Abstract
Black scabbardfish is a deep-water species, common in the NE Atlantic at depths between 450 and 1300 m, currently exploited by some European countries. Between May 1998 and April 2000, specimens collected at three different locations in the NE Atlantic—NW of Scotland, Sesimbra (mainland Portugal) and Funchal (Madeira)—were analysed. The evolution of maturity of both sexes throughout the year was studied based on the macroscopic and microscopic analysis of the gonads. Specimens with the largest total length were found in Funchal, whereas the smallest size was recorded in the NW of Scotland. Neither spawners nor post-spawners were ever observed in NW of Scotland and Sesimbra. In Sesimbra, only a few individuals attained pre-spawning stage and most of the early developing females exhibited atresia in their ovaries. In Funchal, all the maturity stages were found; spawners occurred from September to December (females) and from August to December (males). Length of first maturity for females was estimated to be around 1000 mm. Two groups of spawners with different sizes were observed during the spawning period off Madeira.
Introduction
Black scabbardfish (Aphanopus carbo Lowe, 1839) is a deep-water species of the family Trichiuridae. It has a world-wide distribution, with records in the NW and NE Atlantic, from Iceland to the south of Madeira Island (Anon., 1984; Gordon, 1986; Merrett et al., 1991), southern Indian Ocean (Piotrovskii, 1979) and north-western Pacific (Clarke and Wagner, 1976). This species occurs from 200 m depth around British Isles (Tucker, 1956) to 1800 m to the south of Madeira Island (Martins et al., 1987). The black scabbardfish is the target species of two Portuguese longline fisheries: the long established Madeira fishery (since the early 19th century) and the more recent fishery off the Portuguese mainland (since 1983). In northern European areas, the growing landings of this species result from multi-species deep-water trawl fisheries mainly from France and United Kingdom.
Despite the increasing commercial interest in this species, little is known about its life cycle. The existing contributions on the reproduction usually allude to a short analysis of maturity and to the size range of captured specimens. In the waters to the north of the British Isles, the majority of caught specimens were immature or in an intermediate stage of maturity (Kelly et al., 1998); there is only reference to two individuals caught at the Porcupine Bank in January with ripe gonads (Ehrich, 1983). Specimens in a spent condition were found in Icelandic waters between January and March (Magnússon and Magnússon, 1995). No spawners were ever observed off the Portuguese continental coast (Machado et al., 1998; Anon., 2000). Specimens in pre-spawning and ripe condition were observed in Madeira waters between September and February (Carvalho, 1988; Anon., 2000) and in Azorean waters in August (Anon., 2000). The main objective of this article is to examine recent data on maturity from three distinct areas in the NE Atlantic—NW Scotland, Sesimbra (Portuguese continental coast) and Funchal (Madeiran waters) (Figure 1)—focusing the reproductive behaviour of this species and discussing its reproductive strategies.
NE Atlantic areas (black arrows) from where black scabbardfish samples were obtained.
Methods
Fish samples were obtained from bottom longline landings at Sesimbra (June 1998–April 2000) and Funchal (May 1998–December 1999) fishing ports and from bottom trawls held by the Marine Laboratory, Aberdeen (MARLAB) during research surveys (September 1998, October 1998 and March 1999).
In the laboratory, all individuals were measured to the nearest millimetre and later grouped in 10 mm total length (TL) classes. Individual total weight was also recorded to the nearest 1 g and their gonads removed and weighted to the nearest 0.01 g. Macroscopic maturity stages were assigned to specimens using the maturity scale defined by Gordo et al. (2000). Histological sections of gonads were also made, especially in cases where the assignment of maturity stages was ambiguous. The preparation of sections included the preservation of gonads in Bodian's AFA (Lillie and Fulmer, 1976) during a period of time between 1 and 6 days, depending on their thickness. They were later embedded in paraffin wax, sectioned at 4–9 μm and stained using Masson trichrome (females) and Heidenhain Azan (males).
Results
A total of 2443 fish were sampled in the three NE Atlantic areas: Funchal (1249), Sesimbra (826) and NW of Scotland (368). Females were predominant in the samples, with the exception of those collected in Funchal in July and December. Specimens sampled in the NW of Scotland (length range: 612–1175 mm) were smaller than those from Sesimbra (length range: 667–1365 mm) and Funchal (length range: 712–1510 mm).
In the NW of Scotland, individuals were either in maturity stages I or II. The majority of males were in maturity stage I (87%), while females were more frequently found in stage II (52%) with the exception of October where stage I was more common (64%). These two maturity stages were almost exclusively observed in both males and females from Sesimbra, where no specimens in stage IV or V were found. In this area, some individuals began their gonadal development in July reaching maturity stage III in August—2% of the total number of specimens. However, between December and April, the majority of females in stage II showed a clear increase in the incidence of atresia (from 9.5 to 25%) in early-developed oocytes (Figure 2). In contrast to the other regions, all the maturity stages were recorded in Funchal for both sexes. Stage II (Figure 2) was found throughout the year, being more common between March and April. Stage III appeared in males mostly in May, while in females it appeared later in July. Stage IV occurred mainly from September to December (females) and from August to December (males). For the remaining maturity stages, the very low occurrences (usually below 4%) of stage I for both males and females and the long duration period of stage V (from November to June) must be pointed out.
Histological sections of stage II ovaries from a specimen sampled in Funchal and Sesimbra. In the section from Sesimbra some atretic oocytes are indicated by an arrow.
Spawning should occur preferentially during the last quarter of the year, where the highest GSI values were registered (Figure 3). Since insufficient data on maturity were available for males, the maturity ogive was only adjusted to female data for the period between September and February, which coincides with the spawning period. Based on the estimates obtained, the length of first maturity is about 1028 mm (Figure 4). Frequent macroscopic stage assignment errors (later corrected by microscopic analysis) were registered in stages I and V. However, the analysis of GSI indicated that specimens in maturity stage V presented higher values than those in maturity stage I (Figure 5). Actually, the GSI values of stages I and V were significantly different (t-test; p-value <0.01). As a consequence, this index can be considered a useful and expedite tool to help in the differentiation of these two stages.
Maximum (–) median (•) and minimum (–) values of GSI estimated by month for black scabbardfish sampled in Funchal.
Maturity ogive of black scabbardfish females sampled in Funchal for the period between September and February.
Distribution of GSI values of maturity stages I and V by month in Madeira.
The analysis of histological sections from females in maturity stages III and IV suggested that oocyte development is essentially group-synchronous. Indeed, only one group of well-developed and bigger size oocytes was identified before spawning.
To further understand the reproductive strategy of this species, a comparative analysis of GSI values from Sesimbra and Funchal was carried out. This analysis was restricted to ranges of length and maturity stages common to both areas (stage II females with TL between 1100 and 1210 mm). The highest GSI values were observed in specimens from Funchal, namely, in April and July (Figure 6). In addition, after the analysis of stage IV females sampled versus TL, two different groups of spawners were identified: (i) individuals with TL smaller than 1250 mm, which spawn early in the spawning season (between September and December) and (ii) individuals with TL larger than 1250 mm, which spawn preferentially in January and February. This finding is further corroborated through the monthly distribution of GSI values of maturity stage V females (Figure 5), which showed an increase from October to December followed by a decreasing trend that lasted until May. In June, the variability of GSI values was high. Furthermore, the analysis of GSI values by length from March to June (Figure 7) revealed the existence of two groups of post-spawners: one occurring in June with individuals above 1300 mm TL and other from March to May exhibiting lengths predominantly below 1300 mm TL.
Monthly distribution of stage II GSI values of females with TL between 1100 and 1210 mm sampled in Sesimbra and Funchal.
Variation of GSI values versus total length of stage V specimens.
Discussion
The range of black scabbardfish total length varied between areas. Largest specimens were sampled off Madeira (above 1400 mm TL) while smallest ones were collected in the NW of Scotland (below 650 mm TL). Such length differences between northern and southern areas (separated by parallel 40°N) were also verified in a recent study based on an enlarged length dataset (Carvalho and Figueiredo, 2001). Geographic and fishing gear (trawl in the north and longline in the south) factors may be responsible for these differences although their individual contributions are difficult to disentangle.
In all the areas, juveniles (TL below 900 mm) were scarce, particularly during the pre-recruitment phase. So far, there are only two records of small specimens (100 and 150 mm TL) that were found in the stomach of an Alepisaurus ferox Lowe, 1833, captured off Madeira (Maul, 1954).
The macroscopic assignment of maturity stages was sometimes difficult probably due to the slow rate of gonadal development. However, the analysis of GSI values by maturity stage constituted important auxiliary information for a correct assignment of maturity stages since the ranges of GSI from different stages were different and did not overlap.
Based on our results, black scabbardfish exhibits temporal sexual maturation differences according to region in the NE Atlantic. Vitellogenesis begins in Funchal and Sesimbra at the same time of the year, however, only the specimens from Funchal continue their gonadal development towards maturation and egg release. No spawners were found in Sesimbra and NW Scotland, while off the Portuguese mainland a small percentage of specimens reached the pre-spawning stage, in NW Scotland only initial development stages (I and II) were found. The predominance of pre-adult specimens at NW Scotland, either immature or in an early development stage not evolving to more developed maturity stages, might reflect insufficient levels of energy to proceed with gametogenesis.
In Sesimbra, early maturing specimens larger than the length of first maturity (ca. 1028 mm) enter into an intense process of atresia after October with a maximum in March. Atresia affects oocytes in different developing stages and the reabsortion process occurs throughout the ovary. This suggests that although those specimens are potentially capable of reproducing, they do not enter into a spawning process and remain in a resting phase that can extend far beyond the spawning season. Possible reasons for the observed cessation of the maturation process could also be related to insufficient levels of accumulated energy or unfeasible prospects of a successful reproduction. This arrest in the maturation development due to low levels of energy accumulated has also been observed for the north European eel (Anguilla anguilla) population and related with delays in reproductive migrations (Svedäng and Wickström, 1997).
In Madeiran waters, spawners occurred mainly from September to December, which is in agreement with earlier results (Carvalho, 1988; Anon., 2000). Two distinct reproductive strategies seem to be followed by the species in that area as different size specimens spawn at different time periods. While smaller size spawners occur between September and December, larger individuals preferentially undertake spawning in January and February. These findings were also corroborated by the existence of two female post-spawner groups during the spawning period. At more northern latitudes (Icelandic waters), spent individuals were recorded between January and March by Magnússon and Magnússon (1995), which suggests that the species may also reproduce in northern waters in areas not surveyed by the present study and slightly after the spawning season off Madeira.
Despite the fact that we only analysed data from three locations, it seems that black scabbardfish presents different reproductive strategies according to the sampled area in the NE Atlantic. The maturity data collected at these areas also favour the existence of reproductive migrations to spawning areas. This is in agreement with some authors who have already suggested that the species undertakes horizontal migrations to spawning and nursery grounds (Geistdoerfer, 1982; Kelly et al., 1998; Anon., 2000).
This study was supported by DG XIV of the European Commission through Study project 97/0084 entitled “Environment and biology of deep-water species Aphanopus carbo in NE Atlantic: basis for its management (BASBLACK)”.
