The biology, distribution and abundance of the ridge-scaled rattail (Macrourus carinatus) was studied in four seasonal bottom-trawl surveys in 2006–2009 using biological material collected on board different research and commercial fishing vessels. The species was found to exhibit ontogenetic and seasonal migrations. Upon switching to the demersal lifestyle, juveniles gradually move north with the Falkland Current. Adults return to the spawning areas (50–54°S) and remain there. They move seasonally along the slope from 54°S to 50°S between 500 m and 900 m, with males and females moving separately. The northernmost aggregations (at 50–51°S) occur in autumn, during the major spawning event. In winter, fish migrate south. During spring and summer the entire population gradually shifts north with ongoing minor off-season spawning. Females, which are the larger sex, tend to stay shallower than males. Such a sex-related migratory behaviour should be taken into account when the existence or absence of Heincke's law is considered for a particular species. A complicated migratory pattern should also be accounted for in fishery management.
Laptikhovsky, V. 2011. Migrations and structure of the species range in ridge-scaled rattail Macrourus carinatus (Southwest Atlantic) and their application to fisheries management. – ICES Journal of Marine Science, 68: 309–318.
Over the past 50 years, marine fisheries across the world have exhibited a steady trend towards the exploitation of increasingly deeper resources (Morato et al., 2006). Knowledge of the distribution, range, and migration of species is necessary for stock management, particularly in species such as deep-sea grenadiers that are easily overexploited (Merrett and Haedrich, 1997; Devine et al., 2006). Distribution ranges of deep-sea fish may be difficult to determine, however, particularly because many species are pelagic spawners and their larvae are widely dispersed by currents (Merrett and Haedrich, 1997). Furthermore, life in the deep seas exhibits seasonal responses, including seasonal spawning and migrations, which presumably reflect variability in the amount of organic matter delivered to the seabed over an annual cycle (Gordon, 1979; Bergstad and Gordon, 1994; Merrett and Haedrich, 1997). Such seasonal events have different impacts on the different ontogenetic stages of fish. As they grow, many deep-sea species move from shallower waters to relatively greater depths, and size distributions appear to follow the so-called Heincke's law (Heincke, 1913; Stein and Pearcy, 1982; Macpherson and Duarte, 1991; Merrett and Haedrich, 1997).
The ridge-scaled rattail [Macrourus carinatus (Günther, 1878)] is one of a few potentially commercially exploitable grenadiers (Merrett and Haedrich, 1997), and it is likely soon to become targeted by a trawl fishery in Falkland waters. The species is distributed from Subantarctic to temperate waters along both sides of South America, the Falkland Islands, Discovery Tablemount and Meteor Seamount, South Africa, off Crozet and Prince Edward Islands, and off New Zealand and Macquarie Island between 200 and 1200 m deep (Froese and Pauly, 2009). There is currently no directed fishery for it anywhere except the Southwest Atlantic. A short period of intense commercial exploitation began in 1988 with an annual catch of 48 679 t by a Russian fleet that was operating mostly on the western extension of the Falkland Trough in the Argentine EEZ following bilateral agreements. The catches gradually decreased to 14 822 t in 1991 when the fishery finished. Since then, the annual bycatch of the species in Argentine waters has been 2000–5000 t. In 2008, it increased to 12 348 t (Information of Secretaría de Agricultura, Ganadería, Pesca y Alimentos http://www.sagpya.mecon.gov.ar/) because fishers started to target the species as a result of increased market demand. No specific licence or TAC for this species exists in Argentina. In Falkland Island waters the species is a minor bycatch in longline and trawl fisheries, with annual landings less than 1000 t, including catches from recent research surveys (Laptikhovsky et al., 2008). In other regions of the Southern Ocean and adjacent seas the annual landings do not exceed 100 t (FAO, 2006).
In Falkland waters, the bathymetric range of this species generally coincides with the frontal zone on the western periphery of the northbound Falkland Current, where the surface primary productivity is greater than in either shallower or deeper waters (Laptikhovsky et al., 2008; Lutz et al., 2010). Macrourus carinatus is a large species: around the Falklands females attain 38 cm pre-anal length (PAL) and live up to 37 years, whereas males grow to 28 cm PAL with a maximum age of 34 years; size at 50% maturation is 20.18 and 16.8 cm PAL, respectively (Laptikhovsky et al., 2008). The species reproduces year-round with a major spawning peak in the austral autumn (April–June) and post-spawning females are found most often in July (Laptikhovsky et al., 2008). Macrourus carinatus feeds on a variety of prey which vary seasonally and ontogenetically (Laptikhovsky, 2005).
This study aimed to investigate the distribution of juvenile and adult M. carinatus in the Southwest Atlantic to determine their ontogenetic and seasonal migrations and to evaluate the implications of those factors to fisheries management, using biological data collected from different seasons and areas.
Material and methods
Data on grenadier biology and distribution were collected in the years 2006–2009 during four seasonal surveys carried out in Falkland waters by the commercial trawlers “Manuel Angel Nores” and “Jose Antonio Nores” (Figure 1). In all, 316 semi-commercial bottom trawls were carried out on the continental slope within the Falkland EEZ and in international waters (depth range 401–1391 m). The set-up was as follows: polyvalent doors of 2500 kg; headline 54 m; footrope equipped with rock-hoppers 69.5 m; horizontal opening 50 m; vertical opening 3.4–3 5 m; codend mesh size 95 mm. Towing speed varied from 3.2 to 4.1 knots and haul duration from 4 to 6 h. Another 24 hauls of the same duration were carried out with the Engel semi-pelagic trawl with “Super-V” doors; headline 40.2 m; and footrope equipped with rock-hoppers of 38.7 m. The vertical opening was about 12 m, horizontal opening 30–38 m, codend mesh size 95 mm. Towing speed was 3.2–3.7 knots. The semi-pelagic trawl was deployed on the bottom (i.e. not in the pelagic layers above the seabed). To estimate relative species densities, a catchability coefficient of 1 (i.e. that all fish present on the trawl path were caught) was assumed for all tows. Engel trawl tows were excluded from analysis of density distribution, although biological data collected from them were used. In all, 37 775 fish were sampled from these survey catches.
Another set of data was collected on board RV “Dorada” from 1999 to 2007 between 173 and 1097 m using the same semi-pelagic Engel trawl, although the haul duration was 1–2 h. In all, 6341 grenadiers were sampled.
In addition, 3596 fish from 196 hauls were sampled from 1999 to 2009 on board 26 commercial trawlers (with varying bottom-trawl types) over the shelf edge and upper part of the slope in Falkland waters, depth range 140–465 m. The biological data represented all seasons (Figure 2). To study the variation in maturity of females, the gonadosomatic index (GSI) was calculated during the female pre-spawning migration. Ovary weight, eviscerated weight (EW), and GSI were estimated in 1331 fish sampled in February 2009.
A total of 100 fish was sampled randomly from each haul. In some cases, if only a few fish were caught, all were sampled, with the sample size often as small as 1–20 fish, particularly in shelf waters. The PAL was to the nearest 1 cm and body weight to the nearest 1 g. Sex and maturity stage were assigned following the eight-stage maturity scale (Nikolsky, 1963; see Brickle et al., 2005). Upon achieving maturity, ovaries always contain two groups of yolked oocytes and the fish never return to stage II. Spent testes contain a large amount of sperm and are easy to confuse with those of spawning fish, which is also true for some other species of Macrouridae (Alexeeva et al., 1991, 1992). Because of this, we considered all fish at stage III and above as mature, including fish at stages V and VI (hydrated eggs in the ovary) that were spawning. Fish above size of 50% maturity were considered to be adults.
To estimate GSIs, gonads and all intestines were removed, after which gonad and eviscerated body weight were measured. The GSI was calculated as 100 × gonad weight (GW)/EW.
Because of the delayed oceanographic seasonality at depth (Arkhipkin et al., 2004), the following seasons were assigned for Falklands waters: summer (January–March), autumn (April–June), winter (July–September), and spring (October–December). Spatial distribution of the species was analysed using data from the “Manuel Angel Nores” and “Jose Antonio Nores” surveys. Each haul of these surveys was conducted along the same isobath with no more than 50 m difference between the upper and lower limit. ESRI ArcGIS Version 9.1 was used to average grenadier catches (kg h−1) by the grid squares used in fisheries management around the Falkland Islands. The grid squares were 15′ latitude by 30′ longitude, about the distance covered by one research haul (10–20 nautical miles).
Ontogenetic changes in spatial distribution
Smaller juvenile and subadult fish of PAL <10 cm were found everywhere over the area sampled, with the extent of the northward distribution increasing with length of juveniles (Figures 3 and 4). After fish reached the size at 50% maturity (17–20 cm PAL), both sexes moved to the south and adult fish were recorded predominantly south of 50°S (Figure 4). Because of these ontogenetic differences in distribution, the species range could be divided into two distinct regions with different length frequency distributions. In the north, between 41°S and 50°S, the bulk of the population was represented by subadult fish of 20 cm PAL and less. In the south (50–54°S), most of the fish were adult (21 cm PAL and above). A change occurred relatively suddenly, without either gradual changes in modal size or a transient zone between these two parts of the range (Figure 3).
Seasonal changes in spatial distribution
In spring (October–November), abundance peaked between the Falkland Islands and Burdwood Bank (Figure 5a). In summer (February), fish were more or less evenly distributed along the Falkland slope between 51°S and 54°S (Figure 5b). In early autumn (mid-March–April), when the major peak of spawning appeared, the highest densities of grenadiers were observed on the eastern edge of the Falkland slope, whereas fish abundance south of 53°30′S was low. Distribution of grenadiers in winter (July–August) was similar to that in spring, with most of the adult population having migrated south of 53°S (Figure 5d).
In spring, females were distributed more or less evenly over the population's range (Figure 6a). Adult males were concentrated mostly south of the islands on the northern slope of the Falkland Trough between 53°S and 53°30′S (Figure 7a). In summer, the grenadiers started to move north, with adult females becoming relatively more abundant north of 52°S (Figure 6b), and adult males extending the zone of their maximum abundance to almost 51°S (Figure 7b). In late summer (Figure 6c), females were most dense at the major spawning grounds north of 51°S. Male aggregations shifted to the same position, with their maximum density observed between 50°S and 53°30′S and east of 59°W (Figure 7c). They probably reached the spawning grounds later, during the peak of reproduction in late April–May, but we do not have data on fish abundance for that period. In winter, both sexes migrated back to the south, with females foraging mostly from the northern slope of the Falkland Trough, from 52°30′S to 53°30′S (Figure 6d), whereas males were densely aggregated on the southern slope (Burdwood Bank, 53°30′–54°30′S; Figure 7d). The proportion female decreased with depth in all seasons (Figure 8).
Because the species reproduces year-round, the spawning area changes with the migration of the adults (Figure 9). The major spawning migration at the end of summer takes several months and, at that time, grenadier GW increases. A comparison of the GSI of adult females between different parts of the species range in February 2009 demonstrated an increase from the main foraging area (southwest) through the intermediate region (centre) to the major spawning grounds (northeast). Female GSIs were statistically different between these three areas (ANOVA, p < 0.0001, Kruskal–Wallis test: 24.62; northeast vs. central: t = 3.85, p = 0.0002, F-test, p = 0.009, n = 260; southwest vs. central: t = 2.66, p = 0.008, F-test p = 0.027, n = 458; northeast vs. southwest, t = 4.36, p < 0.0001, F-test p = 0.1199, n = 240).
Ontogenetic changes in spatial distribution
Because the smallest juveniles (PAL <5 cm) were found only in the proximity of the spawning grounds, it is likely that juveniles switch to a demersal lifestyle rather quickly. Eggs and larvae may be transported long distances by the northbound Falkland Current despite a presumably long embryonic development [in concurrence with a large egg size (2.9–3.3 mm; Ciechomski and Booman, 1981) and low temperatures]. The retention of early stages is probably aided by the south-directed counterflow along the 400–800 m isobaths, which is located above the major spawning grounds at the western border of the Falkland Current (Figure 5b in Laptikhovsky et al., 2008). Eggs, larvae, and early juvenile grenadiers, although pelagic, do not rise in the surface waters where current speeds are generally highest, but generally occur in the deeper epipelagic and upper mesopelagic zones (Stein, 1980; Bergstad and Gordon, 1994; Merrett and Haedrich, 1997; Fukui et al., 2008). Large numbers of Macrourus sp. eggs (described as those of M. whitsoni because of uncertainties with systematic status at the time) were found in August in the upper 100 m layer of the Falkland Trough and Burdwood Bank in waters 508–710 m deep (Ciechomski and Booman, 1981). The eggs had hexagonal sculpturing, which inhibits ascent rate upon fertilization and development. This ornamentation is a particular trait of “shallow-water” grenadiers, whose midpoint of their depth range is above 900 m (Merrett and Haedrich, 1997). The period of egg collection at Burdwood Bank also coincided with winter migration of adult M. carinatus to this area (Figure 5d). The eggs collected on the uppermost slope probably belonged to M. carinatus. It is still possible, however, although unlikely, that they were spawned by M. holotrachys, which inhabits water mostly deeper than 1000 m, with spawning females deeper than 1200 m (Laptikhovsky, 2005; this study).
A gradual northward distribution of juvenile fish is likely to reflect drift along the Falkland Current, which moves over the bottom between 500 and 1000 m at latitude 51°40′S (Laptikhovsky et al., 2008). Northern waters are considered nurseries and juvenile feeding areas. As the fish grow older and attain maturity, they appear in the south. The region 42–49°S is inhabited by immature subadults, mostly below the size of 50% maturity, which is 20.2 cm in females and 16.8 cm in males (Laptikhovsky et al., 2008). Adult fish are scarce there and could be caught only in the very south of this zone.
A substantial dataset (22 663 specimens) collected by Russian researchers from 1975 to 1986 (Alexeeva et al., 1992) also demonstrated only subadults at 42°S, that some maturing fish could be caught at 47°S, and that adult fish were only south of 50°S. A particular trait of grenadier reproductive strategy is that spawning fish already possess the oocyte reserves for the next reproductive period and that spent females return to maturity stage III and not to stage II (which occurs only once in a lifetime; Alexeeva et al., 1992). This means that once it has begun, vitellogenesis never stops, and this irreversible change of physiology corresponds to the final migration of adult fish to the spawning areas. Such a pattern of ontogenetic migration probably is an adaptation for better use of feeding resources. It is also likely that juvenile and subadult growth will be accelerated in the warmer waters between 42°S and 49°S, which is extremely important for a slow-growing deep-water species. Such large-scale ontogenetic longitudinal migration was never documented in deep-sea grenadiers, but has been found in some other fish, such as Greenland halibut (Reihardtius hippoglossoides; Albert, 2003) and probably in another abundant deep-sea fish spawning around the Burdwood Bank, the Patagonian toothfish (Dissostichus eleginoides; Arkhipkin et al., 2003; Laptikhovsky et al., 2006).
Seasonal changes in spatial distribution
Grenadiers from the upper part of the continental slope often exhibit seasonal movements between shallower and deeper water (Tuponogov, 1997; Dolgov et al., 2008; Orlov and Tokranov, 2008), similar to many other deep-sea fish (Allen, 2006; Shephard and Rogan, 2006). Long-range seasonal horizontal migrations, however, are apparently unusual for macrourids. The roundnose grenadier (Coryphaenoides rupestris) is probably the best-studied species of the family, because it is also the most important commercially (Cohen et al., 1990). Although the existence of seasonal spawning migrations was suggested for that species (Cohen et al., 1990), Lorance et al. (2008) claims there are no data available to indicate whether or not individuals move around during their lifespan. One species for which such lengthy horizontal migrations were suggested is the giant grenadier (Albatrossia pectoralis; Tuponogov, 1997; Orlov and Tokranov, 2008), which is the world's largest and possibly most mobile grenadier. A possibility of such migrations was also suggested for the deepest-living grenadier species, Coryphaenoides armatus, because of seasonal differences in fish size observed by baited photographic landers (Priede et al., 2003; King and Priede, 2008). Other examples of migratory deep-sea families include benthopelagic halibuts of the family Pleuronectidae, black scabbardfish, and benthopelagic adult Patagonian toothfish (Boje, 2002; Figueiredo et al., 2003; Laptikhovsky et al., 2006; Loher and Seitz, 2006).
Our data suggest that grenadiers, at least the large species studied here, can carry out seasonal migrations over distances of a few hundred kilometres, with both sexes moving separately and at different depths. A possibility of sex segregation by depth should be kept in mind when the existence or absence of Heincke's law is considered for a species with different male and female sizes. Migration patterns of this scale and character should be taken into account in fishery management. Another observation, outside the scope of this paper, is that a significant portion of the northern Falkland slope between 49°S and 50°S is covered by deep-sea coral (mostly Paragorgia arborea). A few trawl hauls carried out in the coral-rich subarea revealed that grenadier abundance in this transient zone is low. To avoid destruction of corals, however, protective measures may still be needed.
The complicated structure of this species' range revealed here raises many issues related to the management of the potentially expanding fisheries. The most important of these are: (i) protection of the spawning fish concentrations that apparently move seasonally along the Falkland slope; (ii) protection of deep-sea coral forests between 49°S and 50°S; (iii) consideration of the bycatch of blue whiting (Micromesistius australis) and hoki (Macruronus magellanicus) in the shallowest part of the species range (<500 m); (iv) the bycatch of Patagonian toothfish in the deepest part of the species range (>900 m); and (v) interaction with fisheries in Argentina which take some large females foraging in winter on the western shallow extension of the Falkland Trough. All these issues should be addressed when regulating fishing seasons, positioning of fishing grounds, and ITQs for commercial harvesting of grenadier stocks.
The ridge-scaled rattail (M. carinatus) is a grenadier that exhibits ontogenetic and seasonal latitudinal migrations. Juvenile grenadiers gradually move from the spawning grounds (50–54°S north with the Falkland Current until the limits of the range evaluated here (41°S). As they grow and mature, they return to what appears to be a spawning area, from which they never return. Adult fish move seasonally across the slope between 500 and 900 m, with males and females apparently migrating separately. The northernmost aggregations (at 50–51°S) are in autumn, during the major spawning event, and thereafter, in winter, fish migrate south with females occupying the shallower part of the depth range. During spring and summer, the entire distribution gradually shifts north, and there is also some spawning.
The range of M. carinatus could be divided into two major parts: (i) a juvenile and subadult foraging and growth area that occupies waters between 50°S and 41°S (and probably farther north); (ii) a reproductive area between 50°S and 54°S. Some juveniles are also found in these waters. The functional structure of the species range within these two major areas could be presented as the following: (i) a zone of larval settlement which probably coincides with spawning grounds (54–50°S; unfortunately, we do not have data on the distribution of early juveniles of 1–2 cm PAL); (ii) nursery grounds, between 54°S and 41°S, gradually extending northward with juvenile growth; (iii) subadult foraging and maturation areas which coincide with nursery grounds at their maximum northward extent; and (iv) spawning grounds, varying seasonally between 54°S and 50°S.
Such a complicated structuring of the distributional area of M. carinatus, as well as adult seasonal migratory behaviour, may also characterize other grenadiers. More investigations should be carried out, even for the best-studied species, to allow the development of proper strategies for the management of grenadier fisheries.
I thank the crew of FVs “Manuel Nores” and “Jose Antonio Nores” and the FIFD scientific observers Lars Jürgens, Alastair Baylis, Alex Blake, and Robert Whiteley for their assistance. I specifically thank fishing master Len Featherstone for his dedication to the investigation of this species and to developing bottom-friendly fishing gear and tactics, A. I. Arkhipkin, O. A. Bergstad, P. Brickle, and G. M. M. Menezes for their comments, Judith Brown for improving the English, and two anonymous referees for their inputs.