Elsevier

Fisheries Research

Volume 238, June 2021, 105898
Fisheries Research

Temperature, maternal effects and density-dependent processes during early life stages of Argentine hake as relevant recruitment drivers

https://doi.org/10.1016/j.fishres.2021.105898Get rights and content

Highlights

  • Spawning of Argentine hake was mainly associated to bottom water temperatures between 9° and 13 °C.

  • Egg production of oldest females was positively correlated with recruitment observed one year later.

  • Egg density in the spawning area was negatively correlated with larval survival index.

  • Size of the optimal spawning area was positive correlated with recruitment.

Abstract

We analyzed the annual variability in total egg production and recruitment of the Patagonian stock of Argentine hake since 1990 and correlated these indices with some environmental variables as temperature and larval density estimated in the spawning area. We used data from research surveys carried out between 2001 and 2018 during the reproductive peak of this stock and information from the assessment model. The optimal spawning area of Argentine hake was associated with a bottom thermal front, with temperature values between 9° and 13 °C. The study revealed that reproductive success is positively influenced by the oldest females of the stock and negatively influenced by the egg density in the spawning area. In the first case, a larger proportion of older spawning females (≥ 7 years-old) produces larvae with greater survival rates; while in the second case, a greater abundance of early larvae in a more limited optimum spawning area could produce a higher rate of mortality due to competition.

Introduction

One of the main goals of fisheries research is to ensure that populations can maintain their reproductive potential at optimum levels, in order to allow sustainable exploitation over time (Marshall et al., 2003). The conservation of sufficient reproductive potential allows successful recruitments and maintains the structure of the stock in the future. For this reason, the relationship between parental stock and recruitment has become a central issue in the study of population dynamics and marine resource assessment (Hilborn and Walters, 1992). Recruitment in fish populations reflects the interaction of different external features, such as physical variables or trophodynamic processes in the environment, that affect demographic rates as growth and mortality during the early life history (Houde, 2009). Thus, it is important to determine in which way these factors contribute to generating variability in the process of incorporation of new individuals into the population.

Currently, the management of many marine stocks is performed based on adult stock-recruitment models, which assume that the population`s reproductive potential is proportional to its adult stock biomass (Trippel et al., 1997). The adult stock-recruitment models developed by Beverton and Holt (1957) and Ricker (1954) originally used the term fecundity (Koslow, 1992), but this term was later replaced by spawning stock biomass (SSB) as a proxy for fecundity. At present, SSB estimated by Virtual Population Analysis (VPA) is one of the reference points used to define harvest strategies for many exploited fish stocks (Lowerre-Barbieri et al., 2016). It is assumed that any adult population with the same biomass generates the same level of recruitment, which means that their offspring survival rates are independent of the population characteristics such as age/size structure or condition (Cardinale and Arrhenius, 2000; Marshall et al., 2003; Murua et al., 2003). Nonetheless, it has been long recognized that this assumption is invalid for several species (Marshall et al., 1998; Saborido-Rey and Junquera, 1999) because many studies demonstrated that relative fecundity, egg quality, and reproductive behavior may be affected by shifts in age/size composition of spawners (Marshall, 2009). At the end of the 1990s, a new concept was introduced as an alternative to SSB, called stock reproductive potential (SRP), defined as the “annual variation in a stock’s ability to produce viable eggs and larvae that may eventually recruit to the adult population or fishery” (Trippel, 1999). Unlike SSB, SRP includes information about parental features that influence the egg viability, which affects the recruitment processes. The association is established by the selective survival of eggs and larvae depending on parental characteristics such as age, size, and nutritional condition of spawners because it was demonstrated that maternal factors could play a key role in determining the mortality rate of the offspring (Marteinsdottir and Steinarsson, 1998; Lambert et al., 2003; Saborido-Rey et al., 2003). Based on this concept, Marshall et al. (1998) suggested the use of age fecundity models to estimate the total egg production (TEP) as a better index of recruitment potential compared with SSB. The individual attributes of females will determine the reproductive performance of the stock, especially the size structure and age diversity of the population (Marteinsdottir and Begg, 2002; Scott et al., 2005; Mehault et al., 2010), or the proportion of repeated spawners (Evans et al., 1996; Trippel, 1998), which also influences the ability of a stock to recover after overfishing (Rijnsdorp et al., 2010). Besides, the parental stock’s structure may determine the time and duration of the spawning season because larger females could have a longer spawning period than younger ones (Macchi et al., 2004; Pájaro et al., 2005). Therefore, variations of the size composition of the stock could have an important effect on recruitment (Wright and Trippel, 2009; Lowerre-Barbieri et al., 2011). These approaches, in general, do not include information on spawning location, which also may vary depending on the demographic structure of the stock (Begg and Marteinsdottir, 2002; Lowerre-Barbieri et al., 2011), affecting reproductive success and offspring survival (Lowerre-Barbieri et al., 2016).

The Patagonian stock of Argentine hake, Merluccius hubbsi, distributed from 41 °S to 55 °S at depths between 50 and 500 m, is the most important population of this species for Argentina, with a total catch of 272,535 tons reported for 2019 (https://www.magyp.gob.ar/sitio/areas/pesca_maritima/desembarques). During the 1990s, the intense fishing activity of different commercial fleets on Argentine hake produced a sharp drop in the abundance of this resource (Aubone, 2004), which led to the implementation of a permanent closure area in waters of Patagonia since 1997 (Irusta et al., 2016). The Patagonian stock of Argentine hake reproduces during the austral spring and summer, between November and April, with the main peak in January (Macchi et al., 2004; Pájaro et al., 2005). Spawning takes place mainly in waters off the Chubut province, between 43° and 45°30′S at depths from 50 to 100 m (Macchi et al., 2007), where large concentrations of eggs and larvae of this species are frequently observed (Ehrlich, 1998; Álvarez-Colombo et al., 2011). The analysis of different reproductive variables estimated for this stock, such as fecundity, spawning frequency, and egg quality, showed that females of greater size/age have a higher reproductive potential, generating more oocytes of better quality than younger individuals (Macchi et al., 2006, 2013). These results suggest the existence of maternal effect in Argentine hake from the Patagonian stock, enhanced by the fact that larger females have a longer reproductive period and a higher spawning frequency (Pájaro et al., 2005; Macchi et al., 2018), affecting the stock-recruitment relationship.

Argentine hake is assessed annually through VPA with an age-structured model using SSB as a biological reference point (Irusta et al., 2016). The stock-recruitment model obtained during the assessment of the Patagonian hake population shows high variability (Santos and Villarino, 2019), which has been a characteristic reported for most of the fishing stocks (Vert-pre et al., 2013). The use of TEP, instead of SSB, as an index of reproductive potential for this stock of Argentine hake, did not show a significant improvement in the relationship with recruitment (Marrari et al., 2019). Probably, environmental factors as the physical conditions in the spawning site, availability of food, inter or intraspecific competition and predation conditions in the nursery area may have a more significant effect on survival rates during the early life stages of this species (Diaz et al., 2014, 2020). Recently, the relationships between some environmental factors and reproductive success in the hake Patagonian stock were analyzed, observing a positive effect of chlorophyll a concentration during the beginning of the reproductive season and a negative effect of surface temperature at the end of spawning (Marrari et al., 2019). Therefore, it is important to consider the environmental characteristics at the spawning site and its annual variation in relation to recruitment. Lowerre-Barbieri et al. (2016) mentioned that adult abundance could be a poor predictor of recruitment and that it is necessary deepening the understanding of the traits resulting in effective reproduction, for example including information on spatiotemporal reproductive behavior.

We propose analyzing the annual variability in total egg production and recruitment of the Patagonian stock of Argentine hake from 1990 to 2017 and correlate these indices with some environmental variables as temperature and larval density estimated in the spawning site by research surveys. We hypothesize that the density-dependent mechanisms operating during spawning increase larval mortality in years of higher egg production, and that variability in the size of the optimal spawning area also contribute to affect the survival of the early life stages of Argentine hake.

Section snippets

Data from research surveys

One of the sources of data came from the research surveys carried out by the National Institute of Fisheries Research and Development (INIDEP) in the reproductive area of the Patagonian stock of Merluccius hubbsi between 2001 and 2018 (Fig. 1). These cruises were performed in January during the spawning peak of this population. In the research surveys, fishing trawls were distributed in transects perpendicularly oriented to the coastline, separated by approximately 20 nmi, in a depth range

Spawning and temperature

The frequency distribution of mature Merluccius hubbsi females (with hydrated oocytes) and in spawning (with new postovulatory follicles and hydrated oocytes) as a function of temperature was analyzed. It was observed that the range of bottom temperature values in which mature individuals were found varied between 7° and 15 °C, with higher frequencies between 8° and 10 °C (Fig. 2 A). However, when only the actively spawning females were considered, a change in the frequency of individuals with

Discussion

The spawning area of the Merluccius hubbsi Patagonian stock coincides spatially with the main nursery area for larvae of this species. In other words, the first life stages of Argentine hake stay in the same region where the greatest abundance of spawning females is concentrated during the austral summer. This area is advantageous for individuals in the early stages of development, given the existence of a highly productive frontal system in that region, the north-patagonian frontal system,

Conclusions

Maturation of Argentine hake in the Patagonian region may occur in a temperature range of 7° - 15 °C, but females in ovulation were mainly recorded when temperatures were between 9° and 13 °C. When considering the variables that determine the reproductive potential of this stock and its relation to reproductive success, measured as survival during the first year of life and recruitment, it was observed a positive effect generated by the oldest females of the stock and a negative influence

Funding

This work was supported by the Instituto Nacional de Investigación y Desarrollo Pesquero (INIDEP), Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET) and Fondo para la investigación Científica y Tecnológica [FONCyT; grant numbers: PICT-2013-1484 and PICT-2018-03872).

CRediT authorship contribution statement

Gustavo J. Macchi: Conceptualization, Methodology, Formal analysis, Project administration, Supervision, Investigation, Writing - original draft, Writing - review & editing. Marina V. Diaz: Visualization, Writing - original draft, Writing - review & editing. Ezequiel Leonarduzzi: Methodology, Software, Data curation, Formal analysis. Martín Ehrlich: Data curation, Methodology, Investigation. Laura Machinandiarena: Data curation, Methodology, Investigation. Mariana Cadaveira: Data curation.

Declaration of Competing Interest

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

Acknowledgements

We wish to thank M. Estrada and H. Brachetta for their work in the preparation of the histological sections of Argentine hake ovaries. Thanks to the technical staff of the Hake Assessment Group of the INIDEP for age determination of the specimens. We would also like to thank the staff of the Oceanography Lab of the INIDEP for the temperature data obtained during the research surveys. This article is referenced by INIDEP as contribution Nº 2234.

References (80)

  • S. Mehault et al.

    Variability in total egg production and implications for management of the southern stock of European hake

    Fish. Res.

    (2010)
  • A. Nissling et al.

    Assessment of egg and larval viability in cod, Gadus morhua: methods and results from an experimental study

    Fish. Res.

    (1998)
  • M. Pájaro et al.

    Reproductive pattern of the Patagonian stock of Argentine hake (Merluccius hubbsi)

    Fish. Res.

    (2005)
  • J.P. Pisoni et al.

    On the variability of tidal fronts on a macrotidal continental shelf, Northern Patagonia, Argentina

    Deep-Sea Res II

    (2015)
  • A.D. Rijnsdorp et al.

    The ecological significance of geographical and seasonal differences in egg size in sole Solea solea (L.)

    Neth. J. Sea. Res.

    (1994)
  • K. Rodrigues et al.

    Comparative study of spawning pattern and reproductive potential of the Northern and Southern stocks of Argentine hake (Merluccius hubbsi)

    J. Sea Res.

    (2015)
  • F. Saborido-Rey et al.

    Fish reproduction and fisheries

    Fish. Res.

    (2013)
  • E.M. Acha et al.

    Ecological Processes at Marine Fronts. Oases in the Ocean

    (2015)
  • G. Álvarez-Colombo et al.

    Distribution and behavior of Argentine hake larvae: Evidence of a biophysical mechanism for self-recruitment in northern Patagonian shelf waters

    Cienc. Mar.

    (2011)
  • G.A. Begg et al.

    Environmental and stock effects on spawning origins and recruitment of cod Gadus morhua

    Mar. Ecol. Prog. Ser.

    (2002)
  • R.J.H. Beverton et al.

    On the dynamics of exploited fish populations

    Fisheries Investigations

    (1957)
  • N.J. Brown-Peterson et al.

    A standardized terminology for describing reproductive development in fishes

    Mar. Coast. Fish. Dyn. Manag. Ecosyst. Sci.

    (2011)
  • M. Cardinale et al.

    The influence of stock structure and environmental conditions on the recruitment process of Baltic cod estimated using a generalized additive model

    Can. J. Fish. Aquat. Sci.

    (2000)
  • J.I. Carreto et al.

    Toxic red tide in the Argentine Sea: phytoplankton distribution and survival of the toxic dinoflagellate Gonyaulax excavata in a frontal area

    J. Plank. Res.

    (1986)
  • J.H. Cowan et al.

    Is density‐dependent growth in young‐of‐the‐year fishes a question of critical weight? Rev

    Fish. Biol. Fish.

    (2000)
  • W.K. De La Mare

    Estimating confidence Intervals for Fish stock abundance estimates from trawl surveys

    CCAMLR Sci.

    (1994)
  • M.V. Diaz et al.

    Evaluating the role of endogenous and environmental features on larval hake nutritional condition

    Fish. Oceanogr.

    (2020)
  • M.D. Ehrlich

    Los Primeros Estadios de Vida de la Merluza Merluccius hubbsi Marini 1933, Como Aporte al Conocimiento de su Reclutamiento y Estructura Poblacional. PhD Dissertation

    (1998)
  • R. Hilborn et al.

    Quantitative Fisheries Stock Assessment: Choice, Dynamics and Uncertainty

    (1992)
  • S. Hinckley

    Variation of egg size of walleye pollock Theragra chalcogramma with a preliminary examination of the effect of egg size on larval size

    Fish. Bull. (Wash. D. C.)

    (1990)
  • E.D. Houde

    Comparative growth, mortality, and energetics of marine fish larvae: temperature and implied latitudinal effects

    Fish. Bull. (Wash. D. C.)

    (1989)
  • E.D. Houde

    Recruitment variability

  • J.R. Hunter et al.

    Spawning incidence and batch fecundity in northern anchovy, Engraulis mordax

    Fish. Bull. (Wash. D. C.)

    (1980)
  • J.R. Hunter et al.

    Batch fecundity in multiple spawning fishes

  • G. Irusta et al.

    Biology and fishery of the Argentine hake (Merluccius hubbsi)

    Rev. Invest. Desarr. Pesq.

    (2016)
  • M.G. Kendall et al.

    The Advanced Theory of Statistics

    (1967)
  • O.S. Kjesbu et al.

    Variation in annual egg production in individual captive Atlantic cod (Gadus morhua)

    Can. J. Fish. Aquat. Sci.

    (1996)
  • J.A. Koslow

    Fecundity and the stock-recruitment relationship

    Can. J. Fish. Aquat. Sci.

    (1992)
  • Y. Lambert et al.

    Using environmental and biological indices as proxies for egg and larval production of marine fishes

    J. Northw. Atl. Fish. Sci.

    (2003)
  • E. Leonarduzzi

    Bioenergética y Condición Nutricional de la Merluza Común, Merluccius hubbsi, del Efectivo Patagónico y sus Implicancias en el Potencial Reproductivo de la Especie. PhD Dissertation

    (2018)
  • View full text