Seasonal Variations in the Smolt Characteristics of

Seasonal Variations in the Smolt Characteristics of Juvenile Atlantic Salmon (Salmo salar) from Estuarine and Riverine Environments Can. J. Fish. Aquat. Sci. Downloaded from www.nrcresearchpress.com by Renmin University of China on 06/04/13 For personal use only.

R. A. Cunjak Department of Fisheries and Oceans, Science Branch, Culf Region, P.O. Box 5030, Moncton, N.B. E 7C 9B6 Canada

and R. L. Saunders Department of Fisheries and Oceans, Biological Station, Scotia-Fundy Region, St. Andrews, N.B. EOG 2x0 Canada

and E. M. P. Chadwick Department of Fisheries and Oceans, Science Branch, Culf Region, P.O. Box 5030, Moncton, N.B. E7C 986 Canada

Cunjak, R. A., R. L. Saunders, and E. M. P. Chadwick. 1990. Seasonal variations in the smolt characteristics of juvenile Atlantic salmon (Salmo salar) from estuarine and riverine environments. Can. J. Fish. Aquat. Sci. 47: 81 3-820. Smolt characteristics such as lipid-moisture dynamics, ATPase activity, salinity tolerance, and condition factor were determined for Atlantic salmon parr (Salmo salar) moving to, or residing in, estuaries of two rivers in eastern Canada. Lipid and water content and gill Na+K+--ATPaseactivity of these parr differed markedly from riverresident parr. ATPase activity, sex ratio, and condition factor indicated more similarity between estuarine parr and smolts. Estuarine parr were unable to tolerate high salinities in spring, summer, or autumn, but there was an indication of an autumnal increase in salinity tolerance which coincided with maximum levels in ATPase activity and a secondary downstream movement of parr and smolt-like salmon i n the autumn. The data suggest that the largest estuarine parr are essentially presmolts which utilize the estuary as a rearing environment prior to subsequent emigration seaward when environmental conditions are again amenable to a reopening of the 'smolt window.' These observations also highlight some inadequacies i n applying existing criteria for the smolting process and for modelling life histories of salmonids. Nous avons etudie certaines caracteristiques des smolts comme le metabolisme des lipides et de I'eau, I'activite de I'ATPase, la tolerance i la salinite et le coefficient de condition chez des tacons du saumon de I'Atlantique (Salmo salar) migrant vers les estuaires de deux rivi6res de l'est du Canada ou y residant. Ces tacons et les tacons vivant en rivi6re ont des contenus en eau et en lipides nettement differents. I1 en va de meme de I'activite de la Na+K+-ATPase au niveau des branchies. L'activite de I'ATPase, le rapport des sexes et le coefficient de conditon etaient davantage similaires chez les tacons estuariens et les smolts. Les tacons estuariens ne pouvaient tolerer les fortes salinites au printemps, i I ' M ou i I'automne mais cette tolerance semblait plus grande a I'automne, periode oG les taux d'activite de I'ATPase 6taient les plus eleves et oG il y a eu une deuxi6me migration vers I'aval de tacons et de saumons montrant des caracteristiques de smolts. Nos donnees laissent entendre que les plus gros tacons estuariens sont en fait des saumons au stade presmolt qui viennent poursuivre leur croissance dans I'estuaire avant de se diriger vers la mer quand les conditions environnementales redeviennent favorables au passage des smolts dans la mer. Ces observations mettent egalement en evidence certaines inexactitudes dans les crit6res utilises pour decrire la smoltification et modeliser le cycle vital des salmonides. Received August 9, 7 989 Accepted November 2 7, 7989

R e ~ le u 9 aoljt 7 989 Accept6 le 2 7 novembre 7 989

(JA2 71)

C

unjak et al. (1989) documented the downstream movements and subsequent estuarine residence of Atlantic salmon (Salmo salar) parr in a river, Western Arm Brook, in northwestern Newfoundland. Their study showed that whereas smolts emigrated within days of entering brackish water, parr, which also entered the estuary, were present throughout the summer and autumn. Further, there was evidence to suggest that the largest parr in the estuary moved seaward, either in the late spring (coincident with, or soon after, downstream migration) or in the autumn together with a secondary downstream movement of parr and smolt-like salmon. If this is the case, then we should expect to find physiological evidence as well as general biological characteristics to support Can. J. Fish. Aquat. Sci., Vol. 47, 1990

our contention that these (i.e. the largest) parr are essentially presmolts which move seaward in the same year that they enter the estuary. Thus, our objective was to determine whether Atlantic salmon parr moving towards, or residing in, estuaries displayed smolt-like characteristics by comparing them with 'true' smolts and riverine parr. Because salinity tolerance and par-smolt transformation are seasonal phenomena (Johnston and Saunders 1981; Langdon and Thorpe 1985; Saunders et al. 1990), a secondary objective was to document any seasonal changes in physiological parameters among the different groups of salmon. A variety of tests and parameters have been used as indicators of smolt status in salmonids (see reviews by Hoar 1976; Folmar 813

Can. J. Fish. Aquat. Sci. Downloaded from www.nrcresearchpress.com by Renmin University of China on 06/04/13 For personal use only.

and Dickhoff 1980; Wedemeyer et al. 1980; McCormick and Saunders 1987). Specifically, we chose to study gill Na+K+ATPase activity and lipid-moisture content (Farmer et al. 1978; Saunders and Henderson 1978; Johnston and Saunders 1981; Langdon and Thorpe 1985) as evidence of physiological changes associated with smolting, and salinity-tolerance tests (Saunders et al. 1985) as a test of the ability to tolerate full strength seawater. Condition factor, sex ratio, and maturity were also determined because these factors, in association with the preceding parameters, can be used as general indicators of smolt status (Saunders and Henderson 1970; Farmer et al. 1978; Eriksson et al. 1987; Rodgers et al. 1987).

Materials and Methods Two river systems were studied, Western Arm Brook (WAB) and South River (SR). WAB is a fourth-order river in Newfoundland (5 1'1 1'N, 56'46'W) with a drainage basin of 150 km2. A fish-counting fence, located near the mouth of the river has been operated (May-October) since 1971. The sampling regimen for the collection of biological data on all salmon and other species moving through the fence was outlined in Chadwick et al. (1985). The estuary of WAB is a shallow delta (total area = 65 ha) with an average summer tidal fluctuation of 1.11.4 m. Mean salinities in the estuary ranged from 1-24%0 during our study; water temperature seldom reaches 20°C. A more detailed description of the estuary and sampling locations was given by Cunjak et al. (1989). SR is a fourth-order river located in Nova Scotia (45"36'N, 61°55'W) which drains an area of approximately 200 km2. A fish counting fence, located approximately 2 krn above the head of tide has been used to monitor upstream and downstream movements of fishes (Chadwick et al. 1985) from spring to autumn, 1981-87. The SR estuary (79 ha) forms the southern portion of a large lagoon (Antigonish Harbour), which experiences maximum summer temperatures 225°C during July and August. Salinities measured during 1987 ranged from 0 to l9%0 depending on the tide and location within the estuary. Atlantic salmon were separated into one of four groups for comparison: smolts (or smolt-like salmon), based on phenotypic characteristics (silvery body colour, absence of parr marks, darkened fins, and streamlined body shape, see Wedemeyer et al. 1980), and captured at the counting fence during their downstream movement; 'migrant' parr, which were clearly distinguished from smolts (Cunjak et al. 1989) and also captured at the counting fence during their downstream movement (WAB only); 'riverine' parr, collected by electrofishing, 0.20.5 km upstream of the counting fences of both rivers and assumed to represent river-resident salmon parr; and, 'estuarine' parr (formerly 'migrant' parr), which were seined from brackish water sites. At SR, estuarine parr were collected exclusively from a single site in the upper estuary (salinity = &5 .O) where salmon parr were most abundant (R. A. Cunjak, unpubl. data). Estuarine parr from WAB were collected from any of four sites throughout the estuary, although most (75%) were collected at a site near the head of the estuary (0-14 ppt). At WAB, salmon were collected in both 1987 and 1988, and depending on the date of capture, samples were divided into one of four seasonal categories: spring (late May), late spring (early June, 7-1 2 days after 'spring' collection), summer (August), and autumn (late September). Because downstream movement of parr (i.e. 'migrants') and smolts had essentially

ceased by late June, these two groups of salmon were absent from summer collections. At SR, where sampling was carried out in 1987 only, salmon pan: were rare in the estuary by midsummer (R. A. Cunjak, unpubl. data) and consequently, only spring (18-22 May) and late spring (12 June) collections were made. All the salmon collected for this study were measured (fork length, centimetres), weighed (wet weight, grams) and dissected for determination of sex and stage of maturity. Carcasses were frozen for subsequent determination of lipid and water content. Additional sampling data of parr and smolts (R. A. Cunjak, unpubl . data) from the different locations at WAB (1987 and 1988) and SR (1987) were also included for determinations of condition factor and sex ratio. In the field, gill filaments of salmon were trimmed from gill arches, placed in 1.0 mL of SEI buffer (0.3 M sucrose, 0.02 M disodium ethylenediaminetetraacetate, and 0.1 M imidazole at pH 7.0), and immediately frozen in dry ice until transport to the laboratory and storage at - 80°C. Gill Na+K+-ATPase activity was determined according to the method of Zaugg (1982a) and incorporating the modifications of McCormick et al. (1987). Enzyme activity was expressed as p,moles inorganic phosphate per milligram protein per hour (p,M PO,-mg protein- '.h- I ) . Whole frozen salmon were freeze-dried in a lyophilizer for 48 h at - 75°C and reweighed to calculate water content. Lipid content was determined, in duplicate, from samples of whole fish that had been homogenized and freeze-dried using the methanol:chloroform extraction technique (Bligh and Dyer 1959). Values for lipid and water content were expressed as percentages of the whole wet weight of each fish. Salinity-tolerance tests (Saunders et al. 1985) were conducted at Western Arm Brook during 1988 (spring, summer, and autumn). Ten salmon sampled from a single location (counting fence, river, or estuary) were introduced to an opaque, 91-L polypropylene container of seawater supplemented with 'Instant Ocean,' such that salinity = 37.5. A salinity of 37.5 was chosen to better test osmoregulatory development and to overcome the confounding factor of survival by some (large) parr at normal seawater concentrations (Wedemeyer et al. 1980). Containers were covered, aerated continuously, and set in the river adjacent to the counting fence for the duration of the tests (48 h). Paired comparisons of salinity tolerance were carried out as follows: in spring, migrant parr versus smolts (May 2830), riverine parr versus estuarine pan: (June 1-3); in summer, riverine parr versus estuarine parr (August 18-19); and in autumn, riverine parr versus estuarine parr (September 25-26). For each comparison, fish were matched as closely as possible for size. Containers were checked every 2 h for mortalities which were subsequently removed, measured, weighed, and frozen. Salmon from these tests were not used in the physiological determinations or for the calculation of condition factor. Linear regression was used to assess the relationship of fish size on ATPase activity and on survival time of salmon used in the salinity-tolerance tests. Student's t-tests were used to check for inter-year differences of each of the physiological parameters measured at WAB. ANOVA (or Kruskal Wallis test) was used to test for inter-seasonal differences of the lipid (and water) content and for differences in mean condition factor among the different sampling locations; a posteriori SNK tests were used to identify where significant differences occurred among the class levels. Kolmogorov-Smirnov tests were used to compare Can. J. Fish. Aquat. Sci., Vol. 47, 1990

I

: I-.... 4

e

E

6

6

4

.

WESTERN ULY BROOK

-

1

SYOLYS

A WESTERN ARM BROOK

- SYOLT-LIKE S W O N

8 WESTERN ARM BROOK

-

LU

RIVERWE PARR

WESTERN ARM BROOK - ESTUARINE PARR

0 SOUTH RlYER

SOUTH RIVER

TABLE1. Mean sizes (FL, cm + SD) of different life stages of Atlantic salmon sampled for physiological parameters at various sites at Westem Arm Brook (WAB), Newfoundland (1987 and 1988 data pooled) and South River (SR), Nova Scotia. Values in parentheses are the range of FL measured; dashed values indicate that no sample was collected. Values in square brackets are sample sizes.

- SYOLYS

-

Collection sites

ESTUARINE PARR

Life Location stage


WAB

SR

P

SPrins

lab Spring

Summer

Autumn

SEASON

FIG. 1. Seasonal changes in mean gill Naf Kf -ATPase activity in Atlantic salmon parr and smolts sampled from different locations in the Western Arm Brook and South River systems. Vertical bars represent the standard errors; numbers denote sample sizes.

the distributions of cumulative mortalities for paired comparisons in the salinity tolerance tests.

Results Gill Naf Kf -ATPase activity differed depending on the life stage of the salmon and the site and season of sampling (Fig. 1). No significant inter-year differences (p>0.05) were noted for ATPase activity (WAB) and consequently data from the two years were pooled. Gill ATPase activity was highest for smolts, particularly at the peak of their downstream movements (spring, SR; late spring, WAB) when activity ranged between 4.2-8.0 (SR) and 3.9-8.3 (WAB). Riverine parr from WAB had negligible Na+ K -ATPase activity (0-0.8) regardless of the season (Fig. l); gill tissue for SR riverine parr was not analysed. Mean gill ATPase activity for migrant salmon parr sampled at the counting fence during their downstream movements did not differ significantly (p>0.70) from that of estuarine parr, when they were sampled concurrently in spring and late spring. Therefore, these data were pooled and will be collectively referred to as estuarine parr (Fig. I). However, estuarine parr had significantly higher @70 g) could be transferred directly from freshwater to saltwater cages in November with resultant low mortality (10-20%). These findings may indicate a need to redefine our criteria for smolting with respect to the seasonal relationship between salinity tolerance and physiological parameters. Our results suggest that the "smolt window" may be reopened in the autumn when environmental conditions (e.g. water temperature, daylength) are similar to the spring and that the term "autumn smolt" may be appropriate not only for WAB, but also for other populations of S . salar. The autumnal migration of smolt-like Atlantic salmon has been documented from rivers in North America (Meister 1962; Power 1969; Hutchings 1986) and Europe (Youngson et al. 1983). Reimers (1973) noted the phenomenon for juvenile chinook salmon (Oncorhynchus tshawytscha) residing in the estuary of an Oregon river and Ewing et al. (1980) correlated autumnal peaks (which were lower than spring peaks) in Na+K+-ATPase activity with seawater entry of juvenile chinook salmon. At WAB, phenotypic evidence of smolting in autumn was provided by the recapture of two smolt-like salmon in the estuary in mid-September of 1987 which were previously marked as parr in the estuary in May and August (R. A. Cunjak, unpubl. data); no other recaptures of smolts (bearing marks given when they were identified

as 'estuarine parr') were found on this or previous dates, although parr were abundant. The inability of estuarine parr to survive the salinity-tolerance tests indicated that their osmoregulatory abilities were not fully developed for immediate entry to seawater, unlike the case for most of the smolts. Much of this may be explained by the small size of the parr used in the experiments. The critical size for smolting of Atlantic salmon is considered to be approximately 12 cm FL (Parry 1960; Farmer et al. 1978; Wedemeyer et al. 1980). In our experiments, only two of the 30 estuarine parr were > 12 cm FL, and it was these individuals which had the longest survival times (28 and 40 h). Larger parr were scarce in the estuary, and we hypothesized (R. A. Cunjak et al. 1989) that they emigrated seaward, either in the spring or autumn, after attainment of a critical size for smolting because they continue growing while in the estuary (Power and Shooner 1966; R. A. Cunjak, unpubl. data). McCormick et al. (1985) considered the protracted estuarine residence of brook trout (Salvelinus fontinalis) from Quebec rivers was a means of acclimating to saltwater especially if size and species-specific, osmoregulatory physiology were inadequate to accommodate an immediate entry to the sea. The results of the tests did suggest that salinity tolerance in estuarine parr showed a seasonal trend with best survival occurring in the autumn. This further supports our contention of an autumnal "smolt window" utilized by larger estuarine parr. The estuary, with its variable but intermediate salinites may provide a suitable environment for the development of salinity tolerance. Tschaplinski (1988), in studying the use of the Carnation Creek estuary in British Columbia by coho salmon (Oncorhynchus kisutch), noted an increase in salinity tolerance from May until November when they emigrated seaward. At Western Arm Brook, during the late spring and autumn when we believe seaward movements to be occurring, the lipid content of smolts, and smolt-like salmon, was low and similar to levels of at least some (i.e. larger) of the estuarine parr which we also believe emigrated at these times. Generally, total body lipid content tends to decrease (and water increase) during the pan-smolt transformation presumably due to the accelerated lipid (and protein) catabolism requisite for osmoregulatory adjustment (Blake et al. 1984) prior to entry to the sea. The low lipid levels (and condition factors) measured for estuarine parr in the summer were in contrast with those for riverine parr and did not reflect conditions in the estuarine environment where food is generally abundant (Haedrich and Hall 1976; Simenstad et al. 1982) and where feeding (and growth) rates of salmonids are often high (Power and Shooner 1966; Reimers 1973; Healey 1980; MacDonald et al. 1988). Instead, it appears that the proximate body composition of estuarine parr is indicative of the smolting process. If the hypothesis that smolting inhibits maturation (Thorpe 1982, 1987) is valid because osmoregulation is metabolically too costly to accomodate gonadal development as well, then the absence of any mature parr in the estuaries of WAB and SR (compared with the river) could well be explained on this basis. Assuming that estuarine parr eventually emigrate seaward based on CPUE data (Cunjak et al. 1989) and physiological changes (this study), these salmon provide an interesting data set for the size-bimodality model of Atlantic salmon (Thorpe 1977, 1986). Briefly, the model suggests that the physiological decision regulating growth in parr occurs in the summer preceding smolt emigration. The 'upper mode' (UM) group maintains growth, completes smolting and emigrates the following Can. J. Fish. Aqua?. Sci., Vol. 47, 1990


spring; the 'lower mode' (LM) group arrests growth and remains in the river as parr. If there are several age-classes in the population (as was the case at WAB and SR), then these classes need to be analysed separately for differentiation of modal groups. At both WAB and SR, mean sizes of estuarine parr indicated distinct differences compared with smolts . At WAB , where age-classes of smolts and estuarine parr overlap, smolts were significantly (p