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Larval growth of sprat, Sprattus sprattus phalericus, larvae in the Northern Adriatic
Fisheries Research 36 (1998) 117±126
Larval growth of sprat, Sprattus sprattus phalericus, larvae in the Northern Adriatic Jakov DulcÏicÂ* Institute of Oceanography and Fisheries, P.O.B.500, 21000 Split, Croatia Received 16 October 1997; accepted 14 March 1998
Abstract Sprat larvae collected in the Northern Adriatic (1995 and 1996) were used to estimate larval growth rates. Daily growth increments were counted on sagittal otoliths of 280 larvae (108 in 1995, and 172 in 1996) using transmission optical microscopy. Larval growth was estimated using the Gompertz and Laird±Gompertz growth curves for larvae ranging from 6.5 to 22.6 mm (1995) and from 6.9 to 22.5 mm (1996) in standard length. The largest growth increments were recorded for the 6day-old (0.639 mm dayÿ1) larvae in 1995, and for the 5-day-old larvae in 1996 (0.632 mm dayÿ1). Mean growth rate was 0.421 mm dayÿ1 (SD0.169) in 1995, and 0.409 mm dayÿ1 (SD0.175) in 1996. There was no signi®cant difference (P>0.05) in the rate of growth between years. # 1998 Elsevier Science B.V. All rights reserved. Keywords: Sprattus sprattus phalericus; Larvae; Otoliths; Growth; Northern Adriatic
1. Introduction The sprat, Sprattus sprattus, is a small, mutiple (batch) spawning species with a protracted spawning season and a large number of spawnings per year (Alheit, 1986). In the Adriatic, Sprattus sprattus phalericus is usually found in the areas of the Gulf of Venice, Kvarner, Kvarneric (Northern Adriatic), the Velebit channel as well as in the channels of the middle Dalmatia (TeskeredzÏicÂ, 1983). The sprat represents, after sardine and anchovy, the main pelagic species of the purse-seine catch in the Croatian Adriatic Sea.
*Corresponding author. Tel.: 00385 21 358688; fax: 00385 21 358650; e-mail: [email protected] 0165-7836/98/$19.00 # 1998 Elsevier Science B.V. All rights reserved. PII S0165-7836(98)00108-8
Larval ®sh growth is of particular importance to population dynamics, especially to recruitment and biological models incorporating environmental parameters (Houde, 1987, 1989). Microscopic markings in thin sections of the otoliths of ®shes are evidence of a record of daily growth (Pannella, 1971, 1974) and provide a means to age tropical species for which seasonal and annual growth rings are often hard to interpret. These marks, or microincrements, are produced in larvae of many ®shes (Brothers et al., 1976; ReÂ, 1983, 1986; Jones and Brothers, 1987; Moksness and Wespestad, 1989). Counting otolith microincrements has been useful in estimating growth of larval ®shes (Barkman, 1978; Methot, 1981; Geffen, 1986; Jones, 1986; DulcÏicÂ, 1995). The objective of this study was to analyze and estimate the growth characteristics of sprat larvae
118
J. DulcÏic / Fisheries Research 36 (1998) 117±126
from the North Adriatic for the ®rst time, as inferred from otolith daily growth increments. This should provide the basis for future studies of sprat growth parameters and of the conditions that affect the renewal of this population in the Adriatic Sea. 2. Material and methods Sprat larvae were collected from the North Adriatic by the research vessel `Vila Velebita'. In January (23.01.1995 and 17.01.1996), specimens were collected from the following stations in the North Adriatic: RV 001 ± depth 30 m, SJ 107 ± depth 37 m, SJ 105 ± depth 36 m, SJ 103 ± depth 33 m, SJ 101 ± depth 28 m and SJ 108 ± depth 31 m (Fig. 1). Material was collected by Hensen plankton net (73/ 100) with 0.280 mm mesh size, 5 m above the bottom to surface vertical hauls. The net was towed at a speed
of 0.5 m/s. The mean surface temperature over the surveyed area was 10.80.628C (1995) and 10.50.518C (1996). The planktonic material was preserved in 5% formalin buffered with borax (pH 8.5±9) (ReÂ, 1983). A total of 280 sprat larvae was examined (108 in 1995, and 172 in 1996). Larval standard lengths were measured (the distance along the midline of the body from the tip of the snout to the end of urostyle) with the aid of a binocular microscope to the nearest 0.1 mm by placing the larva on a transparent grid marked in millimeters and illuminated from below. Larval lengths were corrected for shrinkage using the equation proposed by Theilacker (1980) for Engraulis mordax. All larval lengths correspond to standard lengths corrected for shrinkage. Sprat larvae were aged according to daily growth increments in sagittal otoliths. The methods used for obtaining, mounting and observing the sagittae were described by ReÂ, 1983, 1986. Microgrowth increments were counted with the aid of a compound optical microscope using magni®cations of 600 and 1000. Several counts were made for each sagitta, and the number obtained most frequently was chosen. The mean of the counts of both sagittae from each larva was used for data analysis. Otoliths, unsuitable for examination because of unclear microstructure or de®ciency in the preparation, were discarded. All otolith measurements were taken under the microscope using a calibrated micrometer eyepiece. Yolksac larval otoliths were included in the analysis to establish a start of increment formation. Data from the North Adriatic were mathematically and statistically analyzed. The relationship between age and length of larvae was given by the common non-linear growth equations (Kramer and Zweifel, 1970; Regner, 1980). Two equations were used to describe length at age of sprat larvae. The ®rst equation is given by Gompertz (1825): It a exp ÿbeÿct
(1)
where lt is the length of larvae at time t, a the asymptote, and b and c the constants. The second equation is given by Laird et al. (1965): It I0 exp A0 =c 1 ÿ eÿct Fig. 1. Sampling area and station numbers in the Northern Adriatic.
(2)
where l0 is the length of larvae at time t0, A0 the instantaneous growth rate at time t0, and c the same
J. DulcÏic / Fisheries Research 36 (1998) 117±126
constant as in previous equation. Parameters were calculated from the data on age obtained from otolith readings and on length of larvae by an iterative procedure using the STATISTICA program. Daily growth rates were derived from the Gompertz ®t by examining the Lt ÿ Ltÿ1 = Aget ÿ Agetÿ1 values over the range of ages available. 3. Results Sprat larvae ranged from 6.5 to 22.6 mm in standard length (mean length15.704.45 mm, median16.50 mm) in 1995, and from 6.9 to 22.5 mm (mean length15.054.43 mm, median14.60 mm) in 1996. Typical growth increments composed of dark discontinuous and light incremental zones when viewed under a microscope with transmitted light could only be discerned in sagittae belonging to older larvae with functional mouths, pigmented eyes and little or no residual yolk. Results of ring counts are presented in Table 1. Values for the parameters in Gompertz and Laird± Gompertz functions are given in Table 2. Graphical representations of the data ®tted by the Gompertz function are given in Fig. 2. The largest growth increments were recorded for 6day-old (0.639 mm dayÿ1) larvae in 1995, and for 5day-old larvae in 1996 (0.632 mm dayÿ1) (Fig. 3). Mean growth rate was 0.421 mm dayÿ1 (SD0.169) in 1995, and 0.409 mm dayÿ1 (SD0.175) in 1996. In order to compare the rate of growth between two seasons, the Gompertz curves were linearized and examined for homogeneity of slope using the t-test. There was no signi®cant difference at the 0.05 level. There were no signi®cant differences between the radii of left and right sagittae (Wilcoxon test, P>0.05), or between the number of daily growth increments enumerated from left and right sagittae for both the years (Wilcoxon test, P>0.05). The relationships between the number of daily growth increments and otolith radii were ®tted with exponential curves (Fig. 4), and that between larval length and otolith radius with a power±regression curve Y aX b , taking Y as otolith radius and X as larval length (Fig. 5). The parameters of the relationship between otolith radius and larval length were: a0.027, b2.526 (1995); a0.028, b2.541 (1996), indicating a positive allo-
119
Table 1 Number of daily rings and the standard length range of sprat Sprattus sprattus phalericus larvae in 1995 and 1996, in the Northern Adriatic No. of rings (days)
No. of Larvae
Length range (mm)
Mean length (mm)
1995 0 1 2 4 5 8 11 12 14 15 16 17 18 19 20 24 25 26 30 33 37 Total
5 3 4 3 4 4 6 5 3 7 3 10 8 7 11 6 5 3 5 3 3 108
6.5±7.4 7.4 7.4±7.6 7.9±8.0 9.0±10.9 11.5±12.0 13.4±13.9 13.9±14.4 14.8±14.9 14.8±15.3 15.1±15.6 16.2±16.7 16.4±17.6 16.9±18.2 17.8±18.4 19.5±20.4 20.4±20.7 20.8±21.1 21.5±21.6 21.9±22.0 22.0±22.6
7.080.341 7.40 7.480.100 7.930.058 9.580.903 11.850.238 13.720.183 14.160.195 14.870.058 15.070.198 15.400.265 16.370.231 16.980.423 17.610.406 18.130.224 19.920.313 20.500.141 20.970.153 21.520.045 21.930.058 22.370.321
1996 0 2 3 5 6 7 8 10 11 12 15 17 19 20 24 25 27 30 32 37 Total
4 5 5 6 15 6 11 17 8 10 15 11 9 5 14 7 7 7 4 6 172
6.9±8.0 7.2±8.8 7.5±8.9 9.1±11.0 9.9±11.4 10.5±12.0 10.3±12.2 12.2±13.4 13.3±13.9 13.9±14.8 14.6±15.5 15.8±16.9 16.9±17.8 18.0±18.4 19.6±20.4 20.2±20.7 20.0±21.4 21.0±21.6 21.5±21.9 22.0±22.5
7.380.519 7.820.698 8.180.598 9.680.691 10.640.453 11.480.512 11.660.609 12.790.384 13.550.256 14.270.309 15.080.303 16.390.333 17.610.366 18.180.148 19.960.288 20.440.162 20.930.425 21.390.267 21.730.171 22.200.210
metry. The power±regression curves, describing the otolith radius and standard length relationship, do not ®t well for the smallest and largest larvae, despite
J. DulcÏic / Fisheries Research 36 (1998) 117±126
120
Table 2 Estimated values of Gompertz and Laird±Gompertz functions (SE ± standard error).
Gompertz (1995) Gompertz (1996)
Laird±Gompertz (1995) Laird±Gompertz (1996)
a
SE
b
SE
c
SE
r
P
25.92 25.65
0.632 0.742
1.379 1.336
0.0185 0.0137
0.067 0.067
0.0034 0.0045
0.988 0.986
<0.001 <0.001
l0
SE
A0
SE
c
SE
r
P
6.52 6.74
0.203 0.221
0.092 0.089
0.0056 0.0053
0.067 0.067
0.0039 0.0044
0.988 0.986
<0.001 <0.001
Fig. 2. Gompertz model, adjusted to the observed data (1995 and 1996).
J. DulcÏic / Fisheries Research 36 (1998) 117±126
121
Fig. 3. Growth rates in mm dayÿ1 (1995 and 1996).
relatively high values of correlation coef®cients. Otolith size begins to increase relatively fast when larvae reached 20 mm. Data on larvae length and otolith radius indicated at least two periods of change in their growth rates. These periods could be attributed with relative certainty to intrinsic changes which occur during stage-speci®c periods of growth. The changes in growth rates may be described much better by the ®fth-order polynomials with a high degree of probability levels (1995: yÿ56.8139.646xÿ8.547x2 0.844x3ÿ0.038x40.001x5; 1996: yÿ66.068 45.823xÿ9.468x20.964x3ÿ0.043x40.001x5; y otolith radius, xstandard length) (Fig. 6). Sagittal daily growth increments had different widths and were clearly wider close to the border of the otolith in older larvae. The mean width of daily growth increments varied from 0.60 to 2.85 mm (mean1.56 mm, SD0.36) and was greater in larger larvae. The average radius of the ®rst feeding check was 10.48 mm (SD0.69; mean larval length ± 7.4 mm). 4. Discussion Sprat growth and development rates can be determined by analysis of otolith increments, which can be
counted and measured with an optical microscope, since Re and Gonc,alves (1993) found that the smallest increment, in sagittae of Sprattus sprattus sprattus, measured in addition to mean widths of daily increments was clearly above the functional resolution limit of the optical microscopy (the majority of daily growth increments had widths 1 mm), suggesting that unresolved increments (Campana et al., 1987) were not a problem in this study, but con®rmation of the optical microscope counts by a scanning electron microscope is always highly desirable. All published studies indicate that otolith increments are found at different developmental stages but are characteristic of the species being studied. Some species hatch with increments already formed, while others do not form increments until yolk-sac absorption. Alshuth (1988) studied the deposition of microgrowth increments in the sagittae of laboratoryreared sprat larvae. He noted that increments were ®rst observed 6 days after hatching (at a temperature of 158C) at the time of ®rst feeding and complete absorption of the yolk sac, which is in agreement with results in this study. The increments were formed under a daily rhythm for a period of 29 days. Shields (1989) showed that the daily increment-deposition rate was in late-larval and juvenile stages of sprat. The author also
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J. DulcÏic / Fisheries Research 36 (1998) 117±126
Fig. 4. Relationship between the otolith radius and age of the sprat larvae.
observed that multiple feedings per day did not disrupt the daily increment formation, but intermittent feeding altered the appearance of juvenile increments and resulted in sub-daily increment counts. Re and Gonc,alves (1993) con®rmed the daily nature of otolith growth increments using the marginal increment technique described by Re (1987), indicating that at least
larvae with lengths greater than 11.0 mm form daily growth increments in their otoliths. They also suggested that there is some evidence that daily growth increments are deposited on the otoliths of sprat larvae only after the onset of exogenous feeding. Shields (1989) validated the correspondence between number of increments and age in days of sprat larvae. He found
J. DulcÏic / Fisheries Research 36 (1998) 117±126
123
Fig. 5. Relationship between the otolith radius and length of sprat larvae (power±regression curve YaXb).
a one-to-one relationship when increment widths were >1.5 mm. In the present study, increments were mostly >1.5 mm; thus, their number is assumed to re¯ect age in days. The growth rates in this study (0.639 and 0.632 mm dayÿ1) are comparable to those obtained for similar pelagic clupeoid species (Methot and
Kramer, 1979; ReÂ, 1986; Leak and Houde, 1987; DulcÏicÂ, 1995). Shields (1989) found integrated somatic growth rates that varied from 0.37 to 0.49 mm dayÿ1 for sprat, Sprattus sprattus sprattus, larvae in the Irish Sea. Munk (1993) investigated the daily growth of sprat larvae in the eastern North Sea and found signi®cant differences in growth rate of
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J. DulcÏic / Fisheries Research 36 (1998) 117±126
Fig. 6. Relationship between the otolith radius and length of sprat larvae (fifth-order polynomials).
larvae in relation to their distance from a frontal zone, implying that the best conditions for larval growth and survival may be located close to this zone. Growth rate estimates were highest in the mixed water (absolute growth rate of 12 mm larvae: 0.47 mm dayÿ1). At the mixed side of the front, where larval abundance peaked, growth was slightly lower, whereas growth rate declined signi®cantly further offshore (to a minimum of 0.13 mm dayÿ1 for 16 mm larvae). Re and
Gonc,alves (1993) also found integrated somatic growth was 0.406 mm dayÿ1 for sprat larvae in the German Bight (North Sea). The same authors mentioned that there were no signi®cant differences in growth rates found at contrasting sites (strati®ed ± 0.405 mm dayÿ1 and mixed water masses ± 0.369 mm day). Differences in somatic growth could be connected to the in¯uence of temperature and food availability differences in the areas investigated. In
J. DulcÏic / Fisheries Research 36 (1998) 117±126
this study, there was no signi®cant difference in the rate of growth between years since the mean temperatures were similar during the times of larval collections. This result could imply that growth probably was not a main factor controlling the recruitment process. So, in all cases in future, when the data on age of larvae are needed, the growth parameters should be estimated to every particular survey since there is a great possibility that environment conditions will be different from one year to the next. The in¯uence of primary production on larval growth rate is mediated through its effect on secondary production and zooplankton abundance. In this context, it is not so much the total zooplankton biomass, but the size fraction that larvae are capable of eating that is important. Therefore, further studies on zooplankton concentration and its particle-size distribution, as well as on hydrographical parameters in the Northern Adriatic, are needed since they could determine growth rate and condition of larvae. Acknowledgements The author thanks colleagues, Mr. V. TicÏina and crew of the research vessel `Vila Velebita', for their great help in collecting material. He also offers special thanks to the two anonymous reviewers for their useful comments on the manuscript. References Alheit, J., 1986. Reproductive biology of sprat, Sprattus sprattus: Factors determining annual egg production. Comm. Meet. Int. Coun. Explor. Sea C.M.-ICES/H, 58, p. 16. Alshuth, S., 1988. Daily growth increments on otoliths of laboratory-reared sprat, Sprattus sprattus L. larvae. Meeresforsch. 32, 23±29. Barkman, R.C., 1978. The use otolith growth rings to age young Atlantic sliversides, Menidia menidia. Trans. Am. Fish. Soc. 197, 790±792. Brothers, E.B., Mathews, C.P., Lasker, R., 1976. Daily growth increments in otoliths from larval and adult fishes. Fish. Bull. US 74, 1±8. Campana, S.E., GagneÂ, J.R., Munro, J., 1987. Otolith microstructure of larval herring (Clupea harengus): image or reality?. Can. J. Fish. Aquat. Sci. 42, 1922±1929. DulcÏicÂ, J., 1995. Estimation of age and growth of sardine, Sardina pilchardus (Walbaum, 1792), larvae by reading daily otolith increments. Fish. Res. 22, 265±277. Geffen, A.J., 1986. The growth of herring larvae, Clupea harengus
125
L., in the Clyde: An assessment of the suitability of otolith ageing methods. J. Fish. Biol. 28, 279±288. Gompertz, B., 1825. On the nature of the function expressive of the law of human mortality, and on the mode of determining the value of live contingencies, Phil. Trans. Roy. Soc. Lond. 115, pp. 531±585. Houde, E.D., 1987. Fish early life dynamics and recruitment variability. Am. Fish. Soc. Symp. 2, 17±29. Houde, E.D., 1989. Comparative growth, mortality and energetics of marine fish larvae: Temperature and implied latitudinal effects. Fish. Bull. US 87, 471±495. Jones, C., 1986. Determining age of larval with the otolith increment technique. Fish. Bull. 84, 91±103. Jones, C., Brothers, E.B., 1987. Validation of the otolith increment ageing technique for striped bass, Morone saxatilis, larvae reared under suboptimal feeding conditions. Fish. Bull. 85, 171±178. Kramer, D., Zweifel, J.R., 1970. Growth of anchovy larvae (Engraulis mordax Girard) in the laboratory as influenced by temperature. Calif. Coop. Oceanic Fish. Invest. Rep. 14, 84±87. Laird, A., Tyler, S.A., Barton, A.D., 1965. Dynamics of normal growth. Growth 29, 233±248. Leak, J.C., Houde, E.D., 1987. Cohort growth and survival of bay anchovy, Anchoa mitchilli, larvae in Biscayne Bay. Florida. Mar. Ecol. Prog. Ser. 37, 109±122. Methot, R.D., , Jr.1981. Spatial covariation of daily growth rates of larval northern anchovy, Engraulis mordax, and northern lampfish, Stenobrachius leucopsarus. Rapp. P.-v. ReÂun. Cons. int. Explor. Mer. 178, 424±431. Methot, R.E., Kramer, D., 1979. Growth of northern anchovy Engraulis encrasicholus larvae in the sea. Fish. Bull. 77, 413± 423. Munk, P., 1993. Differential growth of larval sprat, Sprattus sprattus, across a tidal front in the eastern North Sea. Mar. Ecol. Prog. Ser. 99, 17±27. Moksness, E., Wespestad, V., 1989. Ageing and back-calculating growth rates of Pacific herring, Clupea pallasii, larvae by reading daily otolith increments. Fish. Bull. 87, 509±515. Pannella, G., 1971. Fish otoliths: Daily growth layers and periodical patterns. Science 173, 1124±1127. Pannella, G., 1974. Otolith growth patterns: An aid in age determination in temperate and tropical fishes, in: T.B. Bagenal (Ed.), The Ageing of Fish, D. Unwin., London, pp. 28±39. Regner, S., 1980. On semigraphic estimation of Gompertz function and its application on fish growth. Acta Adriat. 21, 227±236. ReÂ, P., 1983. Daily growth increments in the sagitta of pilchard larvae, Sardina pilchardus (Walbaum, 1792) (Pisces: Clupeidae). Cybium 7, 9±15. ReÂ, P., 1986. Otolith microstructure and the detection of life history events in sardine and anchovy larvae. CieÃncia. Biol. Ecol. Syst. 6, 9±17. ReÂ, P., 1987. Ecology of the planktonic phase of the anchovy, Engraulis encrasicolus (L.), within Mira Estuary (Portugal). InvestigacioÂn pesq. 51, 581±598. ReÂ, P., Gonc,alves, E., 1993. Growth of sprat, Sprattus sprattus, larvae in the German Bight (North Sea) as inferred by otolith microstructure. Mar. Ecol. Prog. Ser. 96, 139±145.
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Shields, R.J., 1989. Studies of growth and nutritional status in 0-group sprat, Sprattus sprattus (Clupeidae), using otolith microstructure and lipid analysis techniques. Ph.D. thesis, University of Wales, Bangor. TeskeredzÏicÂ, Z., 1983. The spawning of the sprat, Sprattus sprattus
(L.), in the Kvarner Region and Rijeka Bay. Acta Adriat. 24, 13±25. Theilacker, G.H., 1980. Changes in body measurements of larval northern anchovy, Engraulis mordax, and other fishes due to handling and preservation. Fish. Bull. US 78, 685±692.
Larval growth of sprat, Sprattus sprattus phalericus, larvae in the Northern Adriatic Jakov DulcÏicÂ* Institute of Oceanography and Fisheries, P.O.B.500, 21000 Split, Croatia Received 16 October 1997; accepted 14 March 1998
Abstract Sprat larvae collected in the Northern Adriatic (1995 and 1996) were used to estimate larval growth rates. Daily growth increments were counted on sagittal otoliths of 280 larvae (108 in 1995, and 172 in 1996) using transmission optical microscopy. Larval growth was estimated using the Gompertz and Laird±Gompertz growth curves for larvae ranging from 6.5 to 22.6 mm (1995) and from 6.9 to 22.5 mm (1996) in standard length. The largest growth increments were recorded for the 6day-old (0.639 mm dayÿ1) larvae in 1995, and for the 5-day-old larvae in 1996 (0.632 mm dayÿ1). Mean growth rate was 0.421 mm dayÿ1 (SD0.169) in 1995, and 0.409 mm dayÿ1 (SD0.175) in 1996. There was no signi®cant difference (P>0.05) in the rate of growth between years. # 1998 Elsevier Science B.V. All rights reserved. Keywords: Sprattus sprattus phalericus; Larvae; Otoliths; Growth; Northern Adriatic
1. Introduction The sprat, Sprattus sprattus, is a small, mutiple (batch) spawning species with a protracted spawning season and a large number of spawnings per year (Alheit, 1986). In the Adriatic, Sprattus sprattus phalericus is usually found in the areas of the Gulf of Venice, Kvarner, Kvarneric (Northern Adriatic), the Velebit channel as well as in the channels of the middle Dalmatia (TeskeredzÏicÂ, 1983). The sprat represents, after sardine and anchovy, the main pelagic species of the purse-seine catch in the Croatian Adriatic Sea.
*Corresponding author. Tel.: 00385 21 358688; fax: 00385 21 358650; e-mail: [email protected] 0165-7836/98/$19.00 # 1998 Elsevier Science B.V. All rights reserved. PII S0165-7836(98)00108-8
Larval ®sh growth is of particular importance to population dynamics, especially to recruitment and biological models incorporating environmental parameters (Houde, 1987, 1989). Microscopic markings in thin sections of the otoliths of ®shes are evidence of a record of daily growth (Pannella, 1971, 1974) and provide a means to age tropical species for which seasonal and annual growth rings are often hard to interpret. These marks, or microincrements, are produced in larvae of many ®shes (Brothers et al., 1976; ReÂ, 1983, 1986; Jones and Brothers, 1987; Moksness and Wespestad, 1989). Counting otolith microincrements has been useful in estimating growth of larval ®shes (Barkman, 1978; Methot, 1981; Geffen, 1986; Jones, 1986; DulcÏicÂ, 1995). The objective of this study was to analyze and estimate the growth characteristics of sprat larvae
118
J. DulcÏic / Fisheries Research 36 (1998) 117±126
from the North Adriatic for the ®rst time, as inferred from otolith daily growth increments. This should provide the basis for future studies of sprat growth parameters and of the conditions that affect the renewal of this population in the Adriatic Sea. 2. Material and methods Sprat larvae were collected from the North Adriatic by the research vessel `Vila Velebita'. In January (23.01.1995 and 17.01.1996), specimens were collected from the following stations in the North Adriatic: RV 001 ± depth 30 m, SJ 107 ± depth 37 m, SJ 105 ± depth 36 m, SJ 103 ± depth 33 m, SJ 101 ± depth 28 m and SJ 108 ± depth 31 m (Fig. 1). Material was collected by Hensen plankton net (73/ 100) with 0.280 mm mesh size, 5 m above the bottom to surface vertical hauls. The net was towed at a speed
of 0.5 m/s. The mean surface temperature over the surveyed area was 10.80.628C (1995) and 10.50.518C (1996). The planktonic material was preserved in 5% formalin buffered with borax (pH 8.5±9) (ReÂ, 1983). A total of 280 sprat larvae was examined (108 in 1995, and 172 in 1996). Larval standard lengths were measured (the distance along the midline of the body from the tip of the snout to the end of urostyle) with the aid of a binocular microscope to the nearest 0.1 mm by placing the larva on a transparent grid marked in millimeters and illuminated from below. Larval lengths were corrected for shrinkage using the equation proposed by Theilacker (1980) for Engraulis mordax. All larval lengths correspond to standard lengths corrected for shrinkage. Sprat larvae were aged according to daily growth increments in sagittal otoliths. The methods used for obtaining, mounting and observing the sagittae were described by ReÂ, 1983, 1986. Microgrowth increments were counted with the aid of a compound optical microscope using magni®cations of 600 and 1000. Several counts were made for each sagitta, and the number obtained most frequently was chosen. The mean of the counts of both sagittae from each larva was used for data analysis. Otoliths, unsuitable for examination because of unclear microstructure or de®ciency in the preparation, were discarded. All otolith measurements were taken under the microscope using a calibrated micrometer eyepiece. Yolksac larval otoliths were included in the analysis to establish a start of increment formation. Data from the North Adriatic were mathematically and statistically analyzed. The relationship between age and length of larvae was given by the common non-linear growth equations (Kramer and Zweifel, 1970; Regner, 1980). Two equations were used to describe length at age of sprat larvae. The ®rst equation is given by Gompertz (1825): It a exp ÿbeÿct
(1)
where lt is the length of larvae at time t, a the asymptote, and b and c the constants. The second equation is given by Laird et al. (1965): It I0 exp A0 =c 1 ÿ eÿct Fig. 1. Sampling area and station numbers in the Northern Adriatic.
(2)
where l0 is the length of larvae at time t0, A0 the instantaneous growth rate at time t0, and c the same
J. DulcÏic / Fisheries Research 36 (1998) 117±126
constant as in previous equation. Parameters were calculated from the data on age obtained from otolith readings and on length of larvae by an iterative procedure using the STATISTICA program. Daily growth rates were derived from the Gompertz ®t by examining the Lt ÿ Ltÿ1 = Aget ÿ Agetÿ1 values over the range of ages available. 3. Results Sprat larvae ranged from 6.5 to 22.6 mm in standard length (mean length15.704.45 mm, median16.50 mm) in 1995, and from 6.9 to 22.5 mm (mean length15.054.43 mm, median14.60 mm) in 1996. Typical growth increments composed of dark discontinuous and light incremental zones when viewed under a microscope with transmitted light could only be discerned in sagittae belonging to older larvae with functional mouths, pigmented eyes and little or no residual yolk. Results of ring counts are presented in Table 1. Values for the parameters in Gompertz and Laird± Gompertz functions are given in Table 2. Graphical representations of the data ®tted by the Gompertz function are given in Fig. 2. The largest growth increments were recorded for 6day-old (0.639 mm dayÿ1) larvae in 1995, and for 5day-old larvae in 1996 (0.632 mm dayÿ1) (Fig. 3). Mean growth rate was 0.421 mm dayÿ1 (SD0.169) in 1995, and 0.409 mm dayÿ1 (SD0.175) in 1996. In order to compare the rate of growth between two seasons, the Gompertz curves were linearized and examined for homogeneity of slope using the t-test. There was no signi®cant difference at the 0.05 level. There were no signi®cant differences between the radii of left and right sagittae (Wilcoxon test, P>0.05), or between the number of daily growth increments enumerated from left and right sagittae for both the years (Wilcoxon test, P>0.05). The relationships between the number of daily growth increments and otolith radii were ®tted with exponential curves (Fig. 4), and that between larval length and otolith radius with a power±regression curve Y aX b , taking Y as otolith radius and X as larval length (Fig. 5). The parameters of the relationship between otolith radius and larval length were: a0.027, b2.526 (1995); a0.028, b2.541 (1996), indicating a positive allo-
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Table 1 Number of daily rings and the standard length range of sprat Sprattus sprattus phalericus larvae in 1995 and 1996, in the Northern Adriatic No. of rings (days)
No. of Larvae
Length range (mm)
Mean length (mm)
1995 0 1 2 4 5 8 11 12 14 15 16 17 18 19 20 24 25 26 30 33 37 Total
5 3 4 3 4 4 6 5 3 7 3 10 8 7 11 6 5 3 5 3 3 108
6.5±7.4 7.4 7.4±7.6 7.9±8.0 9.0±10.9 11.5±12.0 13.4±13.9 13.9±14.4 14.8±14.9 14.8±15.3 15.1±15.6 16.2±16.7 16.4±17.6 16.9±18.2 17.8±18.4 19.5±20.4 20.4±20.7 20.8±21.1 21.5±21.6 21.9±22.0 22.0±22.6
7.080.341 7.40 7.480.100 7.930.058 9.580.903 11.850.238 13.720.183 14.160.195 14.870.058 15.070.198 15.400.265 16.370.231 16.980.423 17.610.406 18.130.224 19.920.313 20.500.141 20.970.153 21.520.045 21.930.058 22.370.321
1996 0 2 3 5 6 7 8 10 11 12 15 17 19 20 24 25 27 30 32 37 Total
4 5 5 6 15 6 11 17 8 10 15 11 9 5 14 7 7 7 4 6 172
6.9±8.0 7.2±8.8 7.5±8.9 9.1±11.0 9.9±11.4 10.5±12.0 10.3±12.2 12.2±13.4 13.3±13.9 13.9±14.8 14.6±15.5 15.8±16.9 16.9±17.8 18.0±18.4 19.6±20.4 20.2±20.7 20.0±21.4 21.0±21.6 21.5±21.9 22.0±22.5
7.380.519 7.820.698 8.180.598 9.680.691 10.640.453 11.480.512 11.660.609 12.790.384 13.550.256 14.270.309 15.080.303 16.390.333 17.610.366 18.180.148 19.960.288 20.440.162 20.930.425 21.390.267 21.730.171 22.200.210
metry. The power±regression curves, describing the otolith radius and standard length relationship, do not ®t well for the smallest and largest larvae, despite
J. DulcÏic / Fisheries Research 36 (1998) 117±126
120
Table 2 Estimated values of Gompertz and Laird±Gompertz functions (SE ± standard error).
Gompertz (1995) Gompertz (1996)
Laird±Gompertz (1995) Laird±Gompertz (1996)
a
SE
b
SE
c
SE
r
P
25.92 25.65
0.632 0.742
1.379 1.336
0.0185 0.0137
0.067 0.067
0.0034 0.0045
0.988 0.986
<0.001 <0.001
l0
SE
A0
SE
c
SE
r
P
6.52 6.74
0.203 0.221
0.092 0.089
0.0056 0.0053
0.067 0.067
0.0039 0.0044
0.988 0.986
<0.001 <0.001
Fig. 2. Gompertz model, adjusted to the observed data (1995 and 1996).
J. DulcÏic / Fisheries Research 36 (1998) 117±126
121
Fig. 3. Growth rates in mm dayÿ1 (1995 and 1996).
relatively high values of correlation coef®cients. Otolith size begins to increase relatively fast when larvae reached 20 mm. Data on larvae length and otolith radius indicated at least two periods of change in their growth rates. These periods could be attributed with relative certainty to intrinsic changes which occur during stage-speci®c periods of growth. The changes in growth rates may be described much better by the ®fth-order polynomials with a high degree of probability levels (1995: yÿ56.8139.646xÿ8.547x2 0.844x3ÿ0.038x40.001x5; 1996: yÿ66.068 45.823xÿ9.468x20.964x3ÿ0.043x40.001x5; y otolith radius, xstandard length) (Fig. 6). Sagittal daily growth increments had different widths and were clearly wider close to the border of the otolith in older larvae. The mean width of daily growth increments varied from 0.60 to 2.85 mm (mean1.56 mm, SD0.36) and was greater in larger larvae. The average radius of the ®rst feeding check was 10.48 mm (SD0.69; mean larval length ± 7.4 mm). 4. Discussion Sprat growth and development rates can be determined by analysis of otolith increments, which can be
counted and measured with an optical microscope, since Re and Gonc,alves (1993) found that the smallest increment, in sagittae of Sprattus sprattus sprattus, measured in addition to mean widths of daily increments was clearly above the functional resolution limit of the optical microscopy (the majority of daily growth increments had widths 1 mm), suggesting that unresolved increments (Campana et al., 1987) were not a problem in this study, but con®rmation of the optical microscope counts by a scanning electron microscope is always highly desirable. All published studies indicate that otolith increments are found at different developmental stages but are characteristic of the species being studied. Some species hatch with increments already formed, while others do not form increments until yolk-sac absorption. Alshuth (1988) studied the deposition of microgrowth increments in the sagittae of laboratoryreared sprat larvae. He noted that increments were ®rst observed 6 days after hatching (at a temperature of 158C) at the time of ®rst feeding and complete absorption of the yolk sac, which is in agreement with results in this study. The increments were formed under a daily rhythm for a period of 29 days. Shields (1989) showed that the daily increment-deposition rate was in late-larval and juvenile stages of sprat. The author also
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J. DulcÏic / Fisheries Research 36 (1998) 117±126
Fig. 4. Relationship between the otolith radius and age of the sprat larvae.
observed that multiple feedings per day did not disrupt the daily increment formation, but intermittent feeding altered the appearance of juvenile increments and resulted in sub-daily increment counts. Re and Gonc,alves (1993) con®rmed the daily nature of otolith growth increments using the marginal increment technique described by Re (1987), indicating that at least
larvae with lengths greater than 11.0 mm form daily growth increments in their otoliths. They also suggested that there is some evidence that daily growth increments are deposited on the otoliths of sprat larvae only after the onset of exogenous feeding. Shields (1989) validated the correspondence between number of increments and age in days of sprat larvae. He found
J. DulcÏic / Fisheries Research 36 (1998) 117±126
123
Fig. 5. Relationship between the otolith radius and length of sprat larvae (power±regression curve YaXb).
a one-to-one relationship when increment widths were >1.5 mm. In the present study, increments were mostly >1.5 mm; thus, their number is assumed to re¯ect age in days. The growth rates in this study (0.639 and 0.632 mm dayÿ1) are comparable to those obtained for similar pelagic clupeoid species (Methot and
Kramer, 1979; ReÂ, 1986; Leak and Houde, 1987; DulcÏicÂ, 1995). Shields (1989) found integrated somatic growth rates that varied from 0.37 to 0.49 mm dayÿ1 for sprat, Sprattus sprattus sprattus, larvae in the Irish Sea. Munk (1993) investigated the daily growth of sprat larvae in the eastern North Sea and found signi®cant differences in growth rate of
124
J. DulcÏic / Fisheries Research 36 (1998) 117±126
Fig. 6. Relationship between the otolith radius and length of sprat larvae (fifth-order polynomials).
larvae in relation to their distance from a frontal zone, implying that the best conditions for larval growth and survival may be located close to this zone. Growth rate estimates were highest in the mixed water (absolute growth rate of 12 mm larvae: 0.47 mm dayÿ1). At the mixed side of the front, where larval abundance peaked, growth was slightly lower, whereas growth rate declined signi®cantly further offshore (to a minimum of 0.13 mm dayÿ1 for 16 mm larvae). Re and
Gonc,alves (1993) also found integrated somatic growth was 0.406 mm dayÿ1 for sprat larvae in the German Bight (North Sea). The same authors mentioned that there were no signi®cant differences in growth rates found at contrasting sites (strati®ed ± 0.405 mm dayÿ1 and mixed water masses ± 0.369 mm day). Differences in somatic growth could be connected to the in¯uence of temperature and food availability differences in the areas investigated. In
J. DulcÏic / Fisheries Research 36 (1998) 117±126
this study, there was no signi®cant difference in the rate of growth between years since the mean temperatures were similar during the times of larval collections. This result could imply that growth probably was not a main factor controlling the recruitment process. So, in all cases in future, when the data on age of larvae are needed, the growth parameters should be estimated to every particular survey since there is a great possibility that environment conditions will be different from one year to the next. The in¯uence of primary production on larval growth rate is mediated through its effect on secondary production and zooplankton abundance. In this context, it is not so much the total zooplankton biomass, but the size fraction that larvae are capable of eating that is important. Therefore, further studies on zooplankton concentration and its particle-size distribution, as well as on hydrographical parameters in the Northern Adriatic, are needed since they could determine growth rate and condition of larvae. Acknowledgements The author thanks colleagues, Mr. V. TicÏina and crew of the research vessel `Vila Velebita', for their great help in collecting material. He also offers special thanks to the two anonymous reviewers for their useful comments on the manuscript. References Alheit, J., 1986. Reproductive biology of sprat, Sprattus sprattus: Factors determining annual egg production. Comm. Meet. Int. Coun. Explor. Sea C.M.-ICES/H, 58, p. 16. Alshuth, S., 1988. Daily growth increments on otoliths of laboratory-reared sprat, Sprattus sprattus L. larvae. Meeresforsch. 32, 23±29. Barkman, R.C., 1978. The use otolith growth rings to age young Atlantic sliversides, Menidia menidia. Trans. Am. Fish. Soc. 197, 790±792. Brothers, E.B., Mathews, C.P., Lasker, R., 1976. Daily growth increments in otoliths from larval and adult fishes. Fish. Bull. US 74, 1±8. Campana, S.E., GagneÂ, J.R., Munro, J., 1987. Otolith microstructure of larval herring (Clupea harengus): image or reality?. Can. J. Fish. Aquat. Sci. 42, 1922±1929. DulcÏicÂ, J., 1995. Estimation of age and growth of sardine, Sardina pilchardus (Walbaum, 1792), larvae by reading daily otolith increments. Fish. Res. 22, 265±277. Geffen, A.J., 1986. The growth of herring larvae, Clupea harengus
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L., in the Clyde: An assessment of the suitability of otolith ageing methods. J. Fish. Biol. 28, 279±288. Gompertz, B., 1825. On the nature of the function expressive of the law of human mortality, and on the mode of determining the value of live contingencies, Phil. Trans. Roy. Soc. Lond. 115, pp. 531±585. Houde, E.D., 1987. Fish early life dynamics and recruitment variability. Am. Fish. Soc. Symp. 2, 17±29. Houde, E.D., 1989. Comparative growth, mortality and energetics of marine fish larvae: Temperature and implied latitudinal effects. Fish. Bull. US 87, 471±495. Jones, C., 1986. Determining age of larval with the otolith increment technique. Fish. Bull. 84, 91±103. Jones, C., Brothers, E.B., 1987. Validation of the otolith increment ageing technique for striped bass, Morone saxatilis, larvae reared under suboptimal feeding conditions. Fish. Bull. 85, 171±178. Kramer, D., Zweifel, J.R., 1970. Growth of anchovy larvae (Engraulis mordax Girard) in the laboratory as influenced by temperature. Calif. Coop. Oceanic Fish. Invest. Rep. 14, 84±87. Laird, A., Tyler, S.A., Barton, A.D., 1965. Dynamics of normal growth. Growth 29, 233±248. Leak, J.C., Houde, E.D., 1987. Cohort growth and survival of bay anchovy, Anchoa mitchilli, larvae in Biscayne Bay. Florida. Mar. Ecol. Prog. Ser. 37, 109±122. Methot, R.D., , Jr.1981. Spatial covariation of daily growth rates of larval northern anchovy, Engraulis mordax, and northern lampfish, Stenobrachius leucopsarus. Rapp. P.-v. ReÂun. Cons. int. Explor. Mer. 178, 424±431. Methot, R.E., Kramer, D., 1979. Growth of northern anchovy Engraulis encrasicholus larvae in the sea. Fish. Bull. 77, 413± 423. Munk, P., 1993. Differential growth of larval sprat, Sprattus sprattus, across a tidal front in the eastern North Sea. Mar. Ecol. Prog. Ser. 99, 17±27. Moksness, E., Wespestad, V., 1989. Ageing and back-calculating growth rates of Pacific herring, Clupea pallasii, larvae by reading daily otolith increments. Fish. Bull. 87, 509±515. Pannella, G., 1971. Fish otoliths: Daily growth layers and periodical patterns. Science 173, 1124±1127. Pannella, G., 1974. Otolith growth patterns: An aid in age determination in temperate and tropical fishes, in: T.B. Bagenal (Ed.), The Ageing of Fish, D. Unwin., London, pp. 28±39. Regner, S., 1980. On semigraphic estimation of Gompertz function and its application on fish growth. Acta Adriat. 21, 227±236. ReÂ, P., 1983. Daily growth increments in the sagitta of pilchard larvae, Sardina pilchardus (Walbaum, 1792) (Pisces: Clupeidae). Cybium 7, 9±15. ReÂ, P., 1986. Otolith microstructure and the detection of life history events in sardine and anchovy larvae. CieÃncia. Biol. Ecol. Syst. 6, 9±17. ReÂ, P., 1987. Ecology of the planktonic phase of the anchovy, Engraulis encrasicolus (L.), within Mira Estuary (Portugal). InvestigacioÂn pesq. 51, 581±598. ReÂ, P., Gonc,alves, E., 1993. Growth of sprat, Sprattus sprattus, larvae in the German Bight (North Sea) as inferred by otolith microstructure. Mar. Ecol. Prog. Ser. 96, 139±145.
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Shields, R.J., 1989. Studies of growth and nutritional status in 0-group sprat, Sprattus sprattus (Clupeidae), using otolith microstructure and lipid analysis techniques. Ph.D. thesis, University of Wales, Bangor. TeskeredzÏicÂ, Z., 1983. The spawning of the sprat, Sprattus sprattus
(L.), in the Kvarner Region and Rijeka Bay. Acta Adriat. 24, 13±25. Theilacker, G.H., 1980. Changes in body measurements of larval northern anchovy, Engraulis mordax, and other fishes due to handling and preservation. Fish. Bull. US 78, 685±692.