Marine Biology (2003) 142: 1169–1179 DOI 10.1007/s00227-003-1028-5
K. Ganias Æ S. Somarakis Æ A. Machias A. J. Theodorou
Evaluation of spawning frequency in a Mediterranean sardine population (Sardina pilchardus sardina)
Received: 23 January 2002 / Accepted: 3 January 2003 / Published online: 21 March 2003 Springer-Verlag 2003
Abstract The postovulatory follicle method was used to assess the frequency of spawning of sardine (Sardina pilchardus sardina) in the Central Aegean Sea (eastern Mediterranean) in November–December 1999 and 2000. A field-based aging key for postovulatory follicles (POFs) was developed, and preliminary evidence is presented of a temperature influence on the degeneration of POFs. Bias in the fraction of day-0 spawners (females that had, were, or would spawn the night of sampling) with respect to sampling time was identified and attributed to spawning behavior. An appraisal of consistency in spawners’ fractions and sex ratio, based on four sets of sequential trawl hauls, showed a considerably high small-scale variability, which suggested that spawning schools are structures limited in space and/or ephemeral in time. Sampling gear, i.e. commercial purse seines and research pelagic trawls, did not differ significantly with respect to spawners’ fractions. The fractions of day-1 and day-2 females were the same during both years, and their combination resulted in more precise, composite estimates of spawning frequency. In both years, the Mediterranean sardine spawned every 11–12 days. The incidence of spawning increased significantly with fish size. When compared to all estimates available for other sardine genera, species and subspecies, the spawning frequency of the Mediterranean sardine was lower; this
Communicated by R. Cattaneo-Vietti, Genova K. Ganias (&) Æ A. J. Theodorou Laboratory of Oceanography, University of Thessaly, Fytokou Street, 38446 Magnisia, N. Ionia, Greece E-mail:
[email protected] Tel.: +32-421-093053 Fax: +32-421-093054 K. Ganias Æ S. Somarakis Æ A. Machias Institute of Marine Biology of Crete, P.O. Box 2214, 71003 Iraklio, Crete, Greece S. Somarakis Laboratory of Zoology, Department of Biology, University of Patras, 26500 Patras, Rio, Greece
was attributed to the synergetic effect of oligotrophy and smaller body sizes in the Mediterranean.
Introduction Most clupeoids like anchovies and sardines are indeterminate spawners, producing multiple batches of eggs in a protracted spawning period (Blaxter and Hunter 1982). The spawning frequency or fraction of females spawning per night is an important reproductive variable of indeterminate spawners and a crucial parameter of the daily egg production method (DEPM), a widely used direct method of assessing the spawning biomass of pelagic fishes (Lasker 1985; Hunter and Lo 1997). Besides biomass estimation, series of spawning frequency values for fish stocks can lead to new insights into their reproductive biology, particularly when such values can be compared between species and stocks or habitats and seasons (e.g. Alheit 1993). Since the early 1980s, and based on the pioneer work of Hunter and Goldberg (1980), methods have been developed for the histological estimation of spawning frequency that are based on the state of deterioration of the postovulatory follicles (Hunter and Macewicz 1985). A prerequisite for applying the postovulatory follicle method is validation of the duration that postovulatory follicles (POFs) can be detected in field samples. To develop aging criteria for POFs, fish can be spawned in the laboratory and sampled at known times after spawning (e.g. Hunter and Goldberg 1980). An alternative method is to examine a time-series of field-collected material in relation to peak spawning time (Goldberg et al. 1984; Macewicz et al. 1996). Ideally, the effect of temperature should be taken into account, because the rate of POF resorption is temperature dependent (Fitzhugh and Hettler 1995, and references therein). The estimation of spawning frequency is often subjected to sampling bias, which is usually introduced by the typical behavior of pelagic fish to form spawning
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groups or schools and synchronize spawning within such aggregations. This might result in time-related changes in sex ratio as well as the fraction of day-0 spawners (females that had, were or would spawn the night of sampling) (e.g. Picquelle and Stauffer 1985). Alheit (1993) speculates on the possibility of biased estimates when collecting samples from commercial fisheries and indicates the importance of collecting independent samples for estimating spawning frequency. However, short-term temporal or spatial variability in spawning fractions has never been assessed. The frequency of spawning might vary seasonally and be affected by the age structure of the population or food abundance (Alheit 1993; Hunter and Lo 1997; Somarakis 1999). Nevertheless, at least for some species or stocks, the spawning frequency can be relatively constant as long as environmental conditions do not change (McEvoy and McEvoy 1992; Hunter and Lo 1997). In the present study we assessed the spawning frequency of the Mediterranean sardine Sardina pilchardus sardina in the eastern Mediterranean (Central Aegean Sea) during November–December 1999 and 2000. A field-based aging key for POFs is presented, along with preliminary evidence of a temperature influence on POF degeneration. Sampling bias related to adult spawning behavior was appraised, and spawning frequency estimates were subsequently corrected. Inter-annual, intergear and small-scale variability in spawning fractions were analyzed, and their dependence on fish size was evaluated. Information based on previous applications of the postovulatory follicle method on several stocks of Sardina spp. (Cunha et al. 1992; Garcı´ a et al. 1992; Lago de Lanzo´s et al. 1998; Anonymous 2000; Quintanilla and Pe´rez 2000) and Sardinops spp. (Macewicz et al. 1996; Ward et al. 2001) reveals various intricacies of the method that might affect accuracy and precision of the respective spawning frequency estimates. These include: (1) inter-laboratory differences concerning the interpretation of POFs (Anonymous 2000), (2) indication of extended daily spawning periods (Fig. 2 in Quintanilla and Pe´rez 2000), which might complicate the correct assignment of females as to the day of spawning, and (3) inconsistency in the incidence of bias with respect to day-0 females, which are occasionally over-represented (Garcı´ a et al. 1992, Galicia), under-represented (Quintanilla and Pe´rez 2000), or sampled equally to other daily spawners’ classes (Cunha et al. 1992).
Materials and methods Sample collection and analysis Adult sardines (Sardina pilchardus sardina) were collected at nighttime from coastal locations of the Central Aegean Sea during November–December 1999 and 2000 (Tables 1, 2), i.e. the peak of the spawning period (Ganias et al. 2001b; Somarakis et al. 2001). Sampling was carried out on board the commercial purse seine
fleet, as well as on the R.V. ‘‘Philia", by means of a small pelagic trawl (mouth opening: 10 m, cod-end mesh size: 10 mm) towed near the surface (5–40 m) for 45–60 min, in a stepped oblique manner, at 3–4 knots. The placement of samples was attempted to be proportional to the local fish concentrations. A total of 23 purse seine samples and 5 trawl samples were collected in 1999, and 19 purse seine and 11 trawl samples were collected in 2000 (Fig. 1; Tables 1, 2). Each sample consisted of a random collection of 1.5–2 kg of sardines. Fish were fixed on board in 10% neutral buffered formalin. Sex ratio, i.e. the fraction of females by numbers, was determined from a subsample of 50 specimens per sample. Spawning frequency of reproductively active females, i.e. the fraction of females spawning per night, was estimated by the postovulatory follicle method (Hunter and Macewicz 1985). A total of 15–20 females (or all the females, when their number was
