Life History Parameters of Genypterus brasiliensis (Teleostei: Ophidiidae), an Endemic Fisheries Resource of the Southwestern Atlantic

Abstract

Abstract:Genypterus brasiliensis, a demersal fish of large size (1.3 m of total length), occurs in the southwest Atlantic (23 to 38^oS) and well appreciated due to the quality of its flesh. It was analyzed through longline and trawl fisheries, and the average length and weight of 724 specimens were significantly different between them, with the biggest and heaviest specimens caught by the former. The weight-length relationships were significantly different based upon sex: females Wt=4x10-⁷Lt³.³⁷⁹⁹; r²=0.97; n=262; p<0.001, and males: Wt=4x10-⁷Lt³.³⁸⁸⁶; r²=0.95; n=190; p<0.001. Using the otoliths readings for 153 specimens (APE of 2% and CV of 4.2%), the growth parameters estimates reveal statistical differences between sexes (p=0.05; r²=0.889). The fisheries were composed of individuals aged 1 to 13 (females) and 1 to 14 years old (males), with ring formation in late spring. The back calculated parameters (VBGF) were: L_oo=1,452.38 mm, K=0.0996, t₀=-0.2757 yr^-1 (females) and L_oo=983.07 mm, K=0.155, t0=-0.236 yr^-1 (males), and longevity as 29.8 and 19.1 years old, respectively. The low biological production allied to the slow growth and a late complete maturation and its endemism, allow classify G. brasiliensis as a vulnerable resource, jeopardizing a sustainable fishery. Until reliable quantitative biological data are available, precautionary management must be considered.

Key words
population dynamics; endemism; fishes; fisheries

INTRODUCTION

Although considered “an unpatterned form” and a junior synonym for Genypterus blacodes (Bloch and Schneider 1801) (Nielsen et al. 1999), Genypterus brasiliensis (Regan, 1903) is recognized as a separate taxon (Nakamura 1986) and is accepted herein as an endemic groundfish species from the southwestern Atlantic (23^o to 38^oS) (Figueiredo and Menezes 1978, Menezes et al. 2003). It is one of the most valuable species of bottom trawl and longline fisheries in southern Brazil, operating at depths between 50 and 510 m (Tutui et al. 2000, Graça-Lopes et al. 2002, Perez et al. 2002, Frota et al. 2004, Haimovici et al. 2004). The Brazilian fisheries statistics official series from 1995 to 2012 reported an average of 585.5 t (+/- 58.4 SEM) annual average catch of the species, with an increasing trend of the landings since 2004. This flesh, of an excellent quality, is of a great interest for the gastronomy, and it is sold in local markets as fillets, steaks or whole fish. Unfortunately, fishing effort data is not available, in general and in the present case, for Brazilian fisheries. Most of those catches were completed by trawling in the outer shelf and upper slope between 23^o to 25^oS, an area dominated by an intrusion of cold water mass (Piola et al. 2000, Belem et al. 2013). Meanwhile, early publications revealed catches in small numbers southwards, at the Subtropical Convergence System (Haimovici et al. 1994). In addition, the species lacks information concerning its life cycle and fisheries biology. This study aimed to describe the life history parameters of the species. Therefore, the growth size and weight for instantaneous rates of mortality were first investigated to determine the level of exploitation.

MATERIALS AND METHODS

Sampling was conducted by a survey of longline fisheries of the RV Orion in 1994 and 1995 (Tutui et al 2000), the RV Margus II during Revizee (a Brazilian research program of for Living Resources from Economic Exclusive Zone) in 1997 (Haimovici et al. 2004), and the RV Soloncy Moura otter trawl cruises during the winter and spring of 2001. All the surveys occurred in the outer shelf and upper slope (100 to 500 m depth) between 22°00’S to 34°40’S. Additional data were obtained from commercial fisheries from the double-rig trawl and pair trawl fleets in 2003-2004 and 2006-2007 at diverse fishery wharves in southeastern Brazil.

Total length (L, 1 mm) and weight (W, 0.01 g) were measured for each fish. The weight-length relationship was modeled using a power function (W=a*L^b) and tested for sex by an ANCOVA. Otoliths were removed, cleaned and stored dry. The intact right otoliths were measured with a caliper to the nearest 0.05 mm in length, and weighed to the nearest 0.001 g. Three to five pairs of otoliths from each size class were randomly chosen for cutting in the transverse plane into sections 0.3 mm in width with a Buhler Isomet™ low-speed saw. Two to three sections were cut at each otolith and mounted on glass microscope slides preserved with Canadian balsam. Digital images of the sections with reflected light and 16x magnification were obtained. For age estimation, 263 otoliths of both sexes and of all L sampled classes (1 cm) were used. The ages were estimated based on transitional counts of hyaline and opaque annuli (Turner 1986, Beckman and Wilson 1995), assuming one completed annuli as the presence of both one opaque and one hyaline rings. Two readings had to be equal to be accepted as legible. A coefficient of variation (CV%) and the Average Percent Error (APE) index (Beamish and Fournier 1981) were calculated. Otolith radius and the distance between otolith nucleus to the annuli (opaque ring, Rn) were determined using the software Image Tool (UTHSCSA 2008). ANCOVA was applied to test statistical differences between sexes in addition to Lt and total radius (Rt). The border readings (opaque or hyaline) were seasonally grouped (Spring: September to November, Summer: December to February, Autumn: March to May, Winter: June to August). To support the hypothesis of annual formation of growth increments (annuli), the data (separated by sex) were pooled for each season and by marginal increment analysis (MAI) expressed as: MI%=(Rt–Ru)/Rt, where Rt is the otolith radius and R_u the last annulus radius. All data were analyzed by the Kruskal-Wallis test (Zar 1999), as data was not normally distributed. If growth increments were deposited annually, a single peak could be expected in the seasonal frequency of each margin type (opaque/hyaline) over a year. Annual increments (annuli) were also validated by the spacing pattern between rings for each sex, the relationship among each radius and rings, and by the frequency distribution of the annulus radius; all were tested as proposed by Lai et al. (1996).

The back calculation was applied to verify the period of annuli formation by the body proportional hypothesis (BPH) function, Li=(a+bRi)/(a+bRt), where Li is the fish length obtained from back calculation for each i^th ring, a and b are constants of the linear regression between Rt and Lt, Lt is the observed length, Ri the radius of each i ring, and Rt the total radius. The back calculated lengths in each age class were estimated using a non-linear least-squares regression to estimate the von Bertalanffy growth function (VBGF). The growth parameters L∞ (asymptotic length), K (intrinsic growth ratio) and t₀ (theoretical age at length equal to 0) were estimated by the fitted function VBGF, and the growth performance index (Φ’=logK+2logL∞) (Pauly and Munro 1984) was obtained for comparison with other species from the genus Genypterus.

The longevity of the stock was estimated as t_max=t₀+2.996/K. The instantaneous natural mortality rate (M) was estimated by the empirical expression of Pauly (1980), considering 16 °C as the mean annual bottom water temperature at the fisheries’ grounds. With those value, the von Bertalanffy growth ratio M/K was also estimated.

All statistical analyses were completed with the SYSTAT package (Wilkinson 2000).

RESULTS

A total of 724 specimens in the length range of 235-1,100 mm were measured during the sampling. The average length and weight were significantly different by fisheries (ANCOVA: p<0.001), higher for the longline (Table I). From this total, 452 (62.4%) specimens were sexed, and the sex ratio was favorable for females (1:0.725).

TABLE I
Average length standard errors (L_med± se) in mm, range and sampled number of the pink cusk eel Genypterus brasiliensis for distinct sample sources.

Data Source	Longline fisheries		Otter trawl fisheries
	RV Orion	FV Margus II		RV Soloncy Moura	Commercial fisheries
Lmed± se	720.6 ± 13.3	737.5 ± 20.8		550.1 ± 15.1	503.6 ± 5.9
Range	380–1,100	498-1,100		235-876	279–988
n	170	49		80	425

The weight-length relationship was significantly different between sexes, with females described by W=4x10-⁷L³.³⁷⁹⁹ (r²=0.97; n=262; s_a =3.37; s_b=0.033; p<0.001) and males by W=4x10-⁷L³.³⁸⁸⁶ (r²=0.95; n=190; s_a=0.28; s_b=0.004; p<0.001). For general purposes, a general weight-length relationship was also estimated (W=5x10-⁷L³.³⁷¹²; r²=0.9719; n=557).

The ANOVA indicated no significant difference between the left and right otoliths with respect to mean fish length (n=365; p=0.251). The number of annual increments were recorded along the dorsal axis (Fig. 1), where the increments showed mode differences compared with other regions of the otolith.

Figure 1
Transversal section (0.3 mm width) of otolith from a pink cusk-eel Genypterus brasiliensis (female, 946 mm, 8 annuli, caught in October 2002 south of Rio de Janeiro, Brazil, around 300 m depth) observed through reflected light and 16 x.

From a total of 263 otoliths that were sectioned, 153 (102 females and 51 males) were considered legible and/or had similar ring readings. The reading comparison was consistence for both sexes with high precision (CV of 4.2% and APE of 2.0%), except for rings 1, 8 and 10 (few specimens sampled).

The relationship between Lt and Rt was significantly different between sexes (F=5,573.733; df:610; p=0.105) and were expressed as Lt♂=13.792+154.280Rt (r²=0.827; F=1,147.016; df: 202; p<0.001) and Lt♀=17.617+158.330Rt (r²=0.913; F=4,784.067; df=407; p<0.001). Assuming those results, 72.5% of the females and 58.8% of the males among all otolith sections analyzed corresponded to the 2 to 4 age class interval. The seasonal percentage opaque/hyaline border analysis reported peaks of deposition (austral Autumn and Winter) with no conflicts to marginal increment analysis (MAI, higher median of MI% for hyaline border in Winter to Spring), which suggest an annual deposition period during late Summer, Autumn and Winter (Fig. 2).

Figure 2
Marginal increment analysis (MI%, median and range) for females and males of the pink cusk-eel Genypterus brasiliensis.

The annuli readings showed 13 age classes for females and 14 for males. No difference of statistical significance was observed for the entire age period (1 to 13 years, Kruskal-Wallis: p=0.430) or for the most representative age period in the catches (5 to 8 years, Kruskal Wallis: p=0.217). However, this may indicate an approximate period for annuli formation and may assume that the number of annual increments increased consistently across the age range of fish.

The plots of average back calculated length (BPH, Fig. 3) corresponding to each age class and observed L models allowed the fitting of the von Bertalanffy growth curve for males L=983.07(1-e^{-0.155(t+0.236)}) and females: L=1.452.38(1-e^{-0.0996(t+0.2757)}), with ranges and confidence intervals, and age-at-length keys for each sex shown in Tables II and III, respectively. Because the largest fish measured was a female (1,100 mm), the highest estimated age was almost 14 years, which is essentially the same age for a male of 890 mm. The performances indexes (Φ’) presented values of 3.320 for females and of 3.175 for males, lower than other species of the same genus (Japp 1990, Horn 1993, Withell and Wankowski 1989, Wiff et al. 2007, Chong and Aguayo 1990).

Figure 3
Average back calculated (BPH) and observed lengths (Lt) by age class of the pink cusk-eel Genypterus brasiliensis.

TABLE II
Back calculation growth (BPH) parameters fitted to von Bertalanffy function for the pink cusk-eel Genypterus brasiliensis (CI: 95% confidence interval, ASE: asymptotic standard error).

Parameter	L∞ (mm)	CI (ASE)	K (year-1)	CI (ASE)	t 0 (year-1)	CI (ASE)
Female(n=102; r2=0.973)	1,452	1,192 :1,712 (132.40)	0.100	0.072 : 0.127 (0.014)	-0.276	-0.472 : -0.080 (0.100)
Male(n=48; r2=0.961)	983	765.3 : 1,200 (110.3)	0.155	0.092 : 0.219 (0.032)	-0.236	-0.585 : 0.113 (0.177)

TABLE III
Age-length keys for females and males of the pink cusk-eel Genypterus brasiliensis.

Females
Rings	Midpoint Lt Class (mm)	Age (years)
		1	2	3	4	5	6	7	8	9	10	11	12	13
1+	275	2	1
2+	325		12
	375		25
3+	425		3	31
	475			28
4+	525			5	47
	575				34	3
5+	625					27
	675					7	8
6+	725						9
	775						1	3
7+	825							4	2
	875								3	1
8+	925									1	2
	975										2	1
9+	1,025
	1,075
	1,125													1
N	263	2	41	64	81	37	18	7	5	2	4	1		1
mean Lt		279.5	363.5	456.4	545.1	627.5	707.9	792.7	854.2	908.0	951.5	988.0	-	1,110
sd		17.7	32.1	31.3	24.1	22.0	23.4	21.4	23.9	22.6	7.7	-	-	-
se		17.7	5.1	3.9	2.7	3.7	5.7	8.7	11.9	22.6	4.5
Males
Rings	Midpoint Lt Class (mm)	Age (years)
		1	2	3	4	5	6	7	8	9	10	11	12	13	14
1+	225
	275	6	3
2+	325		10
	375		13	4
3+	425			29
	475			18	10
4+	525				34	3
	575					19
5+	625					3	13
	675						5	9
6+	725								7
	775									3
7+	825										1
	875														2
8+	925
	975
9+	1,025
	1,075
N	192	6	26	51	44	25	18	9	7	3	1				2
mean Lt		274.3	345.0	435.8	513.5	568.3	633.5	676.6	723.7	762.3	807.0	-	-	-	885.0
sd		13.1	32.8	25.1	18.1	18.7	17.5	9.2	8.1	3.5	-	-	-	-	7.1
se		5.8	6.6	3.5	2.8	3.8	4.2	3.3	3.3	2.5	-	-	-	-	7.1

• sd= standard deviation; se: standard error.

The ratio M/K (1.05 and 1.01, for females and males, respectively) invoke optimum catch sizes (L_opt) of 800.2 mm (males) and 955.0 mm (females), which corresponded to ages 7 to 9.5, respectively (see Table III). The optimum catch length-asymptotic length ratio (L_opt/L∞) was 0.658 for females and 0.814 for males, inside the interval (0.323 to 0.938, and slightly higher than the average of 0.620) assumed by Cubillos (2003) for all fish species.

DISCUSSION

The average size among specimens of Genypterus brasiliensis caught in the otter trawl (500-550 mm) and longline fisheries (720-737 mm), all from the same region, revealed a gear selectivity effect. The first interval included the mean length at first maturity of the population (L₅₀ of 527.3 mm, authors’ unpublished data), and the latter was smaller than the length of entire populations that were mature (L₁₀₀ approximately 950 mm) and close to the optimum catch size found for females (~955 mm).

Juveniles (less than 500 mm) were observed in the coastal pair trawl (in areas shallower than 40 m deep), and also in the offshore longline (deeper than 100 m) fisheries of southern Brazil (Haimovici et al. 2004, Perez 2006). In addition to the larger ones, fish sized in the 300-400 mm interval were common in regional fish markets (authors’ unpublished data) but with unknown fisheries areas.

Differing from the results by Villarino and Morioka (1999) for Genypterus blacodes (a close species with a wider geographical distribution along the south Pacific and also in the Argentine waters – south Atlantic), it was possible the recognize of the first age ring in G. brasiliensis. Although criticisms to marginal increment analysis (MAI) as an indicator of annulus formation, the requirements pointed out by Campana (2001), as the well-defined reproductive period (unpublished data), the samples obtained from throughout year (and higher than the minimum sample reported) and the APE and CV low values, may be strong reasons to be assumed the MAI results as realistic for Genypterus brasiliensis.

The estimated longevity, higher than 13 yr, did not differ from those of Chong and Aguayo (1990) (10 to 14 yr) but was smaller than Withell and Wankowski (1989) (21 yr), Horn (1993) (26-27 yr), and Wrzesinski (1984) (30-31 yr) for G. blacodes.

The VBGF fit the back calculated lengths extremely well; however, the values of L∞ seem to be overestimated. The maximum length reported for the species was 1,100 mm, 24.3% smaller than L∞. The overestimated value of L∞ can be due to the lack of older age-classes in the samples. Even though the L∞ is only an indicative of the population, estimated from the existing data, the low representativeness of larger specimens in the samples can be an indication of overfishing.

Females and males of G. brasiliensis have about the same weight-at-length before the estimated mean length at first maturity. After maturity, females are slightly heavier, which is consistent with growth studies of other species of the genus (Payne 1985, Japp 1990, Horn 1993, Baker et al. 2014, Vega et al. 2018), except for Withell and Wankowski (1989). Age at length observations showed that the fastest growth prevails in the earliest five to six years of the life span, thus approximately 50% of growth of asymptotic length is reached before age five for both sexes (491.59 mm in age 4 and 726.19 mm in age 6, respectively). The age-length keys for each sex suggest that at least 65% of the sampled specimens were caught under age of 4 yr, close to the age of first maturity (equivalent to 4.3-4.5 yr). Meanwhile, the age of the entire population maturity was supposed to be reached at 8 to 9 yr. Older specimens (ages higher than 9 yr) were scarce in the population, should be viewed as a risk for the sustainability of the fisheries of the species.

Values of K and mean age at first maturity (t_mat) are related to M (see Pauly 1980, Velasco et al. 2003). High values of M reduce the expected lifespan and consequently tend to be associated with higher K and lower t_mat. Although natural mortality rates estimated with Pauly’s method have been considered inaccurate by some authors (as Gulland and Rosenberg 1992, alternatively see Kenchington 2014 for some others remarks of estimation of M), other methods (such as Taylor, Alagaraja, Hoenig and Hewitt and Koenig) offered close values, particularly for females (0.101/yr, 0.155/yr, 0.152/yr and 0.101/yr). Alagaraja’s and Hoenig’s suggest much higher estimations (0.241/yr and 0.222/yr, respectively), similar to those estimated for G. blacodes (0.2/yr, at Punt and Japp 1994). Conversely, the method of Rikther and Efanov (1976), using the mean age of maturity, showed values of 0.264/yr and 0.406/yr. The M/K ratio (a measure of the validity of mortality estimates) from M values obtained from the Pauly method (1.01 for females and 1.048 for males) were under the range of 1.5 to 2.5 reported by Beverton and Holt (1959). Even using M values from the other estimations cited above, most of values for males were outside this interval (except when using M from Rikther and Efanov, generating M/K=1.72), with extreme values for females, 1.048 to 4.072 (the later estimate using Rikther and Efanov). Then, from the inappropriate use of distinct methods for different sexes, and as the M values estimated through Pauly’s (1980) method are not equal to 1.5K, nor the length of the first maturity is less than 2/3 of L∞, the analysis of Kirkwood et al. (1994) was unsuccessful. This situation leads us to face a distinct perspective to avoid the use of a fixed value for M. Another reason to strengthen not considering the recruitment constant is due to the annual variability of the oceanographic processes along the area, including the effective influences of the El Niño Southern Oscillation phenomena (ENSO), as discussed by Paes and Moraes (2007), to constraint the usefulness of the invariants presented on Beverton and Holt (1959) and Beddington and Kirkwood (2005).

As exposed, it can be inferred that Genypterus brasiliensis was experiencing an excessive fishing pressure, mainly over the juvenile stratum submitted to the coastal trawl fisheries, which suggests a troublesome scenario. Haimovici et al. (2004) reported the highest densities for the species to the upper slope of 32^o to 34^oS followed by 22^o to 23^oS (the later an area influenced by upwelling waters). Both areas are also intensive fishing grounds, especially after the beginning of the decade of 2000, when chartered fishery fleets had operated in southern Brazil (Perez et al. 2002). The most intense fishery efforts continued down the outer shelf and upper slope (100 to 250 m), in the zone whereas this species was one of the most fishable resources (Perez 2006). Moreover, as noted by Patterson (1992), stocks can sustain exploitation rates of only 0.5 to 1.0 times the natural mortality rate and allied to the underestimation of the optimal exploitation rate for long-lived resources, the species should be at risk.

Although no fecundity studies of Genypterus brasiliensis were known to date, and by acceptance of a similar pattern to G. blacodes, which includes the elder females of the genus as BOFFFF (Big Old Fat Fecund Female Fish), and their removal by fisheries should result in potential risk to the structure of the population (Hixon et al. 2013). It must be highlighted that individuals younger than 5 years old composed approximately 66% of male and 71.5% of the female catches of G. brasiliensis. In addition, the smallest fishes of valuable species (such as G. brasiliensis) often have minor interest from fisheries. Thus, the small fishes may not be reported in the landings and may be compounded in the discards (unreported catches), particularly in the trawl fisheries, generating an additional source of fisheries mortality that is not always recognized. Despite this, specimens smaller than 300 mm were reported in the double-rig trawl fisheries (Graça-Lopes et al. 2002), also in the discard of the species from the chartered pot and trawl fisheries fleets operating along upper slope off southern Brazil (Perez et al. 2002). The slow growth and a late complete maturation (7-9 yr), which suggests low biological production, allied to non-target fisheries interest, the low resilience and endemism, classify Genypterus brasiliensis as a potential vulnerable resource, jeopardizing a sustainable fishery. The catchable stock of the species is herein seen as another fisheries resource vulnerable to overexploitation. Until reliable quantitative biological data are available, precautionary management must be considered. Moreover, Genypterus brasiliensis is not cited on the worldwide IUCN and CITES red lists of endangered species. However, the southernmost Brazilian province (State of Rio Grande do Sul) includes this species on a regional list (State Law 51797 of September 8^th, 2014) as near threatened.

ACKNOWLEGMENTS

This text is part of an effort to recognize new fisheries resources from the Brazilian EEZ. The authors also thank Manuel Haimovici (Universidade de Rio Grande/UFRG) and Carmen L.D.B. Rossi-Wongtschowski (Instituto Oceanografico, Universidade de São Paulo/IOUSP) for encouraging this study. Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) provided an undergraduate (ITI ‘Revizee’) scholarship to CLTE, and Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP) provided a Post-doctoral scholarship to GV (Grant number 05/59715-2).

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Publication Dates

• Publication in this collection
  12 Aug 2019
• Date of issue
  2019

History

• Received
  8 Oct 2017
• Accepted
  17 Oct 2018