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Latin american journal of aquatic research

On-line version ISSN 0718-560X

Lat. Am. J. Aquat. Res. vol.48 no.1 Valparaíso Mar. 2020

http://dx.doi.org/10.3856/vol48-issue1-fulltext-2271 

Research Article

Reproductive traits and natural mortality of the cardinalfish Epigonus crassicaudus: crucial information for stock assessment and sustainable management measures

Guillermo Moyano1  2 

Francisco Cerna1 

Elson Leal1 

Guido Plaza2 

Vilma Ojeda1 

1División de Investigación Pesquera, Instituto de Fomento Pesquero (IFOP), Valparaíso, Chile

2Escuela de Ciencias del Mar, Pontificia Universidad Católica de Valparaíso, Valparaíso, Chile

ABSTRACT

Reproductive traits and natural mortality rate of cardinalfish females (Epigonus crassicaudus) were studied from samples collected onboard commercial fishing vessels, from 2012 to 2015, on the Chilean coast. The reproductive cycles of females analyzed thought gonadosomatic index (GSI) showed a maximum reproductive activity in austral fall, between March and May. Length (L50%) and age (A50%) at maturity, estimated using a macroscopic scale of the developed ovary, was 22.3 cm fork length (FL) and 9.3 years, respectively. Natural mortality (M) was estimated by two age-related methods. Using maximum age (tmax) M was estimated in 0.063 yr-1 and through age-at-maturity (A50%) in 0.15 yr-1. A potential bias in the reproductive study is discussed when a macroscopic maturity scale is used. Nevertheless, its usefulness is validated when funding is scarce, and time is limited. Although M uncertainty was not evaluated, the estimated range appears to be into the expected values to long-lived species. The life history parameters estimated in the present study can be used to evaluate possible time variability in maturity and M rates. Also, these results could be used in stock assessment analysis and to apply effective management measures in the fishery.

Keywords: Epigonus crassicaudus; maturity; reproduction; natural mortality; fishery

INTRODUCTION

Information on reproduction and natural mortality (M) is very important to properly manage the exploitation of fisheries resources (Charnov & Berrigan, 1991; Rose et al., 2002; Winker et al., 2011). Revealing the reproductive cycle and length or age-at-maturity provides insight that can help to enable necessary management measures (Jakobsen et al., 2009). Also, M is one of the most influential parameters in fisheries stock assessment and management (Wang & Ellis, 2004; Brodziak et al., 2011).

The cardinalfish (Epigonus crassicaudus) (De Buen, 1959) belongs to the Epigonidae family, a poorly studied group of perciform fishes, with permanent records of new species (Okamoto & Motomura, 2011; Okamoto et al., 2011). This species is endemic along the Chilean coast, distributed mainly between 29°00's and 42°50's, in depths between 100 and 500 m (Wiff et al., 2005; Leal et al., 2009). Cardinalfish landings have been recorded since 1992 with 579 t at that year, its peak in landings was 5,792 t recorded in 2000 (SERNAPESCA, 2000). Today, due to over-exploitation, the fishery is closed, and the government only authorized bycatch of 2 and 12 t for the artisanal and industrial fleets, respectively (SUBPESCA, 2016).

Regarding its biology, some studies addressing the food and trophic levels of this species have been reported (e.g., Arancibia & Meléndez, 1987; Neira & Arancibia, 2004; Leal et al., 2009; Sepúlveda et al., 2018). Also, the annual reproductive cycle and maturity in length to females was reported by Flores et al. (2015). However, to date, there not published information on natural mortality (M) for E. crassicaudus; nevertheless, technical reports (Cubillos et al., 2009; Tascheri & Flores, 2013) have suggested low values to this parameter due to low growth rates and a potential long-life span. Moreover, Moyano et al. (2018) pointed E. crassicaudus as a slow-growing species and with a life span of about 67 years. This species is especially vulnerable to overfishing during recruitment, due to removing the larger individuals can favor slower growing and earlier of maturing fishes (Ziegler et al., 2007; Cailliet & Andrews, 2010).

The recovery of catches of cardinalfish depends on management measures, based on reliable biological background. Hence, information on life-history parameters is crucial for this purpose. Thus, considering, both reproduction and M rates are critical parameters for stock assessment and management because they are important predictors of the risk of overexploitation (Clark, 1991; Reynolds et al., 2005), the current study examined annual reproductive cycle, length and age at maturity and M rates E. crassicaudus for 2012 to 2015 period.

MATERIALS AND METHODS

Reproduction

A total of 4,214 fishes were collected monthly between January 2012 and December 2015, covering an area located between 34°50′s and 39°00′s off the Chilean coast (Fig. 1). Samples were collected randomly during bottom trawls on board of commercial fishing vessels, registering sex, fork length (FL, cm), total weight (TW, g), ovary weight (OW, g) and gutted weight (GW, g). Sagittae otoliths were extracted, dried and stored in paper envelopes and carefully labeled to ensure traceability. Then, in the laboratory, age in years of each specimen was assigned on otoliths transversal sections according to the criteria described by Ojeda et al. (2010) and Moyano et al. (2018). Ovary of each female was classified into six stages, according to macroscopic maturity scale (Balbontín & Bravo, 1993), virginal (1), immature (2), maturation (3), mature (4), mature with recent spawning (5) and regressing (6). The annual reproductive cycle for female cardinalfish was characterized by assessing the monthly gonadosomatic index (GSI) variation (Nikolsky, 1963), using a total of 2,812 ovaries according to:

IGS=(OW/GW)×100

where OW is the ovary weight (g) and GW is gutted weight (g).

Figure 1 Spatial distribution of cardinalfish Epigonus crassicaudus hauls throughout the fishery area for the period 2012-2015. 

Length and age-at-maturity for females were determined using selected data, collected in the main reproductive season of each year, considering a total of 796 samples. Females that had reached at least stage 3 in the macroscopic maturity scale were classified as mature. The proportion of mature fish at length and age was fitted using a logistic function (Schnute & Richards, 1990):

Pm=1/(1+e(α+β×X))

where Pm is the proportion of mature adult fish of length or age (X), and α and β are parameters estimated by least squares with a binomial error distribution. The length or age at which 50% of individuals are estimated to be adult mature (L50% and A50%) was calculated based on the work by Roa et al. (1999):

L50,A50=α/β

Natural mortality

Two approaches as a function of maximum age (tmax) and maturity age (A50%) were used to estimate the natural mortality rate (M).

  1. The model of Rikher & Efanov (1976), as follows:

    M=[1.521tm50%0.72]0.155

    where t 0.72m50% is 50% of mature females estimated in the present study A50%.

  2. The model of Hewitt & Hoenig (2005) as:

    M=4.22tmax

where tmax corresponds at the maximum estimated age in this species (Moyano et al., 2018).

RESULTS

Reproduction

The annual reproductive cycle evaluated through monthly IGS variation to females analyzed between 2012 and 2015, showed a possible reproductive rest in austral spring and summer from August to December with a low index value. A maximum IGS in fall (March, April and May) would be indicating a more intense reproductive activity for the population (Fig. 2). For this period, females analyzed to maturity study in length and age ranged from 15 to 38 cm FL, corresponding to specimens between 4 and 67 years.

Figure 2 Boxplot of monthly variation of gonadosomatic index (IGS) of Epigonus crassicaudus (females). The black line represents the mean value, and the gray rectangle identifies months of maximum sexual activity for the period 2012-2015. The number of samples analyzed is indicated in the monthly bars. 

In terms of length, the logistic model showed a fast maturity process between 18 and 25 cm FL. The mean L50% was estimated in 22.3 cm FL (Fig. 3) from parameters α = 15.71 (SE = 3.42; P > 0.05) and β = −0.71(SE = 0.15; P > 0.05) respectively. Probably due bias in assignment of maturity stages observed data not showed a clear length to full population maturity (L100%). Nevertheless, fitted models suggest 28 cm LF.

Figure 3 Maturity ogives for the female of Epigonus crassicaudus between 2012 and 2015 in the Chilean coast, in the moths of maximum reproductive activity. a) Length maturity, b) age maturity. 

The maturity age with parameters α = 4.68 (SE = 1.42; P > 0.05) and β = −0.50 (SE = 0.14; P > 0.05), indicate A50% for female Epigonus crassicaudus to be 9.3 years. Females analyzed showed an active maturity process in individuals over six years; samples from this age showed the first maturity signals. Observed data and fitted models showed a high probability of a full maturity population from 14 years.

Natural mortality

Considering the parameters tmax = 67 years, which corresponded to the maximum estimated age, the natural mortality rate was 0.063 yr-1 and with the method based on age-at-maturity (A50% = 9.3 years) resulted in 0.15 yr-1.

DISCUSSION

The reproductive cycle showed a period of reproductive maximization from March to May and in resting between august and December. These results are partially coincident with the unique study published before in the reproductive biology of Epigonus crassicaudus. Flores et al. (2015) showed the occurrence of permanent vitellogenesis through the year, although identified through GSI, a reproductive peak between May and June. Hence, the results of the current study confirm the spawning season for this species to be concentrated in austral fall off the Chilean coast. In other species of genus Epigonus, distributed in the southern hemisphere, such as E. telescopus, spawning occurs during fall and winter in the New Zealand coast (Field et al., 1997).

In studies related to the maturity process in size or age, it is common to find 100% of mature individuals after a certain length or age. To E. crassicaudus, Flores et al. (2015), based on histological analysis of ovaries, determined 100% of mature females occurred about 28 cm FL. In the present study, after 28 cm FL, some portion of females continued being assigned to the immature fraction of the population, which is frequent in macroscopic scales of maturity because mature adult females in resting, could be mistakenly classified as immature due to its poor ovarian development (Hunter & Macewicz, 2003; Murua & Saborido-Rey, 2003; Tomkiewicz et al., 2003; Brown-Peterson et al., 2011). Despite this apparent bias in the allocation of maturity states, L50% reached 22.3 cm FL close to the value estimated by Flores et al. (2015), who reported an L50% of 23.2 cm FL for samples coming from a similar study area. Compared with L50% in technical reports, our results were close to 24.3 cm FL estimated by Gálvez et al. (2013) and smaller than 32.1 cm FL, estimated by Cubillos et al. (2009), who considers smaller samples and a more restricted study area.

According to Beverton & Holt invariants hypothesis (Jensen, 1996), the L50% around 22 or 23 cm FL agrees with the expected theoretical value for the ratio L50%/L = 0.67. If L = 34 cm FL, indicated by Moyano et al. (2018), is considered, the value for this relationship in E. crassicaudus would be ~0.65-0.67.

The results for L50% confirmed those reported by Flores et al. (2015), who used the histologic methodology to estimate this value, could validate the macroscopic approach in fish maturity studies when funding is scarce, or a quick estimation is needed.

The estimation of maturity in age is more uncertain in long-lived species (Wilson & Boehlert, 1990). A correct reading criterion for age allocation is key to an adequate characterization of the maturity process. Unfortunately, no published information was found in order to contrast our results regarding the early age at maturation (A50% = 9.3 years) about the longevity of E. crassicaudus (67 years). However, Gálvez et al. (2013), in a technical report, indicated a similar age of maturity (10 years) for this species. Jarić & Gačić (2012) reported that in long-lived species, there is no linear relationship between A50% and tmax, and consequently, females can mature earlier or later. For example, Tracey et al. (2000) estimated an A50% reached at 35 years for Epigonus telescopus to tmax = 104 years. Conversely, Hanselman et al. (2010) reported an A50% of 6.1 years to tmax = 114 years for Anoplopoma fimbria.

Beyond the criteria used in age assignment, it is known that changes in the life-history traits of fishes are induced by high fishing pressure (Jørgensen & Fiksen, 2010; Jørgensen & Holt, 2013). The fishery of E. crassicaudus from 2012 to 2015 removed a high percentage of fish (~60%) undersize and age of maturity (Céspedes et al., 2015). This condition could be critical for a deep-water species because of its lower resilience to fishing pressure, with a lower capacity to recover from heavy exploitation than other continental fishes. The model of Jørgensen & Fiksen (2010) predicted an increase in M rate as an adaptive response to harvesting pressure. Jørgensen & Holt (2013) suggest that an increase in M could be part of the explanation for not recovering collapsed stocks.

M can show high variability associated with life-history parameters used as input values in indirect methods (Quiroz et al., 2006; Dunn, 2009). In this case, uncertainty was not evaluated, and only two methods associated with age were used. Those methods were implemented because they are usually used to evaluate M in long-lived species (Jarić & Gačić, 2012). The range to M in this study (0.06-0.15 yr-1) to females of E. crassicaudus includes the value (0.08 yr-1) reported by Tascheri & Flores (2013). Although indirect estimates of M may contain a high level of uncertainty (Hoenig et al., 2016; Canales et al., 2019), it seems that M in this research is consistent with the life history characteristics of deep-water fishes with long-live cycle. Tracey et al. (2000), for another member of gender (E. telescopus), reported less value (0.034 yr-1), consistent with its expectation life (tmax = 104 years) of the New Zealand coast.

Finally, the life history parameters estimated in the present study could provide an important baseline for future studies, evaluating possible changes on maturity and M. They may also be used in stock assessment analysis and to apply effective fishery management measures.

ACKNOWLEDGMENTS

The authors would like to thank the Fisheries Scientific Observers who collect data overseas, and the Survey Management Department of Instituto de Fomento Pesquero (IFOP), Chile for providing the necessary information for this study. We also thank Mariella Canales for her valuable comments on this research and Francisco Plaza for his help in the manuscript review.

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Received: January 10, 2019; Accepted: September 02, 2019

Corresponding author: Guillermo Moyano (guillermo.moyano@ifop.cl)

Corresponding editor: Alejandra Volpedo

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