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Releasing of hatchery-reared juveniles of the white seabream Diplodus sargus (L., 1758) in the Gulf of Castellammare artificial reef area (NW Sicily)
Aquaculture 233 (2004) 251 – 268 www.elsevier.com/locate/aqua-online
Releasing of hatchery-reared juveniles of the white seabream Diplodus sargus (L., 1758) in the Gulf of Castellammare artificial reef area (NW Sicily) G. D’Anna *, V.M. Giacalone, F. Badalamenti, C. Pipitone CNR-IRMA, Laboratorio di Biologia Marina, via Giovanni da Verrazzano 17, 91014 Castellammare del Golfo (TP), Italy Received 21 February 2003; received in revised form 9 October 2003; accepted 15 October 2003
Abstract A pilot experiment of marine ranching using hatchery-reared juveniles of white seabream, Diplodus sargus, was made in the Gulf of Castellammare (NW Sicily). The research aimed at evaluating (i) if artificial reefs are suitable for the settlement of reared young seabreams, (ii) what are the main causes of mortality and (iii) the growth rate of released fishes in the open sea. A total of 6930 tagged cultured juvenile white seabreams (305 days old) were released in an artificial reefs (AR) area. Underwater visual census, sightings and recaptures were used as a source of data for estimating abundance and size of released fishes. The survey lasted 15 months and was carried out in artificial (AR, breakwaters and harbours) and natural (river mouths, rocky bottoms and Posidonia oceanica meadows) coastal habitats of the Gulf. A few days after the release, more than 90% of the tagged seabreams left AR and moved mainly towards harbours and breakwaters, which resulted to be particularly suitable for their settlement and growth. The recapture was 8.2% of the released stock. During the first days after releasing, the main ascertained sources of mortality were professional fishing (6.7%) and predation by conger eel, Conger conger (1.1%). A behavioural deficit of the reared seabreams in the use of refugia and food was observed in the initial period following the release. The results obtained provide some management suggestion for the feasibility of marine ranching initiatives involving hatchery-reared fishes. D 2004 Elsevier B.V. All rights reserved. Keywords: Marine ranching; Hatchery-reared fish; Released fish; Diplodus sargus; Artificial substrata; Mediterranean
* Corresponding author. E-mail address: [email protected] (G. D’Anna). 0044-8486/$ - see front matter D 2004 Elsevier B.V. All rights reserved. doi:10.1016/j.aquaculture.2003.10.024
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1. Introduction Stock enhancement by hatchery-reared species goes back to the mid-19th century (Howell et al., 1999; Moring, 1986), and it was followed by the growing interest of industry, market and public authorities (Svasand et al., 2000) that it is now flourishing in many areas, particularly in Japan (Fushimi, 2001; Masuda and Tsukamoto, 1998). Nonetheless, most of the hatchery-based release programmes for the enhancement of wild stocks have failed (Bohnsack, 1996), the exceptions being the Japanese experiences (Honma, 1993; Matsuoka, 1989) and the releasing occurred in circumscribed habitats (e.g., coastal lagoons, fiords, estuaries, etc.) (McEachron et al., 1995). Failure has generally been attributed to the releasing at inappropriate habitats and times (Bohnsack, 1996), to the little knowledge on the biology and ecology of released species (Masuda and Tsukamoto, 1998; Travis et al., 1998) and to the production at hatchery of genetically, physiologically and behaviourally inferior individuals (Bohnsack, 1996; Munro and Bell, 1997). Hatchery-raised fish ends up with behavioural deficit (Olla et al., 1994) including the lack of effective anti-predatory and foraging strategies, which in turn could be responsible of the high mortality rate after releasing (Brown and Laland, 2001; Griffin et al., 2000). Only recently marine ranching, a type of stock enhancement aimed at keeping released cultured juvenile fish in coastal waters without cages has acknowledged for some intrinsic behaviour of the released species (e.g., Kuwada et al., 2000). In the Gulf of Castellammare (NW Sicily), several attempts have been made since the mid-1980s by the Sicilian Regional Government in order to rebuild the severely depleted demersal stocks (Whitmarsh et al., 2002). These initiatives included the deployment of a large artificial reef (AR) system of about 20 000 m3 (Badalamenti et al., 2000) and the establishment of a 20 000-ha fishery reserve (Pipitone et al., 2000). Moreover, a project involving a massive release of reared seabreams on artificial reefs has recently been planned (but not yet implemented) by a local Consortium that aggregates the five coastal towns in the Gulf. Since these initiatives have been set, soft bottom benthic and nektobenthic fish biomass has increased (Pipitone et al., 2000), while rocky bottom fishes, on both natural and artificial substrates, did not show a similar trend and remained almost constant in the period between 1990 and 1998 (D’Anna et al., 2001). Such species as the seabreams Diplodus sargus and D. vulgaris, that are characteristic of the Mediterranean rocky infralittoral fish assemblage (Sala and Ballestoros, 1997), were expected to increase following the AR deployment; they were found instead with little numbers (Badalamenti et al., 2000), although food (Badalamenti et al., 1992; Pepe et al., 1996, 1998; Tumbiolo et al., 1997) and shelter (Relini, 2000) were not limited at the AR and surrounding areas. The white seabream, D. sargus is a commercially exploited fish that gains a high market price in the Mediterranean area (Harmelin-Vivien et al., 1995), whose catches have declined in the last decade (FAO, 2002). It is targeted by small-scale and sport fisheries (Reina et al., 1994). Its biology and ecology are well known (Biagi et al., 1998; GarciaRubies and Macpherson, 1995; Gordoa and Moli, 1997; Harmelin, 1987; Harmelin-Vivien et al., 1995; Macpherson, 1998; Macpherson et al., 1997; Planes et al., 1999; Rosecchi, 1987; Vigliola and Harmelin-Vivien, 2001). This species is also successfully bred (Mazzola et al., 1985) and reared up to the age of about 1 year, before its growth rate
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slows down making the rearing process inappropriate for intensive aquaculture as well as economically unprofitable (Abellan et al., 1994). This paper reports the results of a marine ranching experiment aimed at providing baseline data for the above-mentioned Consortium release plan, within a more general management framework of development of the artisanal fishery in the artificial reef area. In particular, the research had the following objectives: (i) evaluating if artificial reefs are suitable for the settlement of hatchery-reared young seabreams, (ii) what are the main causes of mortality, and (iii) assessing the growth rate of released fishes.
2. Materials and methods 2.1. Study site The Gulf of Castellammare is characterised by cliffs on its sides and by shallow sandy shores in the middle, with patches of rocky bottom and Posidonia oceanica, and by the presence of stream and river mouths. In addition, in the Gulf, there are several artificial habitats, represented by harbour areas and breakwater reefs located at 20 –30 m from the coast, and by the submersed artificial reef system further offshore. The artificial reef area, chosen for releasing the seabreams, is arranged in pyramids, each made of 14 concrete boulders of 8 m3 displaced on three levels, located in two sites: Alcamo Marina (AM) and Balestrate (BAL) (Fig. 1). 2.2. Tagging and releasing The ‘‘Ittica Mediterranea’’ fish farm of Petrosino (Trapani) has reared a special batch of seabreams for this experiment, starting from a parent stock caught in the Gulf. Genetic tests have demonstrated the compatibility between the reared batch and the wild population (D’Anna and Badalamenti, 2000). The seabreams were tagged using dart style tags (T-Bar AFD-68B FF, made by ‘‘Floy Tags’’) (Giacalone et al., in press), following the procedure suggested by Parker et al., 1998. In March 1999, 7284 305-day-old seabreams were tagged. The mean total length (TL) was 11.50 F 1.05 cm and the mean weight was 32 F 9.9. During tagging operations, 345 fish died (4.5% of the total number), while 9 died during transportation from the farm to the port of Castellammare del Golfo. A total number of 6930 fish were released, of which 5300 over 16 pyramids at AM and 1630 over 5 pyramids at BAL, with an average number of 330 fish per pyramid. The releasing was done using cages built on purpose to:
reduce transport stress; release fishes underwater as close as possible to the pyramids, without the presence of divers; limit releasing costs as much as possible. Cages, made with a PVC structure and a plastic net, were cylindrical with a volume of about 550 l (Fig. 2), and contained 330 fish on average. Each cage was transported to the
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Fig. 1. Map of the Gulf of Castellammare with tagged seabreams spotting sites. AM = artificial reef at Alcamo Marina; BAL = artificial reef at Balestrate; E = harbours; *= river mouths with rock and sand; z = breakwater reefs; = rock mixed with P. oceanica.
Fig. 2. Opening procedure of the cage used for fish release.
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releasing site within a tank filled with water. Cages were ballasted and provided with a remotely controlled opening mechanism. The opening of the cage was carried out after a few min acclimatisation period on the seabed (Fig. 2). 2.3. Data collection and sampling techniques Data collected by visual census, sightings and recapture were recorded for 15 months after releasing the fish (from March 1999 to May 2000). This time was divided into three periods: P1 (initial, within 1 month from releasing), P2 (intermediate, from the second to the forth month after releasing) and P3 (final, from the fifth to the fifteenth month after releasing). 2.3.1. Visual census on the artificial reefs and the coastal habitats Underwater visual census technique was performed over the three periods on five different habitats including: artificial reefs (AR); river mouths with rock and sand (RM); breakwater reefs (BWR); harbours (Harb.); rocky bottom mixed with P. oceanica (R-P.o.). Censuses were performed by two SCUBA divers who registered in situ each observation on a polyester pad. In each census, tagged seabream abundance (N) and total length (TL) were recorded. N was gathered using class intervals of abundance while TL was estimated to the nearest 1 cm (Harmelin-Vivien et al., 1985; Bortone et al., 1991). Visual census was carried out using random linear transects and point count methods (Bortone et al., 1989): each count lasted about 20 min and the volume of water considered was about 225 m3. A more detailed description of visual census techniques, in both natural and artificial habitats, is reported by D’Anna et al. (1999). 2.3.2. Sightings and recapture Sightings and recaptures by recreational and professional fishermen were used to estimate dispersion patterns and fishing mortality of tagged seabreams. In the first 2 weeks after the release, a daily census of the fish caught by professional and recreational fishing was done in the harbours of Castellammare, Balestrate and Trappeto (Fig. 1), to evaluate the amount of recapture. Moreover, a questionnaire for data collection on sightings and recapture was distributed among fishermen of the Gulf. Fields to be filled included: date, location, type of habitat, number of tagged fish and, where possible, an estimate of their size. If a tagged fish was caught, fishermen were asked to hand over the fish, or at least the tag. An information sheet was posted in the five ports of the Gulf. 2.3.3. Predation on the artificial reefs Based on previous knowledge of the fish assemblage in the AR area (D’Anna et al., 1994), the conger eel, Conger conger, was deemed to be the main fish predator. A longline with 200 hooks was used to catch conger eels at AM and BAL 24 h after the releasing of seabreams. This was done only once to quantify the mortality of tagged seabreams after releasing due to conger eel predation. The longline was set at sunset and hauled at dawn. The same operation was carried out at a control site without marked fish (Trappeto, TRA) (Fig. 1), to test possible differences in the number of predated
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seabreams. Captured conger eels were measured, weighted and eviscerated and their gut content were analysed. Tagged seabreams found in the guts were included among recaptured specimens. 2.3.4. Behaviour of tagged seabreams on artificial reefs Video recording and underwater photography, together with observations made during visual census, allowed to gain qualitative information on the spatial distribution as well as on the behaviour of tagged seabreams on the artificial reefs during the three periods. 2.4. Data analysis Mean abundance values of tagged seabreams taken from the above-mentioned coastal habitats were tested with a three-way analysis of variance (Underwood, 1997) including: type of habitat (five levels: ar, RM, BWR, Harb. and R-P.o.), Orthogonal and fixed; period (p) (three levels: P1, P2 and P3), orthogonal and fixed; date (two levels: 1 and 2), random and nested within the interaction between habitat and period. To analyse differences in the mean size of tagged seabreams through time and in different habitats, a two-way ANOVA was applied between type of habitat and period (P) both fixed and orthogonal. The analysis was performed on an unbalanced number of replicates since all the censed specimens were used. A sample of 36 conger eel stomachs, 12 per each location, was randomly chosen from the whole catch. A one-way ANOVA with location as a fixed factor (three levels: AM, BAL and TRA) was performed on the number of individuals of Diplodus spp. as a response variable. Analyses of variance were carried out using ‘‘Gmav5’’ software after checking the homogeneity of variance with the Cochran test. When differences were found, a-posteriori comparisons were made using the Student –Newman –Keuls test (Underwood, 1997). On the total number of seabreams censed and sighted, size class frequency distribution was calculated for each habitat over the three different periods. Size frequency distributions were compared with the Kolmogorov – Smirnov (K – S) test, and linear regressions between the days following seabream release and the mean abundance and size were used to examine their trends through time.
3. Results 3.1. Visual census on artificial reefs and coastal habitats 3.1.1. Abundance and size of tagged seabream on artificial reefs A total of 628 tagged seabreams was counted in the artificial reef areas over the whole study period. The highest abundance in the artificial reef area was registered 7 days after fish release with a mean value of 47.81 F 12.4 for each pyramid and an estimate of 1004 individuals. The last tagged seabreams were observed 218 and 154 days after the release in AM and BA, respectively (Table 1).
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Table 1 Abundance of tagged seabreams on artificial reefs after their release, as drawn from visual census survey Date
Days
Np
Nm
S.E.
Nt
N%
12/03/99 16/03/99 08/04/99 03/05/99 13/05/99 13/06/99 16/07/99 10/08/99 14/09/99 13/10/99 30/12/99 29/01/00 29/02/00 30/03/00 28/04/00
3 7 30 55 65 96 129 154 189 218 295 326 357 386 416
7 8 7 7 8 8 10 8 10 9 7 7 8 8 8
27.86 47.81 2.71 1.86 1.81 0.00 0.20 0.06 0.00 0.17 0.00 0.00 0.00 0.00 0.00
4.96 12.39 1.02 0.53 0.88 0.00 0.13 0.06 0.00 0.17 0.00 0.00 0.00 0.00 0.00
585 1004 57 39 38 0 4 1 0 4 0 0 0 0 0
8.44 14.49 0.82 0.56 0.55 0.00 0.06 0.02 0.00 0.05 0.00 0.00 0.00 0.00 0.00
Np = number of censed pyramids; Nm = mean number of tagged seabreams per pyramid; S.E. = standard error; Nt = total abundance of tagged seabreams present on artificial reefs; N% = percentage of tagged seabreams in relation to total number of released fish.
The mean size of all counted seabreams at AM and BAL through time is shown in Fig. 3. There were significant regressions of time against abundance (AM, p < 0.01; BAL p < 0.05) and size (AM and BAL, p < 0.001): slopes were negative for abundance (AM, n = 22, R = 0.56, b = 0.12, a = 14.70; BAL, n = 16 R = 0.57 b = 0.48, a = 43.69) and positive for seabream size (AM, n = 22, R = 0.93, b = 0.028, a = 11.56; BAL, n = 16 R = 0.81 b = 0.03, a = 11.29). 3.1.2. Abundance and size of tagged seabream over the coastal habitats The ANOVA showed significant differences in the number of tagged individuals per habitat, period and for the interaction between habitat and period (Table 2). In P1, there
Fig. 3. Mean total length (TL) with standard deviation (S.D.) of tagged seabreams on artificial reefs after fish release. n = number of observations.
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Table 2 ANOVA on number of tagged seabreams censed in five habitats and three periods Source of variation
Abundance of tagged seabreams df
MS
F
Habitat (H) Period (P) Date (H P) HP Residuals Total Pooleda Transformation Cochran’s C-test
4 2 15 8 60 89 75 Ln(X + 1)ns C = 0.1655
5.01 12.29 1.02 3.87 0.50
8.24*** 20.18*** 1.69ns 6.36***
SNK test
Habitat
Period
Period P1 P2 P3
Harb. = AR>RM = BWR = R-P.o. BWR>AR = RM = Harb. = R-P.o. RM = BWR = Harb. = R-P.o.>AR
Habitat AR RM BWR Harb. R.-P.o.
0.6091
P1>P2 = P3 ns ns P1>P2 = P3 ns
ns = not significant. For abbreviations, see text. a Pooled term = residuals+(H P). *** =p < 0.001.
were more seabreams in Harb. and AR (Fig. 4). In P2, there was a higher number of seabreams on BWR than in any other habitat (which are all equal among each other). In P3, all habitats appeared with the same number of seabreams, with the exception of AR,
Fig. 4. Mean number (N) with standard error (S.E.) of tagged seabreams in different habitats over the three periods (P1, P2, P3). n = number of observations. For abbreviations, see text.
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Table 3 ANOVA on the size of tagged seabreams censed in five habitats and three periods Source of variation
The length of tagged seabream df
MS
F
Period (P) Habitat (H) HP Residuals Total Cochran’s C-test
2 4 8 214 228 C = 0.31ns
261.27 10.91 10.74
113.8*** 4.7*** 4.6***
SNK test
Habitat
Period
Period P1 P2 P3
AR = BWR = Harb.>RM = R-P.o. ns ns
Habitat AR RM BWR Harb. R.-P.o.
P3>P2 = P1 ns P3>P2 = P1 P3>P2 = P1 ns
ns = not significant. For abbreviations, see text. *** = p < 0.001.
which had the lowest value. On the whole, the number of seabreams in Harb. and AR was higher in P1 than in P2 and P3, while for the other habitats, there was no difference between the three periods (Fig. 4). Significant differences were found between average lengths among periods, habitats and the interaction habitat – period (Table 3). In P1, the mean length was significantly higher in Harb., BWR and AR, in comparison to RM and R-P.o. (Fig. 5). Significant
Fig. 5. Mean total length (TL) and standard deviation (S.D.) of tagged seabreams in different habitats over the three periods. n = number of observations. For abbreviations see text.
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Fig. 6. Size frequency of tagged seabream sighted in different habitats over the three periods. n = number of observations. For abbreviations, see text.
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differences in size were not recorded among the habitats in P2 and P3. In AR, BWR and Harb., the mean length in P3 was higher than P1 and P2. For what concerns RM and RP.o., no significant differences were found. 3.2. Sightings and recapture of tagged seabreams 3.2.1. Sightings From March 1999 to May 2000, a total number of 2100 tagged seabreams were observed along the coast, at distances between 0.8 and 17 km from the artificial reef (Fig. 1). There is a significant negative regression (n = 13, p < 0.001, R = 0.76, b = 0.02, a = 12.59) between the mean number of sighted tagged fishes and the days after release. An average number of 18 individuals per sighting was recorded in March 1999, and a minimum of 1 fish in May 2000. The last sighting was reported 463 days after fish release. Mean TL of the sighted individuals oscillated from 12.2 F 1.3 cm (May 1999) to 17.8 F 1.5 cm (May 2000). There is a significant positive linear relationships (n = 13, p < 0.001, R = 0.82, b = 0.01, a = 13.03) between the length of sighted seabreams and the number of days after releasing. Size frequency distribution (including also seabreams
Table 4 K – S test results on the size frequency of tagged seabreams between five habitats in three period
n = number of measured seabreams; ns = not significant. For abbreviations, see text. *p < 0.05. **p < 0.01. ***p < 0.001.
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censed in AR) in P1 shows that smaller fish were located at R-P.o. and RM, while bigger fish tended to be found in Harb. and BWR (Fig. 6). In P2, there was an homogeneous distribution of the sizes in all the habitats. In P3, there were few individuals, the bigger ones of which were found in BWR, R-P.o. and in RM. K – S test revealed significant differences in size frequency distribution among all habitats in P1 and P2. Significant differences were reported among Harb., RM, BWR and R-P.o. in P3 (Table 4). 3.2.2. Recapture A total of 570 individuals were recaptured, which makes up to the 8.2% of those released. Professional fishing contributed the most to recapture (82%), while recreational fishing contributed to the 5%. Analysis of the predator’s diet reported another 10% of recaptured individuals and the remaining 3% falls into the unknown recapture methods (Fig. 7). Seabreams (493) were fished in the first 2 weeks in the three ports, 470 of which in the first 3 days, mainly by trammel nets. The last recapture was recorded 193 days after the release. No significant regression was found between the mean number of recaptured seabreams and the days following the release (n = 20, p = 0.19, R = 0.30, b = 0.01, a = 0.66). sizes ranged between 9 and 12 cm (mean = 11 F 1.28) in the earlier period, while they reached 15.5 cm in the last recapture. There is a significant positive linear regression (n = 20, p < 0.001, R = 0.82, b = 0.02, a = 11.11) between recaptured seabream length and the number of days after releasing. 3.3. Predation on artificial reefs Thirty-four conger eels ranging 63– 125 cm TL (mean = 96.2 cm F 14.4) were captured at the release sites (12 in AM and 22 in BAL). Their guts contained a total number of 61
Fig. 7. Percent contribution of each source to tagged fish recapture. Total fishes recaptured = 570.
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tagged seabreams, which equals to 1.1% of the released individuals. CP1 value reached 59% in BAL, 50% in AM and 0% in TRA. CP2 and CP3 both resulted to be 50% in BAL and AM, since the only Diplodus preys found were tagged individuals. Each conger eel has taken on average 2.5 F 1.3 tagged seabreams in AM and 1.2 F 0.7 in BAL, 24 h after the releasing. Significant differences between sizes of conger eels were not found at the three locations ( F2,35 = 1.52; p = 0.2). On the other hand, the mean number of individuals of genus Diplodus preyed upon at the artificial reefs was significantly different to that of the control site ( F2,35 = 4.39; p < 0.05). 3.4. Behaviour of tagged seabreams on artificial reefs In the first days following fish release, tagged seabreams showed group behaviour. At the same time, they showed a high mobility around each single pyramid as well as between pyramids. Groups of about 30 fishes moved between the first and the second pyramid level, and no feeding activity was observed. No attempt of hiding in the boulders’ holes or crevices was recorded in the presence of predators. After about 1 month, small groups of three or four tagged fish were observed, together with other species such as Diplodus vulgaris or D. annularis, while moving, foraging and hiding among the artificial reefs boulders.
4. Discussion Despite the presence of wild specimens of the white seabream have constantly been reported for artificial reef in the Gulf of Castellammare (D’Anna and Badalamenti, 2000), tagged seabreams left the reef rather early to move towards the coast. The same behaviour was reported by Sanchez-Lamadrid (1998, 2002) with the gilthead seabream Spaurus aurata tagged and released on artificial reefs in the Gulf of Cadice (SE Spain). Most likely leaving the artificial reefs is not due to the type of substratum, or to other features of the habitat, but to a peculiar behaviour of individuals reared in captivity. Given the ecological features of the white sea bream (Macpherson, 1998; Harmelin-Vivien et al., 1995; Sala and Ballestoros, 1997; Vigliola and Harmelin-Vivien, 2001), in the Castellammare del Golfo AR system, food and shelter at least should not be limited to the species (Badalamenti et al., 1992; Pepe et al., 1996, 1998; Relini, 2000; Tumbiolo et al., 1997). Many authors believe that farmed individuals, once in the open sea, are not able to perceive environmental stimuli useful for their settlement and they are not able to exploit available food resources (Olla et al., 1994). This phenomenon, referred to as ‘‘behavioural deficit’’, can depend on the long period of time spent in captivity, where individuals do not experience different habitats and substrata, but where they live in big groups within containers without refugia. Furthermore, farmed individuals do not experience the search for food and the hunt for live prey, and they do not know their predators. Observations made in the experiment run in the Gulf of Castellammare highlight that the fishes in the first days after the release tend to show group behaviour (Kudoh et al., 1999), they do not search for refugia in reef holes or crevices, they do not forage, and they are not afraid of potential predators. These results can be partially attributed to behavioural deficit and to the
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gregarious habit of the juveniles of the species (Macpherson, 1998). It is clear that such behaviours might have negative effects on the survival of released individuals and this might compromise the success of the restocking experiment. 4.1. Preference for coastal habitats The decreasing number of seabreams over the coastal habitats through time, showed by the increasingly rarer sightings and recaptures, is likely due to mortality (natural or by fishing). However, it could also be attributed to an ontogenetic migration towards other microhabitats at greater depths as the fish grows (Biagi et al., 1997; Harmelin-Vivien et al., 1995; Macpherson, 1998). At the beginning, abundance was higher on the artificial reefs and in the harbours, where the largest individuals tended to concentrate. In the intermediate period, the higher number of seabreams was recorded around breakwaters, once again a habitat characterised by artificial substrata. In artificial substrates, fish mean size has constantly increased through time, while no significant increase was found in natural habitats. Such preference for coastal artificial habitats could be due to a search for adjacent shallower substrates. Breakwaters, as well as harbours, resulted to be particularly suitable for the settlement and growth of tagged fishes. Refugia availability, such as thousands of holes and crevices of different dimensions, shallow and sheltered waters, mixed bottoms and wild individuals of the same species might be the features that have made breakwater reefs a suitable environment for tagged seabreams. These findings are supported by some studies carried out on wild white seabream (Biagi et al., 1997; Harmelin-Vivien et al., 1995; Macpherson, 1998). These authors confirmed habitat selection in relationship to the early stages of the life cycle in this species. 4.2. Mortality causes: predation and fishing Gut contents analysis of predators caught in the release areas 2 days after fish release highlighted that in only one night about 1% of tagged fish was predated. Captured conger eels had eaten exclusively tagged seabreams, despite wild specimens of the genus Diplodus were present on average at each pyramid of the AR system (D’Anna, unpublished data). Other species of Diplodus were not found in the guts of captured conger eels at the control site. Probably, the high concentration of tagged seabreams on the pyramids, the incapability of recognising predators and the increased visibility created by the presence of the tag increased attraction by predators. Although a more specific experiment, with more spatial replicates, would have provided more robust data, the results confirm that in the days following the release, predation can represent an important cause of mortality. Even if the farming techniques of marine species have made important progresses, issues linked to the behaviour and learning capacity of captive individuals have not been fully developed (Brown and Laland, 2001; Howell and Baynes, 1993; Olla et al., 1994; Olla and Davis, 1989). Some behavioural deficits could maybe be reduced by a pre-acclimatisation period before the release (Griffin et al., 2000; Howell, 1994). Professional fishing has been a primary source of mortality, especially during the first days after releasing, while recreational fishing had a minor impact. Captures, concentrated
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in the first 3 days, have occurred mainly during seabream migration from the artificial reefs towards coastal habitats. High mortalities of released fish, during the first days, occur as fish are not totally adapted to the new habitat (Sanchez-Lamadrid, 2002). The presence of the tag has probably increased the chance for the fish to get entrapped in trammel nets (Nielsen, 1992). Recapture decrease through time could be due to the spreading of fishes along the coast, and to the development of a behaviour increasingly similar to that of wild individuals, characterised by the use of refugia and the formation of smaller groups compared to those observed at the beginning on artificial reefs.
5. Conclusion This paper refers to the first experience of the white sea bream enhancement, and leads to understand some aspects related to the release of farmed fish into the open sea. It also gives possible answers to questions that might arise in this kind of experience. The monitoring carried out using direct (visual census and sightings) and indirect (recaptures) methods has allowed to clarify some aspects which were previously difficult to describe and quantify or even left unconsidered during restocking experiments (Bohnsack, 1996). In particular, new knowledge has been acquired about mortality causes and diffusion patterns through coastal habitats. These aspects represent important factors in the success of marine ranching experiments. The results obtained give some suggestions for the management of initiatives based on farmed fish releasing. Among such suggestions, there is the need of a pre-acclimatisation stage for the fishes prior to their release in order to allow an easier adaptation to the wild conditions. At the same time, there is the need to limit fishing activities around releasing areas in the first days following fish release.
Acknowledgements We wish to thank the ‘‘Consorzio Golfo di Castellammare’’ and the ‘‘Ittica Mediterranea’’ staff for the collaboration during the rearing and releasing phases of fishes. We are grateful to Ms. M. Coppola, Mr. G. Di Stefano, Dr. C. De Cordova and Dr. P. Pepe for their help in field and in lab. This work was funded by the Ministero Politiche Agricole e Forestali (Mi.P.A.F., Italy). We are also grateful to the anonymous referees for their precious suggestions and comments.
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Releasing of hatchery-reared juveniles of the white seabream Diplodus sargus (L., 1758) in the Gulf of Castellammare artificial reef area (NW Sicily) G. D’Anna *, V.M. Giacalone, F. Badalamenti, C. Pipitone CNR-IRMA, Laboratorio di Biologia Marina, via Giovanni da Verrazzano 17, 91014 Castellammare del Golfo (TP), Italy Received 21 February 2003; received in revised form 9 October 2003; accepted 15 October 2003
Abstract A pilot experiment of marine ranching using hatchery-reared juveniles of white seabream, Diplodus sargus, was made in the Gulf of Castellammare (NW Sicily). The research aimed at evaluating (i) if artificial reefs are suitable for the settlement of reared young seabreams, (ii) what are the main causes of mortality and (iii) the growth rate of released fishes in the open sea. A total of 6930 tagged cultured juvenile white seabreams (305 days old) were released in an artificial reefs (AR) area. Underwater visual census, sightings and recaptures were used as a source of data for estimating abundance and size of released fishes. The survey lasted 15 months and was carried out in artificial (AR, breakwaters and harbours) and natural (river mouths, rocky bottoms and Posidonia oceanica meadows) coastal habitats of the Gulf. A few days after the release, more than 90% of the tagged seabreams left AR and moved mainly towards harbours and breakwaters, which resulted to be particularly suitable for their settlement and growth. The recapture was 8.2% of the released stock. During the first days after releasing, the main ascertained sources of mortality were professional fishing (6.7%) and predation by conger eel, Conger conger (1.1%). A behavioural deficit of the reared seabreams in the use of refugia and food was observed in the initial period following the release. The results obtained provide some management suggestion for the feasibility of marine ranching initiatives involving hatchery-reared fishes. D 2004 Elsevier B.V. All rights reserved. Keywords: Marine ranching; Hatchery-reared fish; Released fish; Diplodus sargus; Artificial substrata; Mediterranean
* Corresponding author. E-mail address: [email protected] (G. D’Anna). 0044-8486/$ - see front matter D 2004 Elsevier B.V. All rights reserved. doi:10.1016/j.aquaculture.2003.10.024
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1. Introduction Stock enhancement by hatchery-reared species goes back to the mid-19th century (Howell et al., 1999; Moring, 1986), and it was followed by the growing interest of industry, market and public authorities (Svasand et al., 2000) that it is now flourishing in many areas, particularly in Japan (Fushimi, 2001; Masuda and Tsukamoto, 1998). Nonetheless, most of the hatchery-based release programmes for the enhancement of wild stocks have failed (Bohnsack, 1996), the exceptions being the Japanese experiences (Honma, 1993; Matsuoka, 1989) and the releasing occurred in circumscribed habitats (e.g., coastal lagoons, fiords, estuaries, etc.) (McEachron et al., 1995). Failure has generally been attributed to the releasing at inappropriate habitats and times (Bohnsack, 1996), to the little knowledge on the biology and ecology of released species (Masuda and Tsukamoto, 1998; Travis et al., 1998) and to the production at hatchery of genetically, physiologically and behaviourally inferior individuals (Bohnsack, 1996; Munro and Bell, 1997). Hatchery-raised fish ends up with behavioural deficit (Olla et al., 1994) including the lack of effective anti-predatory and foraging strategies, which in turn could be responsible of the high mortality rate after releasing (Brown and Laland, 2001; Griffin et al., 2000). Only recently marine ranching, a type of stock enhancement aimed at keeping released cultured juvenile fish in coastal waters without cages has acknowledged for some intrinsic behaviour of the released species (e.g., Kuwada et al., 2000). In the Gulf of Castellammare (NW Sicily), several attempts have been made since the mid-1980s by the Sicilian Regional Government in order to rebuild the severely depleted demersal stocks (Whitmarsh et al., 2002). These initiatives included the deployment of a large artificial reef (AR) system of about 20 000 m3 (Badalamenti et al., 2000) and the establishment of a 20 000-ha fishery reserve (Pipitone et al., 2000). Moreover, a project involving a massive release of reared seabreams on artificial reefs has recently been planned (but not yet implemented) by a local Consortium that aggregates the five coastal towns in the Gulf. Since these initiatives have been set, soft bottom benthic and nektobenthic fish biomass has increased (Pipitone et al., 2000), while rocky bottom fishes, on both natural and artificial substrates, did not show a similar trend and remained almost constant in the period between 1990 and 1998 (D’Anna et al., 2001). Such species as the seabreams Diplodus sargus and D. vulgaris, that are characteristic of the Mediterranean rocky infralittoral fish assemblage (Sala and Ballestoros, 1997), were expected to increase following the AR deployment; they were found instead with little numbers (Badalamenti et al., 2000), although food (Badalamenti et al., 1992; Pepe et al., 1996, 1998; Tumbiolo et al., 1997) and shelter (Relini, 2000) were not limited at the AR and surrounding areas. The white seabream, D. sargus is a commercially exploited fish that gains a high market price in the Mediterranean area (Harmelin-Vivien et al., 1995), whose catches have declined in the last decade (FAO, 2002). It is targeted by small-scale and sport fisheries (Reina et al., 1994). Its biology and ecology are well known (Biagi et al., 1998; GarciaRubies and Macpherson, 1995; Gordoa and Moli, 1997; Harmelin, 1987; Harmelin-Vivien et al., 1995; Macpherson, 1998; Macpherson et al., 1997; Planes et al., 1999; Rosecchi, 1987; Vigliola and Harmelin-Vivien, 2001). This species is also successfully bred (Mazzola et al., 1985) and reared up to the age of about 1 year, before its growth rate
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slows down making the rearing process inappropriate for intensive aquaculture as well as economically unprofitable (Abellan et al., 1994). This paper reports the results of a marine ranching experiment aimed at providing baseline data for the above-mentioned Consortium release plan, within a more general management framework of development of the artisanal fishery in the artificial reef area. In particular, the research had the following objectives: (i) evaluating if artificial reefs are suitable for the settlement of hatchery-reared young seabreams, (ii) what are the main causes of mortality, and (iii) assessing the growth rate of released fishes.
2. Materials and methods 2.1. Study site The Gulf of Castellammare is characterised by cliffs on its sides and by shallow sandy shores in the middle, with patches of rocky bottom and Posidonia oceanica, and by the presence of stream and river mouths. In addition, in the Gulf, there are several artificial habitats, represented by harbour areas and breakwater reefs located at 20 –30 m from the coast, and by the submersed artificial reef system further offshore. The artificial reef area, chosen for releasing the seabreams, is arranged in pyramids, each made of 14 concrete boulders of 8 m3 displaced on three levels, located in two sites: Alcamo Marina (AM) and Balestrate (BAL) (Fig. 1). 2.2. Tagging and releasing The ‘‘Ittica Mediterranea’’ fish farm of Petrosino (Trapani) has reared a special batch of seabreams for this experiment, starting from a parent stock caught in the Gulf. Genetic tests have demonstrated the compatibility between the reared batch and the wild population (D’Anna and Badalamenti, 2000). The seabreams were tagged using dart style tags (T-Bar AFD-68B FF, made by ‘‘Floy Tags’’) (Giacalone et al., in press), following the procedure suggested by Parker et al., 1998. In March 1999, 7284 305-day-old seabreams were tagged. The mean total length (TL) was 11.50 F 1.05 cm and the mean weight was 32 F 9.9. During tagging operations, 345 fish died (4.5% of the total number), while 9 died during transportation from the farm to the port of Castellammare del Golfo. A total number of 6930 fish were released, of which 5300 over 16 pyramids at AM and 1630 over 5 pyramids at BAL, with an average number of 330 fish per pyramid. The releasing was done using cages built on purpose to:
reduce transport stress; release fishes underwater as close as possible to the pyramids, without the presence of divers; limit releasing costs as much as possible. Cages, made with a PVC structure and a plastic net, were cylindrical with a volume of about 550 l (Fig. 2), and contained 330 fish on average. Each cage was transported to the
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Fig. 1. Map of the Gulf of Castellammare with tagged seabreams spotting sites. AM = artificial reef at Alcamo Marina; BAL = artificial reef at Balestrate; E = harbours; *= river mouths with rock and sand; z = breakwater reefs; = rock mixed with P. oceanica.
Fig. 2. Opening procedure of the cage used for fish release.
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releasing site within a tank filled with water. Cages were ballasted and provided with a remotely controlled opening mechanism. The opening of the cage was carried out after a few min acclimatisation period on the seabed (Fig. 2). 2.3. Data collection and sampling techniques Data collected by visual census, sightings and recapture were recorded for 15 months after releasing the fish (from March 1999 to May 2000). This time was divided into three periods: P1 (initial, within 1 month from releasing), P2 (intermediate, from the second to the forth month after releasing) and P3 (final, from the fifth to the fifteenth month after releasing). 2.3.1. Visual census on the artificial reefs and the coastal habitats Underwater visual census technique was performed over the three periods on five different habitats including: artificial reefs (AR); river mouths with rock and sand (RM); breakwater reefs (BWR); harbours (Harb.); rocky bottom mixed with P. oceanica (R-P.o.). Censuses were performed by two SCUBA divers who registered in situ each observation on a polyester pad. In each census, tagged seabream abundance (N) and total length (TL) were recorded. N was gathered using class intervals of abundance while TL was estimated to the nearest 1 cm (Harmelin-Vivien et al., 1985; Bortone et al., 1991). Visual census was carried out using random linear transects and point count methods (Bortone et al., 1989): each count lasted about 20 min and the volume of water considered was about 225 m3. A more detailed description of visual census techniques, in both natural and artificial habitats, is reported by D’Anna et al. (1999). 2.3.2. Sightings and recapture Sightings and recaptures by recreational and professional fishermen were used to estimate dispersion patterns and fishing mortality of tagged seabreams. In the first 2 weeks after the release, a daily census of the fish caught by professional and recreational fishing was done in the harbours of Castellammare, Balestrate and Trappeto (Fig. 1), to evaluate the amount of recapture. Moreover, a questionnaire for data collection on sightings and recapture was distributed among fishermen of the Gulf. Fields to be filled included: date, location, type of habitat, number of tagged fish and, where possible, an estimate of their size. If a tagged fish was caught, fishermen were asked to hand over the fish, or at least the tag. An information sheet was posted in the five ports of the Gulf. 2.3.3. Predation on the artificial reefs Based on previous knowledge of the fish assemblage in the AR area (D’Anna et al., 1994), the conger eel, Conger conger, was deemed to be the main fish predator. A longline with 200 hooks was used to catch conger eels at AM and BAL 24 h after the releasing of seabreams. This was done only once to quantify the mortality of tagged seabreams after releasing due to conger eel predation. The longline was set at sunset and hauled at dawn. The same operation was carried out at a control site without marked fish (Trappeto, TRA) (Fig. 1), to test possible differences in the number of predated
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seabreams. Captured conger eels were measured, weighted and eviscerated and their gut content were analysed. Tagged seabreams found in the guts were included among recaptured specimens. 2.3.4. Behaviour of tagged seabreams on artificial reefs Video recording and underwater photography, together with observations made during visual census, allowed to gain qualitative information on the spatial distribution as well as on the behaviour of tagged seabreams on the artificial reefs during the three periods. 2.4. Data analysis Mean abundance values of tagged seabreams taken from the above-mentioned coastal habitats were tested with a three-way analysis of variance (Underwood, 1997) including: type of habitat (five levels: ar, RM, BWR, Harb. and R-P.o.), Orthogonal and fixed; period (p) (three levels: P1, P2 and P3), orthogonal and fixed; date (two levels: 1 and 2), random and nested within the interaction between habitat and period. To analyse differences in the mean size of tagged seabreams through time and in different habitats, a two-way ANOVA was applied between type of habitat and period (P) both fixed and orthogonal. The analysis was performed on an unbalanced number of replicates since all the censed specimens were used. A sample of 36 conger eel stomachs, 12 per each location, was randomly chosen from the whole catch. A one-way ANOVA with location as a fixed factor (three levels: AM, BAL and TRA) was performed on the number of individuals of Diplodus spp. as a response variable. Analyses of variance were carried out using ‘‘Gmav5’’ software after checking the homogeneity of variance with the Cochran test. When differences were found, a-posteriori comparisons were made using the Student –Newman –Keuls test (Underwood, 1997). On the total number of seabreams censed and sighted, size class frequency distribution was calculated for each habitat over the three different periods. Size frequency distributions were compared with the Kolmogorov – Smirnov (K – S) test, and linear regressions between the days following seabream release and the mean abundance and size were used to examine their trends through time.
3. Results 3.1. Visual census on artificial reefs and coastal habitats 3.1.1. Abundance and size of tagged seabream on artificial reefs A total of 628 tagged seabreams was counted in the artificial reef areas over the whole study period. The highest abundance in the artificial reef area was registered 7 days after fish release with a mean value of 47.81 F 12.4 for each pyramid and an estimate of 1004 individuals. The last tagged seabreams were observed 218 and 154 days after the release in AM and BA, respectively (Table 1).
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Table 1 Abundance of tagged seabreams on artificial reefs after their release, as drawn from visual census survey Date
Days
Np
Nm
S.E.
Nt
N%
12/03/99 16/03/99 08/04/99 03/05/99 13/05/99 13/06/99 16/07/99 10/08/99 14/09/99 13/10/99 30/12/99 29/01/00 29/02/00 30/03/00 28/04/00
3 7 30 55 65 96 129 154 189 218 295 326 357 386 416
7 8 7 7 8 8 10 8 10 9 7 7 8 8 8
27.86 47.81 2.71 1.86 1.81 0.00 0.20 0.06 0.00 0.17 0.00 0.00 0.00 0.00 0.00
4.96 12.39 1.02 0.53 0.88 0.00 0.13 0.06 0.00 0.17 0.00 0.00 0.00 0.00 0.00
585 1004 57 39 38 0 4 1 0 4 0 0 0 0 0
8.44 14.49 0.82 0.56 0.55 0.00 0.06 0.02 0.00 0.05 0.00 0.00 0.00 0.00 0.00
Np = number of censed pyramids; Nm = mean number of tagged seabreams per pyramid; S.E. = standard error; Nt = total abundance of tagged seabreams present on artificial reefs; N% = percentage of tagged seabreams in relation to total number of released fish.
The mean size of all counted seabreams at AM and BAL through time is shown in Fig. 3. There were significant regressions of time against abundance (AM, p < 0.01; BAL p < 0.05) and size (AM and BAL, p < 0.001): slopes were negative for abundance (AM, n = 22, R = 0.56, b = 0.12, a = 14.70; BAL, n = 16 R = 0.57 b = 0.48, a = 43.69) and positive for seabream size (AM, n = 22, R = 0.93, b = 0.028, a = 11.56; BAL, n = 16 R = 0.81 b = 0.03, a = 11.29). 3.1.2. Abundance and size of tagged seabream over the coastal habitats The ANOVA showed significant differences in the number of tagged individuals per habitat, period and for the interaction between habitat and period (Table 2). In P1, there
Fig. 3. Mean total length (TL) with standard deviation (S.D.) of tagged seabreams on artificial reefs after fish release. n = number of observations.
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Table 2 ANOVA on number of tagged seabreams censed in five habitats and three periods Source of variation
Abundance of tagged seabreams df
MS
F
Habitat (H) Period (P) Date (H P) HP Residuals Total Pooleda Transformation Cochran’s C-test
4 2 15 8 60 89 75 Ln(X + 1)ns C = 0.1655
5.01 12.29 1.02 3.87 0.50
8.24*** 20.18*** 1.69ns 6.36***
SNK test
Habitat
Period
Period P1 P2 P3
Harb. = AR>RM = BWR = R-P.o. BWR>AR = RM = Harb. = R-P.o. RM = BWR = Harb. = R-P.o.>AR
Habitat AR RM BWR Harb. R.-P.o.
0.6091
P1>P2 = P3 ns ns P1>P2 = P3 ns
ns = not significant. For abbreviations, see text. a Pooled term = residuals+(H P). *** =p < 0.001.
were more seabreams in Harb. and AR (Fig. 4). In P2, there was a higher number of seabreams on BWR than in any other habitat (which are all equal among each other). In P3, all habitats appeared with the same number of seabreams, with the exception of AR,
Fig. 4. Mean number (N) with standard error (S.E.) of tagged seabreams in different habitats over the three periods (P1, P2, P3). n = number of observations. For abbreviations, see text.
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Table 3 ANOVA on the size of tagged seabreams censed in five habitats and three periods Source of variation
The length of tagged seabream df
MS
F
Period (P) Habitat (H) HP Residuals Total Cochran’s C-test
2 4 8 214 228 C = 0.31ns
261.27 10.91 10.74
113.8*** 4.7*** 4.6***
SNK test
Habitat
Period
Period P1 P2 P3
AR = BWR = Harb.>RM = R-P.o. ns ns
Habitat AR RM BWR Harb. R.-P.o.
P3>P2 = P1 ns P3>P2 = P1 P3>P2 = P1 ns
ns = not significant. For abbreviations, see text. *** = p < 0.001.
which had the lowest value. On the whole, the number of seabreams in Harb. and AR was higher in P1 than in P2 and P3, while for the other habitats, there was no difference between the three periods (Fig. 4). Significant differences were found between average lengths among periods, habitats and the interaction habitat – period (Table 3). In P1, the mean length was significantly higher in Harb., BWR and AR, in comparison to RM and R-P.o. (Fig. 5). Significant
Fig. 5. Mean total length (TL) and standard deviation (S.D.) of tagged seabreams in different habitats over the three periods. n = number of observations. For abbreviations see text.
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Fig. 6. Size frequency of tagged seabream sighted in different habitats over the three periods. n = number of observations. For abbreviations, see text.
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differences in size were not recorded among the habitats in P2 and P3. In AR, BWR and Harb., the mean length in P3 was higher than P1 and P2. For what concerns RM and RP.o., no significant differences were found. 3.2. Sightings and recapture of tagged seabreams 3.2.1. Sightings From March 1999 to May 2000, a total number of 2100 tagged seabreams were observed along the coast, at distances between 0.8 and 17 km from the artificial reef (Fig. 1). There is a significant negative regression (n = 13, p < 0.001, R = 0.76, b = 0.02, a = 12.59) between the mean number of sighted tagged fishes and the days after release. An average number of 18 individuals per sighting was recorded in March 1999, and a minimum of 1 fish in May 2000. The last sighting was reported 463 days after fish release. Mean TL of the sighted individuals oscillated from 12.2 F 1.3 cm (May 1999) to 17.8 F 1.5 cm (May 2000). There is a significant positive linear relationships (n = 13, p < 0.001, R = 0.82, b = 0.01, a = 13.03) between the length of sighted seabreams and the number of days after releasing. Size frequency distribution (including also seabreams
Table 4 K – S test results on the size frequency of tagged seabreams between five habitats in three period
n = number of measured seabreams; ns = not significant. For abbreviations, see text. *p < 0.05. **p < 0.01. ***p < 0.001.
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censed in AR) in P1 shows that smaller fish were located at R-P.o. and RM, while bigger fish tended to be found in Harb. and BWR (Fig. 6). In P2, there was an homogeneous distribution of the sizes in all the habitats. In P3, there were few individuals, the bigger ones of which were found in BWR, R-P.o. and in RM. K – S test revealed significant differences in size frequency distribution among all habitats in P1 and P2. Significant differences were reported among Harb., RM, BWR and R-P.o. in P3 (Table 4). 3.2.2. Recapture A total of 570 individuals were recaptured, which makes up to the 8.2% of those released. Professional fishing contributed the most to recapture (82%), while recreational fishing contributed to the 5%. Analysis of the predator’s diet reported another 10% of recaptured individuals and the remaining 3% falls into the unknown recapture methods (Fig. 7). Seabreams (493) were fished in the first 2 weeks in the three ports, 470 of which in the first 3 days, mainly by trammel nets. The last recapture was recorded 193 days after the release. No significant regression was found between the mean number of recaptured seabreams and the days following the release (n = 20, p = 0.19, R = 0.30, b = 0.01, a = 0.66). sizes ranged between 9 and 12 cm (mean = 11 F 1.28) in the earlier period, while they reached 15.5 cm in the last recapture. There is a significant positive linear regression (n = 20, p < 0.001, R = 0.82, b = 0.02, a = 11.11) between recaptured seabream length and the number of days after releasing. 3.3. Predation on artificial reefs Thirty-four conger eels ranging 63– 125 cm TL (mean = 96.2 cm F 14.4) were captured at the release sites (12 in AM and 22 in BAL). Their guts contained a total number of 61
Fig. 7. Percent contribution of each source to tagged fish recapture. Total fishes recaptured = 570.
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tagged seabreams, which equals to 1.1% of the released individuals. CP1 value reached 59% in BAL, 50% in AM and 0% in TRA. CP2 and CP3 both resulted to be 50% in BAL and AM, since the only Diplodus preys found were tagged individuals. Each conger eel has taken on average 2.5 F 1.3 tagged seabreams in AM and 1.2 F 0.7 in BAL, 24 h after the releasing. Significant differences between sizes of conger eels were not found at the three locations ( F2,35 = 1.52; p = 0.2). On the other hand, the mean number of individuals of genus Diplodus preyed upon at the artificial reefs was significantly different to that of the control site ( F2,35 = 4.39; p < 0.05). 3.4. Behaviour of tagged seabreams on artificial reefs In the first days following fish release, tagged seabreams showed group behaviour. At the same time, they showed a high mobility around each single pyramid as well as between pyramids. Groups of about 30 fishes moved between the first and the second pyramid level, and no feeding activity was observed. No attempt of hiding in the boulders’ holes or crevices was recorded in the presence of predators. After about 1 month, small groups of three or four tagged fish were observed, together with other species such as Diplodus vulgaris or D. annularis, while moving, foraging and hiding among the artificial reefs boulders.
4. Discussion Despite the presence of wild specimens of the white seabream have constantly been reported for artificial reef in the Gulf of Castellammare (D’Anna and Badalamenti, 2000), tagged seabreams left the reef rather early to move towards the coast. The same behaviour was reported by Sanchez-Lamadrid (1998, 2002) with the gilthead seabream Spaurus aurata tagged and released on artificial reefs in the Gulf of Cadice (SE Spain). Most likely leaving the artificial reefs is not due to the type of substratum, or to other features of the habitat, but to a peculiar behaviour of individuals reared in captivity. Given the ecological features of the white sea bream (Macpherson, 1998; Harmelin-Vivien et al., 1995; Sala and Ballestoros, 1997; Vigliola and Harmelin-Vivien, 2001), in the Castellammare del Golfo AR system, food and shelter at least should not be limited to the species (Badalamenti et al., 1992; Pepe et al., 1996, 1998; Relini, 2000; Tumbiolo et al., 1997). Many authors believe that farmed individuals, once in the open sea, are not able to perceive environmental stimuli useful for their settlement and they are not able to exploit available food resources (Olla et al., 1994). This phenomenon, referred to as ‘‘behavioural deficit’’, can depend on the long period of time spent in captivity, where individuals do not experience different habitats and substrata, but where they live in big groups within containers without refugia. Furthermore, farmed individuals do not experience the search for food and the hunt for live prey, and they do not know their predators. Observations made in the experiment run in the Gulf of Castellammare highlight that the fishes in the first days after the release tend to show group behaviour (Kudoh et al., 1999), they do not search for refugia in reef holes or crevices, they do not forage, and they are not afraid of potential predators. These results can be partially attributed to behavioural deficit and to the
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gregarious habit of the juveniles of the species (Macpherson, 1998). It is clear that such behaviours might have negative effects on the survival of released individuals and this might compromise the success of the restocking experiment. 4.1. Preference for coastal habitats The decreasing number of seabreams over the coastal habitats through time, showed by the increasingly rarer sightings and recaptures, is likely due to mortality (natural or by fishing). However, it could also be attributed to an ontogenetic migration towards other microhabitats at greater depths as the fish grows (Biagi et al., 1997; Harmelin-Vivien et al., 1995; Macpherson, 1998). At the beginning, abundance was higher on the artificial reefs and in the harbours, where the largest individuals tended to concentrate. In the intermediate period, the higher number of seabreams was recorded around breakwaters, once again a habitat characterised by artificial substrata. In artificial substrates, fish mean size has constantly increased through time, while no significant increase was found in natural habitats. Such preference for coastal artificial habitats could be due to a search for adjacent shallower substrates. Breakwaters, as well as harbours, resulted to be particularly suitable for the settlement and growth of tagged fishes. Refugia availability, such as thousands of holes and crevices of different dimensions, shallow and sheltered waters, mixed bottoms and wild individuals of the same species might be the features that have made breakwater reefs a suitable environment for tagged seabreams. These findings are supported by some studies carried out on wild white seabream (Biagi et al., 1997; Harmelin-Vivien et al., 1995; Macpherson, 1998). These authors confirmed habitat selection in relationship to the early stages of the life cycle in this species. 4.2. Mortality causes: predation and fishing Gut contents analysis of predators caught in the release areas 2 days after fish release highlighted that in only one night about 1% of tagged fish was predated. Captured conger eels had eaten exclusively tagged seabreams, despite wild specimens of the genus Diplodus were present on average at each pyramid of the AR system (D’Anna, unpublished data). Other species of Diplodus were not found in the guts of captured conger eels at the control site. Probably, the high concentration of tagged seabreams on the pyramids, the incapability of recognising predators and the increased visibility created by the presence of the tag increased attraction by predators. Although a more specific experiment, with more spatial replicates, would have provided more robust data, the results confirm that in the days following the release, predation can represent an important cause of mortality. Even if the farming techniques of marine species have made important progresses, issues linked to the behaviour and learning capacity of captive individuals have not been fully developed (Brown and Laland, 2001; Howell and Baynes, 1993; Olla et al., 1994; Olla and Davis, 1989). Some behavioural deficits could maybe be reduced by a pre-acclimatisation period before the release (Griffin et al., 2000; Howell, 1994). Professional fishing has been a primary source of mortality, especially during the first days after releasing, while recreational fishing had a minor impact. Captures, concentrated
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in the first 3 days, have occurred mainly during seabream migration from the artificial reefs towards coastal habitats. High mortalities of released fish, during the first days, occur as fish are not totally adapted to the new habitat (Sanchez-Lamadrid, 2002). The presence of the tag has probably increased the chance for the fish to get entrapped in trammel nets (Nielsen, 1992). Recapture decrease through time could be due to the spreading of fishes along the coast, and to the development of a behaviour increasingly similar to that of wild individuals, characterised by the use of refugia and the formation of smaller groups compared to those observed at the beginning on artificial reefs.
5. Conclusion This paper refers to the first experience of the white sea bream enhancement, and leads to understand some aspects related to the release of farmed fish into the open sea. It also gives possible answers to questions that might arise in this kind of experience. The monitoring carried out using direct (visual census and sightings) and indirect (recaptures) methods has allowed to clarify some aspects which were previously difficult to describe and quantify or even left unconsidered during restocking experiments (Bohnsack, 1996). In particular, new knowledge has been acquired about mortality causes and diffusion patterns through coastal habitats. These aspects represent important factors in the success of marine ranching experiments. The results obtained give some suggestions for the management of initiatives based on farmed fish releasing. Among such suggestions, there is the need of a pre-acclimatisation stage for the fishes prior to their release in order to allow an easier adaptation to the wild conditions. At the same time, there is the need to limit fishing activities around releasing areas in the first days following fish release.
Acknowledgements We wish to thank the ‘‘Consorzio Golfo di Castellammare’’ and the ‘‘Ittica Mediterranea’’ staff for the collaboration during the rearing and releasing phases of fishes. We are grateful to Ms. M. Coppola, Mr. G. Di Stefano, Dr. C. De Cordova and Dr. P. Pepe for their help in field and in lab. This work was funded by the Ministero Politiche Agricole e Forestali (Mi.P.A.F., Italy). We are also grateful to the anonymous referees for their precious suggestions and comments.
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