. is Senior research fellow (307994/2020-1) and L. C. received a scholarship (132469/2012-0) from the Brazilian National Scientific and Technological Research Council. We also thank the anonymous reviewers and the editor for their useful recommendations.

References (73)

  • L.M. Cavole et al.

    The use of otolith microstructure in resolving issues of ageing and growth of young Micropogonias furnieri from southern Brazil

    Mar. Biol. Res.

    (2015)
  • N.L. Chao

    Family Sciaenidae Micropogonias furnieri (Unpaged)

  • E. Chiesa et al.

    Características biológicas de la corvina (Micropogonias furnieri) en el Río de la Plata y su Frente Marítimo

  • J. Cope

    The Stock Synthesis Data-limited Tool (SS-DL tool)

    (2020)
  • M.D.P. Costa et al.

    Estuarine early life stage habitat occupancy patterns of whitemouth croaker Micropogonias furnieri (Desmarest, 1830) from the Patos Lagoon, Brazil

    Fish. Res.

    (2013)
  • C.P. Cotrina et al.

    Estudio preliminar de la determinación de edad en la corvina (Micropogonias furnieri)

    Publ. Com. Téc. Mix. Fr. Mar.

    (1986)
  • J. Csirke

    Report of the working group on fisheries management, implications and interactions (part V)

  • CTMFM

    El recurso corvina (Micropogonias furnieri) en el área del Tratado del Río de la Plata y su Frente Marítimo. Diagnóstico poblacional. Documento conjunto DINARA-INIDEP-SSPyA

    (2017)
  • U. Dieckmann et al.

    Probabilistic maturation reaction norms: their history, strengths, and limitations

    Mar. Ecol. Prog. Ser.

    (2007)
  • K. Enberg et al.

    Fishing- induced evolution of growth: concepts, mechanisms and the empirical evidence

    Mar. Ecol.

    (2012)
  • FAO

    Fishery and Aquaculture Statistics. Global Capture Production 1950-2016 (FishstatJ)

    (2018)
  • A.A. Gonçalves et al.

    Descrição trófica dos primeiros estágios de vida de Micropogonias furnieri (Sciaenidae), no estuário da Lagoa dos Patos, RS, Brasil

    Atlantica

    (1999)
  • M. Haimovici

    Estratégia de amostragens de comprimentos de teleósteos demersais nos desembarques da pesca de arrasto no litoral sul do Brasil

    Atlntica

    (1987)
  • M. Haimovici

    Present state and perspectives for the Southern Brazil shelf demersal fisheries

    Fish. Manage. Ecol.

    (1998)
  • M. Haimovici et al.

    Long-term changes in the fisheries in the Patos Lagoon estuary and adjacent coastal waters in Southern Brazil

    Mar. Biol. Res.

    (2017)
  • M. Haimovici et al.

    Reproductive biology of the castanha Umbrina canosai (Pisces, Scianidae) in southern Brazil

    Ver. Bras. Biol.

    (1989)
  • M. Haimovici et al.

    Micropogonias furnieri (Desmarest, 1823), Micropogonias furnieri (Desmarest, 1823)

  • M. Haimovici et al.

    Variaciones estacionales en la estructura poblacional y cambios de crecimiento de la corvina Micropogonias furnieri (Desmarest, 1823) en el extremo sur de Brasil

    Atlântica

    (1996)
  • M. Haimovici et al.

    Distribuição e abundância de teleósteos demersais sobre a plataforma continental do sul do Brasil

    Rev. Bras. Biol.

    (1996)
  • M. Haimovici et al.

    Desenvolvimento da pesca industrial sediada em Rio Grande: uma visão histórica sob a ótica de atores privilegiados

  • M. Haimovici et al.

    Stocks and management units of Micropogonias furnieri (Desmarest, 1823) in southwestern Atlantic

    Lat. Am. J. Aquat. Res.

    (2016)
  • M.A. Hixon et al.

    BOFFFFs: on the importance of conserving old-growth age structure in fishery populations

    ICES J. Mar. Sci.

    (2014)
  • C.H. Hsieh et al.

    Fishing effects on age and spatial structures undermine population stability of fishes

    Aquat. Sci.

    (2010)
  • D.M. Keith et al.

    Population dynamics of marine fishes at low abundance

    Can. J. Fish. Aquat. Sci.

    (2012)
  • K. Kellner

    jagsUI: A Wrapper Around’ rjags’ to Streamline’ JAGS’ Analyses. R package version 1.5.1

    (2019)
  • P.G. Kinas et al.

    Introdução à Análise Bayesiana (com R)

    (2010)
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