Biological characteristics of a resident population of Atlantic cod (Gadus morhua L.) in southern Labrador
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1 ICES Journal of Marine Science, 59: doi:1.16/jmsc , available online at on Biological characteristics of a resident population of Atlantic cod (Gadus morhua L.) in southern Labrador Corey J. Morris and John M. Green Morris, C. J., and Green, J. M. 2. Biological characteristics of a resident population of Atlantic cod (Gadus morhua L.) in southern Labrador. ICES Journal of Marine Science, 59: The growth, length at age, time of spawning, food, and movements of the genetically distinct, resident northern Atlantic cod (Gadus morhua L.) in Gilbert Bay, Labrador, were studied over four consecutive years (1998 1). Angling and plankton nets were used to sample all stages of the life history. During the study, 2453 cod were tagged with Floy t-bar tags, but none were recaptured outside the bay. Length-at-age is smaller than those of other Atlantic cod off Newfoundland and Labrador. Males mature at cm total length (TL) and 4 6 years of age, and females at cm, 4 8 years of age. Spawning starts shortly after ice retreats from the bay, usually in mid-may, and lasts for 3 weeks, a much shorter duration than reported for other northern cod. Timing appears critical to the retention of spawning products in the bay. Stomach contents indicated a wide range of benthic prey but that food availability may be low, contributing to the slow growth rate, individual cod targeting a small number of prey types. Gilbert Bay cod could be threatened if they continue to be managed as part of the Newfoundland Labrador northern cod stock. 2 International Council for the Exploration of the Sea. Published by Elsevier Science Ltd. All rights reserved. Keywords: bay cod, feeding, Gadus morhua, growth, local adaptation, reproduction, site fidelity. Received 9 July 1; accepted 1 April 2. C. J. Morris and J. M. Green: Department of Biology, Memorial University of Newfoundland, St John s, Newfoundland, Canada A1B 3X9. Correspondence to J. M. Green: tel: ; fax: ; jmgreen@mun.ca. Introduction Historically most northern Atlantic cod (Gadus morhua L.) off Newfoundland and Labrador migrated inshore in summer, feeding on capelin, and returned offshore in autumn to overwinter and spawn (Lear, 1984; Lear and Green, 1984). Reports of Atlantic cod overwintering and spawning inshore, however, have long indicated that a component of the northern population is resident (Thompson, 1943; Templeman, 1979). This inshore component never supported large fisheries and therefore was considered relatively unimportant from a management perspective (Lilly, 1996). Since the collapse of the northern cod fishery in the early 199s, the greatest densities have been found in a few inshore locations (Shelton and Healey, 1999), leading to an increased interest in the so-called bay cod. The Atlantic cod found in NAFO divisions 2J3KL off Newfoundland and Labrador differ in growth rate, age and size at maturity, spawning areas, timing of spawning, migration patterns, and morphology (Templeman, 1962, 1979, 1981). Genetic data have also pointed to a population structure within the range of the species (Ruzzante et al., 1997, 1999, ), the most genetically distinctive population recognized to date being in Gilbert Bay, Labrador (Beacham et al., 1999, ; Ruzzante et al., ). As anticipated from the genetic data, sonic tracking of Gilbert Bay cod has revealed that they are resident within the bay throughout the year (Green and Wroblewski, ), even though there are no obstacles to their movement away. The importance of maintaining such genetic and phenotypic diversity in Atlantic cod, and other commercial species, has been emphasized by Smedbol and Stephenson (1). Based on genetic distinctiveness and the restricted movements of Gilbert Bay cod, we hypothesized that they would exhibit life history characteristics different from those of other northern cod. Here we report on four years of data on the growth, size- and age-at-maturity, time of spawning, movement patterns, and food of Gilbert Bay cod which demonstrate differences in life history between this population and other northern cod /2/ $35./ 2 International Council for the Exploration of the Sea. Published by Elsevier Science Ltd. All rights reserved.
2 Biology of a resident population of cod in southern Labrador ' Snooks Arm Gilbert Bay Main Arm Latitude (N) The Shinneys River Out Long Arm Williams Harbour Labrador Gilbert Bay Alexis Bay 52 3 ' Newfoundland 5 1 km 56 ' Longitude (W) Figure 1. Map of Gilbert Bay, Labrador, and surrounding areas ' Materials and methods Study site Gilbert Bay, a narrow inlet on the southeast coast of Labrador, N W (Figure 1), is approximately km long and has an area of 6 km 2. Entrances to the bay from the Labrador Sea and neighbouring Alexis Bay are restricted to three channels each approximately 5 m wide. The maximum water depth is 8 m, but most of the bay is shallower than 3 m. Adjoining the bay s main arm are several smaller arms, The Shinneys, Long Arm, and Snooks Arm (Figure 1), each with a shallow, narrow entrance. These three arms meet in an area known as River Out. Two major rivers (Shinneys and Gilbert) empty into the bay, and each contributes significant inflow of freshwater during the spring thaw. Owing to this influx of freshwater, surface water is usually discoloured, particularly near the mouths of the major rivers. Surface water temperature in Gilbert Bay is sub-zero for 6 months, from December until May (Figure 2). When ice retreats from the bay, usually between early and mid-may, near-surface water temperature increases rapidly. During 1999, water temperature 3 m deep in The Shinneys increased from 1 to4 C between 7 and 1 May, and that 8 m deep increased from 1 to C between 1 May and 11 June, and then to 4 C between 1 and 16 June (Figure 2). Near-surface ( 1 m) water temperatures rise rapidly in spring, reaching >6 Cbythe
3 668 C. J. Morris and J. M. Green Temperature ( C) m 13 8 m May Jun. Jul. Aug. Sep. Oct. Nov. Dec. Jan. Feb. Mar. Apr. May Jun. Jul. Aug. Sep. Oct. Nov. Dec. Figure 2. Water temperature recorded in The Shinneys, Gilbert Bay, Labrador, at depths of 3 and 8 m, May 1998 December Depth (m) Temperature ( C) 7 Salinity Station 1 Station 2 Station 3 35 σt (g cm 3 ) Figure 3. Vertical profiles of temperature, salinity, and density at three stations in The Shinneys, Gilbert Bay, Labrador, on 1 June Stations 1, 2, and 3 were approximately 1, 2, and 4 km respectively from the mouth of the Shinneys River first week of June, and can exceed 15 C at their maximum. Vertical profiles of temperature, salinity, and density collected on 1 June 1997 at three stations at increasing distances from the mouth of the Shinneys River (Figure 3) revealed steep temperature and salinity gradients in the upper 4 5 m of the water column during May and early June. By the end of July, river flow has decreased significantly, and surface waters have a salinity >. Temperature and salinity conditions are similar during spring in the main arm of Gilbert Bay, near the mouth of the Gilbert River. Sampling Samples of Gilbert Bay cod were collected between 1998 and 1. Adult and juvenile fish were caught by angling, at depths usually between 2 and 1 m during two or three sampling trips each year (Table 1).
4 Biology of a resident population of cod in southern Labrador 669 Table 1. Summary of angling, tagging, and recapture data for Atlantic cod in The Shinneys, Gilbert Bay, Labrador, Recaptures include those made in the same year as tagging. Sampling date Number caught Number tagged Number sampled Recaptures 3 1 June June July 5 August May 1 June and 25 June August June August May 1 June June July 5 August Total Sampling began in late May or early June, 2 3 weeks after land-fast ice had dispersed. Most fish were caught in The Shinneys, but limited angling was also carried out in River Out and the main arm of the bay. Some data were also obtained from cod caught in the main arm of the bay by recreational fishers during the food fishery of 28/29 August Total length (TL) was measured to the nearest mm, and weight to the nearest 1 g, on an Acculab model VI balance. Most fish >25 cm (2453) were tagged with Floy t-bar tags (Floy Tag Company), and released. Approximately every 12th fish was sampled to determine age, sex, maturity, and stomach contents. This number included all tagged fish recaptured at least one winter after being tagged. Otoliths were removed and stored dry in scale envelopes; their age was later determined as described by Wells (198). Otoliths were also read by Canadian Department of Fisheries and Oceans (DFO) personnel with extensive experience of age determination of Atlantic cod. Ovaries and testes were inspected visually to determine sex and maturity status, following Morrison (199). Stomachs from 229 cod were opened and their contents examined in the field. Those with food were recorded as being X, Y-, Z-filled, or full, and the number of individual food items in each taxa were counted. Early life history stages (eggs, larvae, and pelagic juveniles) were sampled with a plankton net of 1 m diameter and mesh size 333 μm. Horizontal tows of 15 minutes duration were made at depths of 2 m and 7 m. The depth of the net was determined by the angle of the tow rope, which was controlled by boat speed. Surface tows and deeper tows were 914 and 655 m long respectively, as estimated from aerial photographs on which tow tracks had been drawn, and on average sampled 718 and 515 m 3 respectively. Series of tows were made during the spawning season (late May early June), close to the time when cod eggs were estimated to be hatching (mid-june early July), and in their pelagic larval and post-larval stages (late July early August). Hatching date was estimated from the relationship between developmental rate and temperature (Pepin et al., 1997). Sampling for eggs (May and June) was restricted to The Shinneys, and for larval and post-larval cod to the main arm of the bay as well as The Shinneys. Eggs were preserved in a 5% unbuffered formalin/ seawater solution. Using a dissecting microscope, developing embryos were placed into one of four stages identified and described by Markel and Frost (1985). Stage 1 included eggs from the time of spawning to the formation of the embryonic axis, about mid-gastrula. From this stage to the point where the embryonic axis reached half-way around the yolk, eggs were classed as stage 2. Stage 3 extended from the end of stage 2 to the point where the tip of the tail reached the snout, and stage 4 from the end of stage 3 to hatching. Results Growth During the study 3267 cod were captured and measured; of these, 84 were weighed. Angling catches from 1998 to 1 are summarized in Table 1. Age was determined for 32 fish, ranging in total length from 17 to 65 cm and in age from 2 to 15 years (Figure 4). There was an 87% agreement between our readings and those made by DFO personnel. Where there were differences, 7% involved a single year. A von Bertalanffy growth curve was fitted separately to length and age data for fish sampled in The Shinneys and the main arm of Gilbert Bay (Figure 4). Fish from the main arm of Gilbert Bay were longer at age than those from The Shinneys; L-infinity was 63.2 cm for the former and 61.6 cm for the latter. Although some cod as long as 1 cm were
5 67 C. J. Morris and J. M. Green Length (cm) n = 11 n = 2 n = 4 n = n = 29 n = 12 n = 7 n = 14 n = 28 n = 27 n = 25 n = 18 n = 5 n = 1 n = 2 n = 4 n = 1 n = 9 n = 13 n = 26 n = 38 n = 1 n = 1 Gilbert Bay Main Arm I = 63.2 (1 e.16(t + 2.9) ) The Shinneys I = 61.6 (1 e.17(t.74) ) Age (years) Figure 4. Length-at-age of male and female Atlantic cod sampled in The Shinneys (1998 1) and in the main arm of Gilbert Bay (1998). The latter samples were from recreational fishers. Data are fitted to the von Bertalanffy growth curve and 95% confidence intervals are shown. captured, few ages were determined for fish >65 cm because most of those were released because of their small numbers. In all, 34 fish were recaptured in The Shinneys between 334 and 798 days after being tagged. Their ages were determined from otoliths, and their growth rates between tagging and recapture were calculated. These values were then converted to annual growth rates and are plotted in Figure 5 along with annual growth rates based on the von Bertalanaffy growth curve calculated for fish from The Shinneys (Figure 4). Yearly growth of 2-, 3- and 4-year-old fish is evident from the modes in the length frequency distributions of fish caught in The Shinneys during June of each year of sampling (1998 1; Figure 6). The weight-on-length relationship (Figure 7) was W= L 3.11,r 2 =.98, where W is weight (g) and L is length (cm). Table 2 gives the mean Fulton s condition (k) values, where k=length weight 3, of cod caught in The Shinneys by length, sampling date, and sex. Mean k for all fish was.88. Reproduction On the basis of observations on the maturity state of females and the presence and stage of development of eggs collected from the water column, spawning begins in The Shinneys within a week or two of the bay becoming ice-free in spring; it lasts for about 3 weeks only. In 1998 most spawning is thought to have been in May, because few ripe females were observed among the 747 fish tagged or sampled in June. In 1999 and 1, Growth rate per year (cm) Age (years) Figure 5. Post-tagging growth rate of age-determined Atlantic cod recaptured in The Shinneys at least one winter after they were tagged. The von Bertalanffy growth curve was plotted from data in Figure 4. spawning had commenced by the last week in May (Figure 8) and had peaked by the end of the first week in June. In contrast, spawning was approximately 2 weeks later in, when the delayed retreat of the ice also delayed sampling. Most cod captured during the first sampling period of each year, with the exception of 1998 as mentioned above, were ripe, releasing milt or eggs when pressure was placed on the abdomen. Among ripe fish, males outnumbered (74.7%) females. Males as small as 32 cm released milt, and females as small as 36 cm released eggs, and 81% (133) of those fish that did not release eggs or sperm were <4 cm long. To confirm the size at sexual maturity determined by stripping fish, 74 cod caught during early June that did not release eggs or milt were selected, based on their length, for macroscopic examination of their gonads. Testes of 27 Atlantic cod ranging in length from 24 to 52 cm were examined. The smallest mature male was 31 cm, and the largest immature male was 35.5 cm. Males reached sexual maturity between 4 and 6 years of age. Ovaries of 47 females ranging in length from 28.8 to 61.3 cm were examined. The smallest mature female was 31.4 cm TL and the largest immature female was 42.1 cm TL. Females matured at 4 8 years of age. Some females were suspected on macroscopic examination of their gonads of being skip-spawners. Of 18 such fish
6 Biology of a resident population of cod in southern Labrador Estimated age (years) n = Number of cod n = 594 n = n = Length (cm) Figure 6. Length frequency distributions of Atlantic cod caught by angling in The Shinneys during June of the years ranging in length from 3.8 to 42 cm examined histologically, only one was confirmed as a skip-spawner on the basis of the histological criteria described by Rideout et al. (). During the spawning period, eggs were concentrated 4 7 m deep, none being taken in surface ( 2 m) tows (n=7). Egg concentrations were as high 53.8 eggs m 3. Eggs were taken in both surface and deep tows during
7 672 C. J. Morris and J. M. Green Weight (g) W = L 3.11 r 2 =.98 n = 84 Movement In all, 77% (34 of 44) of cod recaptured by angling in The Shinneys were caught at the site where they were tagged (Table 3). Other tagged fish were recaptured by commercial and recreational fishers near the mouth, or in the main arm, of Gilbert Bay. An index fishery took place between 24 September and 16 October 1998 throughout the main arm of Gilbert Bay, whereas the 1999 and commercial fisheries were limited to the outer part of Gilbert Bay. A total of 67 tags was returned to DFO from commercial fishing in Gilbert Bay between 1998 and. None of the 2453 cod tagged in Gilbert Bay have been reported from elsewhere along the Labrador coast or from offshore Length (cm) Figure 7. Weight length relationship of Atlantic cod (males and females combined) caught in The Shinneys during all sampling, the later part of June, and most then were at an advanced stage of development. Larval and planktonic juvenile Atlantic cod ranging in length from 12 to 51 mm were taken in plankton tows made in early August of all four years sampled. The average catch of larvae per tow for each year (1998 1) was 2.4 (n=37), 1.6 (n=57),.15 (n=44), and 6.5 (n=21) respectively. Stomach contents Atlantic cod in The Shinneys had a wide variety of benthic invertebrates in their stomachs (Figure 9). Fish, sticklebacks (Gasterosteus aculeatus), gunnels (Pholis spp.), radiated shannies (Ulvaria subbifurcata), and sculpins (Myxocephalus scorpius), constituted a small percentage of the food items. Individual cod tended to have a small number of different types of food item in their stomach. On average, 1.7 food types were found in cod stomachs from The Shinneys, suggesting that cod there specialized on certain prey. Cod from other parts of the bay on average had 2.4 different food items in their stomachs, brittle stars, spider crabs, and shrimp being the most frequently encountered food items. Stomachs were generally half-filled, and no cod sampled had distended stomachs. There was no significant difference (χ 2 =3.64, d.f.=1, α=.5) between ripe and unripe Atlantic cod of either sex in the percentage of empty stomachs. On average, % of stomachs were empty. As all samples were collected by angling, cod were actively pursuing a potential food item at the time of capture. Discussion To our knowledge, Gilbert Bay has the only resident population of Atlantic cod along the Labrador coast. The only other bay- or lake-resident cod population so far described in the western Atlantic is that in Ogac Lake, Baffin Island (62 52 N W; Patriquin, 1967). Ogac Lake is a meriomictic lake covering 14.8 km 2 which is only seasonally connected to Frobisher Bay across a narrow, shallow sill. While Ogac Lake is isolated from Frobisher Bay for most of the year, and may have been completely isolated, Gilbert Bay continuously exchanges water with the Labrador Sea and Alexis Bay, permitting the unimpeded movement of fish throughout the year. Moreover, Gilbert Bay is unlikely ever to have been completely isolated. It is years old (Clark and Fitzhugh, 1992), so its cod population has probably become genetically and behaviourally differentiated from contiguous cod populations within that period. Although seawater flow into and out of Gilbert Bay is much less restricted than in Ogac Lake, shallow sills, coupled with its large inflow of freshwater during spring, likely provide conditions in the inner portions of the bay for retention of cod eggs and early stage larvae. No cod eggs were collected in near-surface plankton tows in The Shinneys during the spawning season, but they were abundant at depths of 4 7 m. Whether it is their distribution at a depth where water exchange with the Labrador Sea is reduced by sills in the bay and/or other hydrographic conditions, some mechanism(s) retains non-motile and weakly motile spawning products in the bay, as evidenced by our sequential sampling of spawners, eggs, larvae, and pelagic juveniles in The Shinneys. Such conditions are not unique to Gilbert Bay; there are numerous examples of local stocks of marine fish (Sinclair, 1988). For example, Westerberg (1994) described how cod eggs become concentrated at the halocline between brackish surface water and more dense saline Baltic water in Oresund Sound. These eggs
8 Biology of a resident population of cod in southern Labrador 673 Table 2. Mean Fulton s condition factors, k, for Atlantic cod caught by angling in The Shinneys, Gilbert Bay, Labrador, in 1998 and Data for males and females are combined except for the May June samples in cm 3 cm 3 4 cm 4 5 cm 5 6 cm >6 cm n Mean s.d. n Mean s.d. n Mean s.d. n Mean s.d. n Mean s.d. n Mean s.d. Sampling date (and sex) 1 1 June June July 6 August May 1 June May 1999 (males) May 1999 (females) August are only transported to the Baltic from the sound during several short outflow periods, when the depth of the halocline decreases. Local adaptation of Gilbert Bay cod is inferred from genetic data (Beacham et al., 1999, ; Ruzzante et al., ) and tracking studies (Green and Wroblewski, ), and the present study identified a number of life history characteristics apparently shaped by the local environment. These include growth, feeding habits, movement patterns, and the timing and duration of spawning. Growth of Gilbert Bay cod is slower than that of Atlantic cod off southern Labrador (NAFO division 2J), and more similar to, but still less than, Atlantic cod farther north (NAFO divisions 2G and 2H; May, 1966). Cod from NAFO division 2J are approximately 47 cm long during their 5th year (May, 1966; Lilly et al., 1999). Of the May-sampled cod in Gilbert Bay, 5- and 6-yearolds were on average 34 and 37 cm long respectively. Age 5 Atlantic cod from Ogac Lake, Baffin Island (the most northern Atlantic cod population in Canadian waters), range in length from 27 to 65 cm (Patriquin, 1966). As female cod in NAFO division 2J mature between 5 and 6 years of age (Lilly et al., 1999) and historically only half the females mature by the age of 6.5 years (May, 1966), these differences in growth are unlikely the result of differences in the onset of sexual maturation and reproduction. Cod aged 1 years caught in division 2J during 1991 bottom-trawl surveys were 65.5 cm long, much smaller than the average 1-year-old Atlantic cod (Lilly et al., 1999). Even so, they were considerably bigger than cod of the same age in Gilbert Bay, which had an average length of 47 cm. On the other hand, age 1 cod from Ogac Lake, Baffin Island, ranged from 4 to 11 cm long (Patriquin, 1966). Variations in length-at-age of Gilbert Bay cod are similar to those of northern cod in NAFO divisions 2J, 3K, and 3L (Lilly et al., 1999). However, the ages of few cod >65 cm TL were determined, so the variation in size-atage, particularly in older fish, may be greater than indicated. The relatively slow growth of Gilbert Bay cod may be partially attributable to low water temperature (< C for approximately 6 months). However, most of Gilbert Bay is shallow, and summer water temperatures can be relatively high. For example, surface water temperatures in August are similar to surface ( 5 m) temperatures in Placentia Bay (Bradbury et al., 1999), along the south coast of Newfoundland. Nearly all our sampling was in this depth range, so Gilbert Bay cod can, and many do, inhabit relatively warm (>7 C) water during summer and autumn. Even cod >7 cm long were caught in <3 m of water, where the water temperature was >1 C. Consequently, factors other than water temperature are likely involved in the relatively slow growth of Gilbert Bay cod.
9 674 C. J. Morris and J. M. Green May Jun % of eggs sampled Jun May Jun Egg development stage Figure 8. Frequency of occurrence of the four developmental stages of Atlantic cod eggs (see text for explanation) taken in 15-min plankton tows in spring, , in The Shinneys. A total of 3 eggs was staged from each sample. Food availability is likely the most important other factor affecting their growth. Although a wide range of food items was found in stomachs, it was rare to catch individuals with full stomachs, and no stomach was distended. Although this may partially reflect the method of capture (angling), it probably indicates an overall low abundance of food. Also, although a wide range of food items was being consumed, individual cod had a relatively small number of taxa in their stomach, indicating that they were targeting a few prey types at a given time. Often, cod caught at the same site, and of the same size, were targeting different prey. Fish made a conspicuously small contribution to the diet. Resident fish such as stichaeids, pholids, gasterosteids, and cottids were found in stomachs, but their frequency of occurrence was low. On the other hand, migratory prey species such as capelin (Mallotus villosus), herring (Clupea harengus), and sandlance (Ammodytes sp.), important food of northern cod in other areas (de Graaf et al., 198; Lilly and Rice, 1983), were absent from the stomachs examined. These forage species were not observed in the inner parts of Gilbert Bay during the study, although local fishers report that they are occasionally present during summer, particularly near the mouth of the bay. Their absence from the bay during the present study may not therefore be a regular occurrence, and could have a significant effect on feeding behaviour and growth. The fish sampled from the food fishery in the main arm of Gilbert Bay in 1998 were significantly longer-at-age than fish caught in The Shinneys. This may indicate that they had more food available to them than fish farther inside the bay, particularly because (a) Brittle Stars 14% Hermit Crab 11% (b) Bivalves 5% Spider Crab 1% Scallop adductor muscle 17% Brittle Stars 12% Hermit Crab 1% Spider Crab 16% Gastropods 6% Polychaetes 9% Sea Cucumber 2% Amphipods 16% Fish 6% Sea Urchins 2% Shrimp and Mysids 19% Scallop gonad 9% Shrimp and Mysids % Scallop shell piece 1% Polychaetes 1% Sea Cucumber 2% Amphipods Fish 3% 7% Sea Urchins 2% Figure 9. Occurrence of major food types in 167 Atlantic cod stomachs sampled in (a) The Shinneys in 1998, and (b) in 62 Atlantic cod stomachs sampled in the main arm of Gilbert Bay in 1998.
10 Biology of a resident population of cod in southern Labrador 675 Table 3. Recapture location and growth of Atlantic cod tagged with Floy t-bar tags in The Shinneys, Gilbert Bay, Labrador, Age at recapture (years) Days between capture Initial length (cm) Increase in length (cm) Growth rate per year Distance from tagging location (km) * * *Inaccurate length recorded, so no growth rate determined. Fish recaptured in same season as initially tagged and released; no age or growth data were determined. summer water temperature tends to be lower near the mouth of the bay. In Ogac Lake, Patriquin (1967) found that some cod were cannibalistic, and that it was these which showed the fastest growth rates and largest size. In and 1 we caught a few large (>7 cm) cod with cod in their stomachs. These fish were indeed longer than predicted from their age when based on our length-atage data. However, more data are needed before it can be stated that cannibalism is a strategy that some Gilbert Bay cod use to outgrow their age cohort, as seems to be the case in Ogac Lake. Interestingly, a significant number of cod sampled in the main arm of the bay had scallop adductor muscles as
11 676 C. J. Morris and J. M. Green well as other scallop parts in their stomachs. An active scallop fishery is currently conducted in Gilbert Bay, and it appears that cod feed on offal thrown from the vessels as well as on scallops damaged by dredges. Local fishers report that cod follow the scallop draggers, and the current stomach analyses suggest that this might be true. If so, it might be further evidence of a low availability of food generally. If forage fish do enter the mouth of the bay during summer and autumn, cod from the inner parts of the bay might be expected to move there to feed. Sonic tracking by Green and Wroblewski () confirmed such movements. About half the fish they implanted with sonic transmitters in The Shinneys moved to the lower half of the main arm of the bay during summer, then returned to The Shinneys by autumn. In the present study, cod in The Shinneys were tagged with Floy t-bar tags. The majority of recaptures in The Shinneys of fish that had been at large for at least one winter were made at the site of tagging. As tagging sites were not far from each other, these recaptures indicate a strong level of site fidelity and/or a return to these sites after excursions from them. Green and Wroblewski () also observed that sonically tagged fish that did not leave The Shinneys showed strong site fidelity, either staying in a small home range or returning to it after excursions to other sites. Also, fish which they displaced homed to the capture site even when this involved swimming through a shallow (<1 m deep) channel. Tags returned from the commercial and food fisheries restricted to the main arm or the outer part of the main arm of Gilbert Bay confirmed the pattern of movement observed in sonically tagged fish. It is therefore possible, and even likely, that some of the fish recaptured at their tagging site in The Shinneys moved as far as the mouth of Gilbert Bay between tagging and recapture. Others probably moved very little. Although tagged fish as small as 35 cm move out of The Shinneys during summer, more larger fish leave, as evidenced by the fewer larger fish in angling catches in The Shinneys in August compared with June (Morris, ). The return of fish to The Shinneys during late summer and autumn means that they overwinter in the same area of the bay where they spawn shortly after ice retreats from the bay the following spring. In this respect they differ from cod in Ogac Lake, which spawn while the lake is still ice-covered (Patriquin, 1967). Gilbert Bay cod have a much shorter spawning season than the two or three months reported for other northern Atlantic cod (May, 1966; Templeman, 1981; Myers et al., 1993; Smedbol and Wroblewski, 1997), with spawning lasting less than a month, from mid- to late May to early or mid-june. Skewed sex ratios in spawning shoals of Atlantic cod have been reported in a number of previous studies on Atlantic cod (see Morgan and Trippel, 1996). It is not clear, though, whether the higher percentage of males in our early June samples represents a difference in the abundance and/or distribution of males and females, or simply a greater tendency for males to be caught by angling. Ripe females were, however, caught by angling and were as likely to have food in their stomachs as males. For northern cod in general, spawning occurs first in more northern areas and progressively later southwards (Templeman, 1981; Myers et al., 1993). Along the Labrador coast, most spawning is in March and April (May, 1966). The timing of spawning in Gilbert Bay and offshore therefore does not coincide. This difference in the timing of spawning is one of the mechanisms that reproductively isolates Gilbert Bay cod and is likely the result of local adaptation to those conditions that allow for the retention of spawning products and adequate conditions for survival and growth of early stage larvae. The water column is only briefly highly stratified at the time of spawning and egg development, perhaps providing a narrow time-window for spawning and early development of larvae. The proximal cues used by Gilbert Bay cod to spawn within this narrow window are not known, but the process seems to be finely controlled. The current age structure of Gilbert Bay cod indicates that most fish were born just before or after the closure of the northern cod fishery in Most of the fish sampled were between 35 and 6 cm long, and few were older than 1 years. Given that cod can live to + years, and that there had been an active commercial fishery in the bay for more than 1 years (Wroblewski, 1998), it seems likely that this population was depressed prior to the 1992 fishing moratorium introduced by the Canadian Government. If this statement is correct, the Gilbert Bay cod population, unlike other northern cod, rebuilt following the moratorium. The few three-year-olds caught in 1998 relative to 1999 indicates that the 1996 year-class was stronger than that of It was also stronger than the 1997 yearclass, based on the larger number of two-year-olds caught in 1998 relative to If these inferences are correct, it is an indication that year-class strength in Gilbert Bay is, as elsewhere, highly variable. Also, a strong 1996 year-class in Gilbert Bay is interesting in that surveys from other areas suggest that the 1996 year-class of northern cod was poor (Lilly et al., 1999), further indicating a disassociation between those factors influencing year-class strength in northern cod and those in Gilbert Bay. Given our lack of understanding about mechanisms influencing year-class strength in Atlantic cod, and the relative ease of sampling and monitoring year-classes from the egg through to sexual maturation in Gilbert Bay, the bay appears to be an ideal place to study the interplay between biotic and abiotic factors in determining recruitment. Regardless, the small population size, genetic distinctiveness, and local adaptations exhibited
12 Biology of a resident population of cod in southern Labrador 677 by Atlantic cod in Gilbert Bay all emphasize the need for special management considerations if this population is to be maintained for food, recreation, or further research. If it is managed as a component of northern cod, as is currently the case, its future may be threatened. Acknowledgements We thank George Rowe for assistance in the field, J. S. Wroblewski, J. Brattey, and P. Pepin for the loan of equipment, and D. H. Steele, R. L. Tilney, and an anonymous reviewer for valuable comments on the paper. Field facilities in Gilbert Bay were provided by the Canadian Department of Fisheries and Oceans. We remember the kindness extended to us by Margery Rowe in Port Hope Simpson. Financial support was provided by the Canadian Centre for Fisheries Innovation in partnership with the Labrador Fishermen s Union Shrimp Company, the Canadian Department of Fisheries and Oceans (B. Atkinson), the Marine Protected Areas Program of DFO, the Labrador Metis Nation, Memorial University, and an NSERC operating grant to J.M.G. References Beacham, T. D., Brattey, J., Miller, K. M., Le, K. D., Schulze, A. D., and Withler, R. E.. Population structure of Atlantic cod (Gadus morhua) in the Newfoundland and Labrador area determined from genetic variation. Canadian Stock Assessment Secretariat Research Document, /99. Beacham, T. D., Brattey, J., Miller, K. M., Le, K. D., and Withler, R. E Population structure of Atlantic cod (Gadus morhua) in the Newfoundland and Labrador area based on microsatellite variation. Canadian Stock Assessment Secretariat Research Document, 99/35. Bradbury, I. R., Snelgrove, R. V. R., and Fraser, S Transport and development of cod eggs and larvae in Placentia Bay (3Ps) Newfoundland, Department of Fisheries and Oceans, Atlantic Fisheries Research Document, 99/ pp. Clark, P. U., and Fitzhugh, W. W Postglacial relative sea level history of the Labrador coast and interpretation of the archaeological record. In Paleoshores Lives and Prehistory: an Investigation on Method, pp Ed. by L. L. Johnson and M. Straight. CRC Press, London. 243 pp. degraaf, D. A., Chaput, G. J., Sandman, M. R., and Buchanan, R. A Offshore Labrador biological studies, The food habits of cod (Gadus morhua) and turbot (Reinhardtius hippoglossoides) along the Labrador coast, summer Unpublished Report by Atlantic Biological Service Ltd for Total Eastcan Explorations Ltd. 17 pp. Green, J. M., and Wroblewski, J. S.. Movement patterns of Atlantic cod in Gilbert Bay, Labrador: evidence for bay residency and spawning site fidelity. Journal of the Marine Biological Association of the United Kingdom, 8: Lear, W. H Discrimination of the stock complex of Atlantic cod (Gadus morhua) off southern Labrador and eastern Newfoundland, as inferred from tagging studies. Journal of Northwest Atlantic Fishery Science, 5: Lear, W. H., and Green, J. M Migration of the northern Atlantic cod and the mechanisms involved. In Mechanisms of Migration in Fishes, pp Ed. by J. D. McCleave, G. P. Arnold, J. J. Dodson, and W. H. Neill. Plenum Press, New York. 574 pp. Lilly, G. R Observations on cod in the inshore environment of eastern Newfoundland. North Atlantic Fishery Organization Science Council Report. Document 96/59, Serial No. N pp. Lilly, G. R., and Rice, J. C Food of Atlantic cod (Gadus morhua) on the northern Grand Bank in spring. North Atlantic Fishery Organization Science Council Report. Document 83/87, Serial No. N pp. Lilly, G. R., Shelton, P. A., Brattey, J., Cadigan, N. G., Murphy, E. F., and Stransbury, D. E An assessment of the cod stock in NAFO division 2J+3KL. Canadian Stock Assessment Secretariat Research Document, 99/ pp. Markel, D., and Frost, L. A Comparative morphology, seasonality and a key to planktonic fish eggs from the Nova Scotian shelf. Canadian Journal of Zoology, 63: May, A. W Biology and fishery of Atlantic cod (Gadus morhua morhua L.) from Labrador. Masters thesis, Memorial University, Newfoundland. 212 pp. Morgan, M. J., and Trippel, E. A Skewed sex ratios in spawning shoals of Atlantic cod (Gadus morhua). ICES Journal of Marine Science, 53: Morris, C. J.. Biology of a resident cod (Gadus morhua) population in Gilbert Bay, Labrador. Masters thesis, Memorial University of Newfoundland. 95 pp. Morrison, C Histology of the Atlantic cod, Gadus morhua: an atlas. 3. Reproductive tract. Canadian Special Publication in Fisheries and Aquatic Sciences, pp. Myers, R. A., Mertz, G., and Bishop, C. A Cod spawning in relation to physical and biological cycles of the northern Northwest Atlantic. Fisheries Oceanography, 2: Patriquin, D. G The biology of a relict population of Atlantic cod, Gadus morhua L. in Ogac Lake, Baffin Island, NWT. M.Sc. thesis, McGill University. 66 pp. Patriquin, D. G Biology of Gadus morhua in Ogac Lake, a landlocked fjord on Baffin Island. Journal of the Fisheries Research Board of Canada, 24: Pepin, P., Orr, D. C., and Anderson, J. T Time to hatch and larval size in relation to temperature and egg size in Atlantic cod (Gadus morhua). Canadian Journal of Fisheries and Aquatic Sciences, 54 (Supplement 1): 2 1. Rideout, R. M., Burton, M. P. M., and Rose, G. A.. Observations on mass atresia and skipped spawning in northern Atlantic cod, from Smith Sound, Newfoundland. Journal of Fish Biology, 57: Ruzzante, D. E., Taggart, C. T., and Cook, D A review of the evidence for genetic structure of cod (Gadus morhua) populations in the NW Atlantic and population affinities of larval cod off Newfoundland and the Gulf of St Lawrence. Fisheries Research, 43: Ruzzante, D. E., Taggart, C. 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13 678 C. J. Morris and J. M. Green Shelton, P. A., and Healy, B. P Should depensation be dismissed as a possible explanation for the lack of recovery of the northern cod (Gadus morhua) stock? Canadian Journal of Fisheries and Aquatic Sciences, 56: Sinclair, M Marine populations: an essay on population regulation and speciation. University of Washington Press. 26 pp. Smedbol, R. K., and Stephenson, R. 1. The importance of managing within-species diversity in cod and herring fisheries of the north-western Atlantic. Journal of Fish Biology, 59 (Supplement A): Smedbol, R. K., and Wroblewski, J. S Evidence for inshore spawning of northern Atlantic cod (Gadus morhua)in Trinity Bay, Newfoundland, Canadian Journal of Fisheries and Aquatic Sciences, 54 (Supplement 1): Templeman, W Canadian research report A. Subareas 2 and 3. International Commission for the Northwest Atlantic Fisheries. Redbook, Part II: 3. Templeman, W Migration and intermingling of stocks of Atlantic cod, Gadus morhua, of the Newfoundland and adjacent areas from tagging in International Commission for the Northwest Atlantic Fisheries Research Bulletin, 14: 6 5. Templeman, W Vertebral numbers in Atlantic cod, Gadus morhua, of the Newfoundland and adjacent areas, , and their use for delineating cod stocks. Journal of Northwest Atlantic Fishery Science, 2: Thompson, H A biological and economic study of cod (Gadus callarius L.) in the Newfoundland area including Labrador. Newfoundland Department of Natural Resources Research Bulletin, 14: 16. Wells, R The determination of the ages of cod from otoliths collected in NAFO Divisions 2J, 3K and 3L. Northwest Atlantic Fisheries Organization Scientific Council Report Document 8/IX/156, Serial No. N pp. Westerberg, H The transport of cod eggs and larvae through Oresund. ICES CM 1994/Q: 4. Wroblewski, J. S Substocks of northern cod and localized fisheries in Trinity Bay, eastern Newfoundland and in Gilbert Bay, southern Labrador. In Implications of Localized Fishery Stocks, pp Ed. by I. Hunt von Herbing, I. Kornfield, M. Tupper, and J. Wilson. NRAES, Ithaca, New York. pp.
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