Reburial time and indirect mortality of Spisula ... - Site de utilizadores

Fisheries Research 59 (2002) 247–257

Short communication

Reburial time and indirect mortality of Spisula solida clams caused by dredging L. Chıćharoa,*, M. Chıćharoa, M. Gasparb, J. Regalaa, F. Alvesa a

Faculdade de Cieˆncias do Mar e do Ambiente (FCMA)-CCMAR, Centro de Cieˆncias do Mar, Universidade do Algarve, Campus de Gambelas, P-8000 810 Faro, Portugal b Instituto Portugueˆs de Investigaçaõ das Pescas e do Mar (IPIMAR), CRIPSul, Av. 5 de Outubro s/n, 8700 Olhaõ, Portugal Received 6 February 2001; received in revised form 6 December 2001; accepted 6 January 2002

Abstract Clam-dredging results in the exposure of Spisula solida individuals not caught by the dredge. Subsequent survival depends on clam damage, reburial time, and the time needed by predators to reach the impacted area. We analyse these variables and discuss the importance of predation on exposed S. solida caused by dredge fishing. Sampling was performed in July 2000 off the southern coast of Portugal, at Vilamoura, a traditional S. solida sandy fishing ground. We compared the time needed for S. solida individuals to rebury themselves, relative to the abundance of potential predators. Bivalves collected by divers were placed on the seabed, and the times required for reburial were measured. These were compared with the times needed for reburial of the clams exposed by dredge impact. At each of three dredge tracks, we analysed the number of predators that entered three equal quadrats (0.0250 m2) per minute. These results were compared with a non-affected control area. Impact caused by the fishing dredge significantly increases the number of exposed S. solida clams ðp < 0:05Þ and the abundance of potential predatory species ðp < 0:05Þ. The brittle star Ophiura texturata was the most abundant and first species to reach the dredge track (less than 3 min after dredge impact). Other species reaching the dredge track were Pomatochistus spp. (6 min after impact), Diogenes pugilator, and Nassarius reticulatus (both 9 min after impact). Although predators reached the impacted area while S. solida bivalves were still exposed, our results suggest that predation on the non-buried clams in the dredge track is not a major factor for subsequent indirect mortality of S. solida. # 2002 Elsevier Science B.V. All rights reserved. Keywords: Indirect mortality; Fishing impact; Reburial time; Spisula solida

1. Introduction The environmental effects of shellfish dredging area well documented (Caddy, 1968, 1973; Conner and Simon, 1979; Meyer et al., 1981; Hall et al., 1990; McLoughlin et al., 1991; Dare et al., 1993; Kaiser et al., 1998; Gilkinson et al., 1999). *

Corresponding author. Tel.: þ351-289-800-900; fax: þ351-289-818-353. E-mail address: [email protected] (L. Chıćharo).

In Portugal, fishing for bivalves has been an important commercial enterprise since 1969. Today, the industry targets the species Donax trunculus, Venus striatula, Pharus legumen, Ensis siliqua, and Spisula solida. Bivalves are caught with a dredge that can penetrate into the sediment for up to 50 cm, depending on target species and sediment type. Even if fishing efficiency is high, as for the Portuguese clam-dredge (Gaspar, 1996), some clams not retained by the dredge bag may also die as a consequence of the activity. The passage of the fishing gear across the

0165-7836/02/$ – see front matter # 2002 Elsevier Science B.V. All rights reserved. PII: S 0 1 6 5 - 7 8 3 6 ( 0 2 ) 0 0 0 1 2 - 7

248

L. Chıćharo et al. / Fisheries Research 59 (2002) 247–257

seabed leads to direct mortality and also to indirect mortality through subsequent predation. The extent of this additional mortality must be quantified if we are to calculate total mortality associated with the fishing (Kaiser and Spencer, 1995). Murawski and Serchuk (1989) observed variable survival rates among those clams returned to the seabed as ‘‘undersized’’, and thus providing potential food in the dredge track for scavengers and predators (Ramsay et al., 1998). The survival of non-damaged individuals may be related to the time they need to rebury. Exposed individuals are preferential targets for opportunistic invertebrate (Wassenberg and Hill, 1987) and fish predators (Kaiser and Spencer, 1994). It is reasonable to predict that predation on the clams that escape the dredging gear will increase with exposure time. However, this time is probably influenced by stress resulting from the impact of the passage of the dredge. Thus, the indirect mortality of the uncaught S. solida attributable to predation will depend on the relation between the time needed for reburial and the time available for predators to reach the impacted area. If the reburial time is longer than the time taken for the initiation of predation, then an expected important indirect mortality can be attributed to predation activity on the dredge track. If exposed clams rebury themselves before significant numbers of predators can reach the area, then indirect mortality due to predation will be negligible. The aims of this work were to analyse: (1) the impact of dredging on the exposed S. solida clams; (2) the impact of dredging on the abundance of potential predators; (3) the time needed for predators to reach the dredged area. These factors were analysed in relation to the ability of exposed S. solida individuals to rebury themselves, and for their implications to indirect mortality.

2. Methods 2.1. Study site The Algarve coast of Portugal extends from Cabo Sa˜ o Vicente in the west (88590 W), to the border with Spain in the east (78240 W). Currents on the continental shelf of Algarve are usually weak, with wind-caused

drift currents running along the shore from east to west, predominating over tidal currents to a depth of 30 m or more. Normally, current speeds are under 0.25 m/s, but during extreme conditions may reach 0.5 m/s or more (Fiu´ za, 1983). Water temperatures were 14–22 8C. The study took place off Vilamoura on a sandy fishing ground 8 m deep (Fig. 1). 2.2. Fishing gear used Bivalve dredges used on the south coast of Algarve are large, heavy, iron structures, with a 25 mm mesh net bag, a metal semicircle parallel bar grid and a toothed lower bar at the mouth. The mouth is 43 cm wide; bars are 2.3 cm apart, and the teeth are 34 cm long, acting as a rake when the dredge is dragged through the sediment. 2.3. Sampling strategy and laboratory procedures The in situ experiments were performed in July 2000. Three areas studied before dredging were control areas. Three independent sites were impacted by dredge, and within each site, three independent samples were taken. The sampling strategy focused on two main objectives: first, determination of the time taken for S. solida individuals to rebury; second, the time taken for predators to arrive. To measure the time needed for S. solida to rebury before there was any impact from fishing, divers carefully hand-collected three groups of 10 bivalves from the sediment. This procedure was done very gently to avoid stress on the clams. Immediately after collection, the clams were replaced on the seabed. Divers directly assessed the numbers of bivalves both reburied and exposed every 3 min for 30 min (this time was found to permit the reburial of almost all bivalves). To determine the impact of fishing activity on exposed S. solida clams, normal dredge fishing was performed and three 50 m dredge-tracks were created (approximately 1 min of towing). Divers already near the sea bottom immediately collected 10 exposed clams from each dredge track. These were all placed in an area of 1 m2 for ease of observation by the divers. The numbers of bivalves reburied and exposed were assessed every 3 min for 30 min. The numbers and level of damage of bivalves was recorded in situ as


249

Fig. 1. Map of the South Portugal (Algarve) coast, showing the sampling location: Vilamoura.

follows: level 1 (none or only slight damage)—bivalve intact; level 2 (medium damage)—small breakage of the shell; level 3 (severe damage)—more than twothirds of the shell broken. In a non-fished control area and to minimize the risk of predator avoidance, divers buried three square quadrats measuring 50 cm 50 cm into the sediment, so that the structure was invisible, but leaving each of the corners identifiable by a vertical marker. The numbers of predators that entered the quadrat marks were assessed for 30 min at 3 min intervals. Individuals re-entering the quadrat areas were counted only once. The fishing procedure was repeated three times. Immediately after passage of the dredging gear, divers repeated the same procedure described above for the non-fished control area. Highly mobile species such as fish or cuttlefish were identified in situ. Potential benthic predator macrofauna species were collected and brought to the laboratory for identification.

Predators were defined and counted as individuals with lengths at least twice that of the prey (S. solida: 20–25 mm). For characterisation of the area, sediment was analysed. Sediment samples were collected and in the laboratory any organic matter was eliminated using H2O2 (130 volumes). Sediment was then dried on a stove (WTB binder) at 608 for 24 h, and passed through 1/2f interval sieves comprising between 2f and 4f (equivalent to 4.0–0.063 mm), using stacked sieves (Retsch AS 200 basic) for 10 min. 2.4. Data analysis The effects of dredge and time on predator abundance and on the number of exposed bivalves were examined by a two-way ANOVA performed with Statistic V.5 software. Because the data lacked normal distribution and showed inhomogeneous variances ðp < 0:05Þ, they were log transformed. As more than


250

Fig. 2. Distribution of sediment grain size in the Vilamoura area (see Fig. 1 for details).

two comparisons were made, this analysis was followed by a Tukey test to compare means between times.

3. Results The study area was dominated by sediment grain size of 0.5 and 0.355 mm (Fig. 2). The number of exposed S. solida clams increased significantly ðp < 0:05Þ after dredge impact (Fig. 3, Table 1), Table 1 Summary of a two-way ANOVA, using a fixed effect for log number of exposed bivalves with nested designa Effect

d.f. effect

MS effect

d.f. error

MS error

F value

p-level

1b 2c

1 17

4.177 1.037

52 52

0.462 0.462

9.029 2.245

0.004* 0.001*

a

d.f.: degrees of freedom; MS: mean square. Before and after dredge. c Time. b

especially after 3 min of dredge impact according to Tukey testing (Fig. 4). All S. solida individuals from control areas were reburied 12 min after being exposed, while in the dredge impacted areas, more than 30 min were needed for all bivalves to rebury. Not only did more clams rebury during the period of observations, but they also reburied faster in the control areas. In these areas, 50% of the clams were completely reburied after 3 min, while in the dredge impacted areas this was increased to 9 min. By this time, all the clams in the control study had reburied. In the impacted area, 80% of the clams were reburied after 15 min, 90% after 24 min, and some of them never reburied during the study period. Thus, 50% of the clams that suffered the impact of dredging took 6 min longer to rebury than did the clams that had not suffered any impact (Fig. 5). Comparisons between the abundance of potential predators before (control) and after the fishing disturbance, measured 30 min after the beginning of the experiments, showed that significant differences


251

Fig. 3. Comparison between the number of exposed S. solida individuals, before and after the dredge impact (Std. Dev. is standard deviation of the mean).

Fig. 4. Changes in average numbers of exposed S. solida over the 30 min observation. Error bars are standard deviations. Numbers at each bar show the significant differences (s.d.) between times, results of a Tukey test ðp < 0:05Þ, which was carried out after ANOVA, with significant F values (Table 1).


252

Fig. 5. Cumulative percentages of reburied S. solida clams, before (control) and after the dredge impact, during the 30 min experiment.

occurred (p < 0:05: Table 2 and Fig. 6). In the control study, predator abundance was almost constant (5–6 individuals per square metre). Predator abundance on the dredge track started to increase 3 min after dredging (ranging from 6 to 21 individuals per square metre). During the following 27 min, average predator densities remained similar, with a minimum of 18 individuals per square metre (Fig. 7). The brittle star Ophiura texturata was the most abundant species that moved to the dredge tracks during the 30 min experiment (72–100% of the total potential predators observed). It was also the first species to reach the impacted area, increasing in density in the first minute after the passage of the gear. The presence of fishes (Pomatochistus spp.) was

Table 2 Summary of a two-way ANOVA, fixed effect for log number of predators with nested designa Effect

d.f. effect

MS effect

d.f. error

MS error

F value

p-level

1b 2c

1 19

53.153 4.611

160 160

1.023 1.023

51.961 4.503

0.001* 0.001*

a

d.f.: degrees of freedom; MS: mean square. Before and after dredge. c Time. b

observed 6 min after the passage of the gear, while the anomuran Diogenes pugilator and the gastropod Nassarius reticulatus were observed at 9 min (Fig. 8). The flatfish Solea solea, cuttlefish Sepia officinalis, mullet Chelon labrosus and an unidentified blenniid fish were also observed on dredge track areas. Our in situ observations revealed that the most damaged and/or exposed species due to dredging were the urchin Echinocardium cordatum and the brittle star Amphiura mediterranea. Infaunal polychaete species, the bivalves Mactra sp. and Callista chione, seastar Astropecten sp., and the gastropod Cymbium olla were affected. Damage to the fishing target species S. solida was, however, negligible. Less than 6% of the bivalves not caught on the dredge track were damaged, and less than 2% suffered severe damage. Most of the bivalve damage (94.2%) was classified as level 1 (none or slight damage) (Fig. 9). When comparing the time needed for the impacted clams to rebury themselves with the time needed for potential predators to reach the impacted area, at least 50% of the clams reburied themselves before the arrival of predators (Fig. 10). Moreover, potential predator abundance became more important. More than 50% of the total potential predators were counted after 12–15 min, when 40–20% of clams were still exposed.


253

Fig. 6. Comparison between the average abundance of potential predators (log transformed data) that reached the study areas before and after dredge impact.

Fig. 7. Change in the average of potential predators abundance (log transformed data) over the 30 min observation, before and after the dredge impact. Error bars are standard deviations. Numbers at each bar show s.d. between times, based on the results of Tukey tests ðp < 0:05Þ, which were done after the ANOVA, with significant F values (Table 2).

254


Fig. 8. Variations in the abundance of the potential predator species that reached the area after the dredge impact during the 30 min experiment.

Fig. 9. Percentage of damaged S. solida. The numbers and level of damage to bivalves were recorded in situ as follows: level 1 (none or slight damage)—bivalve intact; level 2 (medium damage)—small breakage of the shell; level 3 (severe damage)—more than two-thirds of the shell broken.


255

Fig. 10. Relation between the cumulative percentages of reburied S. solida and the abundance of potential predator species reaching the area after the dredge impact.

4. Discussion Studies have indicated that a variety of fishing gear, such as beam trawls (Bergman and Hup, 1992; Kaiser and Spencer, 1994), otter trawls (Van Dolah et al., 1987; Rumohr and Krost, 1991), and dredges (Van der Veer et al., 1985), can cause mortality of some epi- and infaunal benthic organisms. Although the direct effects of this activity on benthic communities appear obvious, and may cause large-scale alterations to predator populations (Kaiser et al., 1998), the magnitude of the effects has been very difficult to evaluate and has often been considered equivocal (Thrush et al., 1998). In our study, the impact of the dredge increased the time needed for S. solida individuals to rebury. Interestingly, Breum (1970) reported that S. subtruncata, a species with a depth distribution similar to S. solida, exhibited increased burrowing activity when disturbed by wave action. Disturbance to the sea bottom caused by dredging also affected the abundance of potential predators in the fishing area. These increased after the passage of the fishing gear, as was also observed by Meyer et al. (1981) and Kaiser and Spencer (1994). Kaiser et al. (1998) observed specific differences in aggregating behaviour between species of the same genera, Pagurus. In addition, Evans et al. (1996) reported rapid movement of

whelks (Buccinum undatum) towards animals damaged or killed by the impact of fishing. Ramsay et al. (1998) observed a significantly higher proportion of the predator seastar Asterias rubens after fishing. In our study, O. texturata was the most abundant and quickest species to reach the dredge track (less than 3 min). According to Feder (1981), O. texturata, a potential predator of meiofauna and small benthic macrofauna. Also, Pomatochistus spp., which reached the impacted area 6 min after impact, may prey effectively on exposed bivalves, according to Zander (1982) and Fitzhugh and Fleeger (1985). However, other species that appeared occasionally at the dredge track areas may be more importance to S. solida as predators, such as the flatfish S. solea (Molinero and Flos, 1991), cuttlefish S. officinalis (Najai and Ktari, 1979), and mullet C. labrosus (Gisbert et al., 1995). These species may also feed on fragile non-target species, such as E. cordatum, A. mediterranea or polychaetes, all damaged heavily by the passage of dredges. Because half of the clams exposed on the dredge track needed 9 min to rebury and 80% needed 15 min, when the last predator species arrived at the dredge track there were still 20–40% of the clams exposed. This predatory impact was smaller than expected, due to the high selectivity of the dredge (Gaspar, 1996). Thus, less than 5% of the bivalves showed medium or severe damage.

256


The impact of predators will probably be greater during the early post-larval period, when bivalves are much smaller and more fragile. In fact, D. pugilator and N. reticulatus, species that occurred in the impacted area 9 min after impact, are described as scavengers or predators upon meiofauna (Ramsay et al., 1996; Volvenko, 1994). However, observations by Alexander (1993) on Anadara ovalis and by Ambrose et al. (1998) on Mya arenaria, suggest that the time to re-burrow increases with shell length. Therefore, if similar behaviour occurs in S. solida, it can be expected that the main potential targets of the predator species found in the dredge tracks may escape, leaving the larger clams that, unless damaged, do not appear available as prey. Thus, it seems unlikely that a significant number of exposed S. solida would be effectively preyed upon. Our results suggest that predatory action upon unharvested clams on the dredge track is not a major factor in the mortality of S. solida and that potential predators reaching the dredge track areas do greater damage to the fragile non-target species. However, as a relation could be established between the reburial time of impacted target species and the arrival of predators at the harvesting area after fishing impact, this minor aspect should be considered in indirect mortality estimations caused by fishing activities. Moreover, it is important to note that while the study tried to infer indirectly whether predation was increased by dredging, mortality rates of clams were not actually measured, and commercial dredging occurs repeatedly, which may have a greater effect than the one-pass tow tested in this study. Acknowledgements This study was supported by the FAIR ECODREDGE (PL-4465) Project. Thanks are also due to the EcoResources Group for help with laboratory sample processing and to Dr. Pedro Lino for collaboration in taxonomic identification. References Alexander, R.R., 1993. Correlation of shape and habit with sediment grain size for selected species of the bivalve Anadara. Lethaia 26 (2), 153–162.

Ambrose Jr., W.G., Dawson, M., Gailey, C., Ledkosky, P., O’Leary, S., Tassinari, B., Vogel, H., Wilson, C., 1998. Effects of baitworm digging on the soft-shelled clam, Mya arenaria, Maine: shell damage and exposure on the sediment surface. J. Shellfish Res. 17, 4–6. Bergman, M., Hup, M., 1992. Direct effects of beam trawling on macrofauna in a sandy sediment in the southern North Sea. ICES J. Mar. Sci. 49, 5–11. Breum, O., 1970. Stimulation of burrowing activity by wave action in some marine bivalves. Ophelia 8, 197–207. Caddy, J.F., 1968. Underwater observations on scallop (Plactopecten magellanicus L.) behaviour and drag efficiency. J. Fish. Res. Board Canada 25, 2123–2124. Caddy, J.F., 1973. Underwater observations on tracks of dredges and trawls and some effects of dredging on a scallop ground. J. Fish. Res. Board Canada 30, 173–180. Conner, W.G., Simon, J.L., 1979. The effects of oyster shell dredging on an estuarine benthic community. Estuar. Coast. Mar. Sci. 9, 749–758. Dare, P.J., Key, D., Connor, P.M., 1993. The efficiency of springloaded dredges used in the Western English Channel fishery for scallops, Pecten maximus (L.), ICES Fish Capture Committee CM1993/B: 15, p. 8. Evans, P.L., Kaiser, M.J., Hughes, R.N., 1996. Behaviour and energetics of whelks, Buccinum undatum (L.), feeding on animals killed by beam trawling. J. Exp. Mar. Biol. Ecol. 197 (1), 51–62. Feder, H.M., 1981. Aspects of the feeding biology of the brittle star Ophiura texturata. Ophelia 20 (2), 215–235. Fitzhugh, G.R., Fleeger, J.W., 1985. Goby (Pisces: Gobiidae) interactions with meiofauna and small macrofauna. Bull. Mar. Sci. 36 (3), 436–444. Fiu´ za, A.F., 1983. Upwelling patterns off Portugal. In: Suess, E., Thiede, J. (Eds.), Coastal Upwelling: Its Sediment Record. Part A: Responses of the Sedimentary Regime to Present Coastal Upwelling. Plenum Press, New York, pp. 175–197. Gaspar, M.B., 1996. Bivalves do litoral oceaˆ nico algarvio. Aspectos da biologia, ecologia e da pescaria dos mananciais de interesse econo´ mico: aplicaça˜ o a` gesta˜ o dos recursos (Bivalves of the Algarve coast. Biology aspects, ecology and fisheries of the commercial stocks: application to the resource management). Ph.D. Thesis. University of Algarve, 317 pp. Gilkinson, K.D., Schwinghamer, D.C., Gordon Jr., D.C., Prena, J., Rowell, T.W., McKeown, D.L., Vass, W.P., McIsaac, K., Bourbonnais, C., Paulin, M., Hurley, S., 1999. Impacts of otter-trawling on infaunal bivalves living in sandy bottom habitats on the Grand Banks of Newfoundland. Abstract Book, ICES/SCOR Symposium—Ecosystem Effects of Fishing. Montpellier, France, March 15–19, 1999, p. 34. Gisbert, E., Cardona, L., Castello-Orvay, F., 1995. Feeding habits of mullet fry in the Ebro Delta. Misc Zool. 18, 145– 151. Hall, S.J., Basford, D.J., Robertson, M.R., 1990. The impact of hydraulic dredging for razor clams Ensis sp. on an infaunal community. Neth. J. Sea Res. 27 (1), 119–125. Kaiser, M.J., Spencer, B.E., 1994. Fish scavenging behaviour in recently trawled areas. Mar. Ecol. Prog. Ser. 112, 41–49.

L. Chıćharo et al. / Fisheries Research 59 (2002) 247–257 Kaiser, M.J., Spencer, B.E., 1995. Survival of by-catch from a beam trawl. Mar. Ecol. Prog. Ser. 126 (1–3), 31–38. Kaiser, M.J., Ramsay, K., Hughes, R.N., 1998. Can fisheries influence interspecific competition in sympatric populations of hermit crabs? J. Nat. Hist. 32 (4), 521–531. McLoughlin, R.J., Young, P.C., Martin, R.B., Parslow, J., 1991. The Australian scallop dredge: estimates of catching efficiency and associated indirect fishing mortality. Fish. Res. 11, 1–24. Meyer, T.L., Cooper, R.A., Pecci, K.J., 1981. The performance and environmental effects of a hydraulic clam dredge. Mar. Fish. Rev. 43 (9), 1–9. Molinero, A., Flos, R., 1991. Influence of sex and age on the feeding habits of the common sole Solea solea. Mar. Biol. 111 (3), 493–501. Murawski, A.S., Serchuk, F.M., 1989. Environmental effects of offshore dredge fisheries for bivalves. ICES-CM-K27, p. 23. Najai, S., Ktari, M.H., 1979. Study of the diet of the common cuttlefish Sepia officinalis Linn 1758 (Mollusc, Cephalopoda) in the Tunis Gulf. Bull. Inst. Natl. Sci. Tech. Oceanogr. Peche, Tunisia 6 (1–4), 53–61. Ramsay, K., Kaiser, M.J., Hughes, R.N., 1996. Changes in hermit crab feeding patterns in response to trawling disturbance. Mar. Ecol. Prog. Ser. 144 (1–3), 63–72.

257

Ramsay, K., Kaiser, M.J., Hughes, R.N., 1998. Responses of benthic scavengers to fishing disturbance by towed gears in different habitats. J. Exp. Mar. Biol. Ecol. 224 (1), 73–89. Rumohr, H., Krost, P., 1991. Experimental evidence of damage to benthos by bottom trawling with special reference to Arctica islandica. Meeresforsch 33, 340–345. Thrush, S.F., Hewitt, J.E., Cummings, V.J., Dayton, P.K., Cryer, M., Turner, S.J., Funnell, G.A., Budd, R.G., Milburn, C.J., Wilkinson, M.R., 1998. Disturbance of the marine benthic habitat by commercial fishing: impacts at the scale of the fishery. Ecol. Appl. 8, 866–879. Van der Veer, H.W., Bergman, M.J.N., Beukema, J.J., 1985. Dredging activities in the Dutch Wadden Sea: effects on macrobenthic infauna. Neth. J. Sea Res. 19, 183–190. Van Dolah, R.F., Wendt, P.H., Nicholson, N., 1987. Effects of a research trawl on a hard bottom assemblage of sponges and corals. Fish Res. 5, 39–54. Volvenko, I.V., 1994. Food and feeding behaviour of hermit crabs. Biol. Morya Mar. Biol. 20 (6), 411–418. Wassenberg, T.J., Hill, B.J., 1987. Feeding by the sand crab, Portunus pelagicus, on material discarded from prawn trawlers in Moreton Bay. Aust. Mar. Biol. 95, 387–393. Zander, D.C., 1982. Feeding ecology of littoral gobiid and blenniid fish of the Banyuls area (Mediterranean Sea). 1. Main food and tropic dimension of niche and ecotope. Vie Milieu 32 (1), 1–10.