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Benthic primary producers––a neglected environmental problem in Mediterranean maricultures?
Marine Pollution Bulletin 46 (2003) 1372–1376 www.elsevier.com/locate/marpolbul
Focus
Benthic primary producers––a neglected environmental problem in Mediterranean maricultures? Marianne Holmer
a,*
, Marta Perez b, Carlos M. Duarte
c
a Institute of Biology, University of Southern Denmark, Campusvej 55, DK5230 Odense M, Denmark Department d’Ecologıa, Facultad de Biologıa, Universitat de Barcelona, Avda. Diagonal 645, 08028 Barcelona, Spain Grupo de Oceanografia Interdisciplinar, Instituto Mediterr aneo de Estudios Avanzados (IMEDEA), CSIC-UiB, C/Miquel Marqu es 21, 07190 Esporles (Islas Baleares), Spain b
c
Abstract Marine fish farming is increasing rapidly in the Mediterranean and in contrast to the Atlantic the coastal zone in the Mediterranean is characterized by clear waters with high transparency. This allows benthic primary producers such as the slow-growing seagrass Posidonia oceanica to grow at large depths at locations suitable for fish farming and generating a conflict between the conservation of these meadows and the growth of aquaculture operations in the Mediterranean. In this paper we review the current knowledge on environmental interactions between fish farming and benthic primary producers with particular focus on P. oceanica, as this seagrass is a key component along Mediterranean coasts. The recovery times of P. oceanica are very long, in the order of centuries, and losses of this species are thus considered to be irreversible at managerial time scales. Ó 2003 Elsevier Ltd. All rights reserved. Keywords: Aquaculture; Posidonia; Seagrass; Mediterranean
1. Introduction During the last two decades culturing of marine fishes aquaculture has increased rapidly in the Mediterranean (UNEP, 2002) with an expected expansion rate of 4% annually over the next few years. The expansion of marine aquaculture in the Mediterranean basin is a necessary consequence of the collapse of overexploited wild fisheries (FAO, 1997) and the high demand for fish products in the diet of Mediterranean countries. The species cultured in the Mediterranean are primarily warm water species, such as seabream (Sparus auratus) and sea-bass (Dicentrarchus labrax), which target local markets. Several new species are being investigated, and recently culturing of tuna fish to market size has increased tremendously. Common for all these species is a demand for high water quality and rapid water exchange. To fulfill these requirements new farms are primarily installed in open coastal areas at large water depths in excess of >15 m, which enhances the disper-
*
Corresponding author. Tel.: +45-65-502605; fax: +45-65-930457. E-mail address: [email protected] (M. Holmer).
0025-326X/$ - see front matter Ó 2003 Elsevier Ltd. All rights reserved. doi:10.1016/S0025-326X(03)00396-5
sion of dissolved and particulate waste products and minimize the negative impacts on the local environment (Ervik et al., 1997).
2. Environmental impacts specific to fish farming in the Mediterranean The environmental impacts of marine fish farming in the Mediterranean are consistent with those in other parts of the world. Increased nutrient concentrations may stimulate phytoplanktonic and bacterial activity (Karakassis et al., 2001; La Rosa et al., 2002). However, due to the rapid water exchange in most Mediterranean fish farms the water quality appears to be relatively unaffected, with minor increases in nutrient concentrations close to the cages during feeding (Pitta et al., 1999; Karakassis et al., 2001). In contrast, impacts on the benthic ecosystem are far more severe, resulting in organic enrichment of the sediments (Vezzuli et al., 2002) with a consequent reduced biodiversity (Karakassis, 1998). Organic inputs increase by 2–3 fold below and adjacent to fish farms (Karakassis et al., 2000; Holmer, unpublished data). This organic enrichment enhances
M. Holmer et al. / Marine Pollution Bulletin 46 (2003) 1372–1376
bacterial activity (La Rosa et al., 2001) and in particular the anaerobic activity (Karakassis et al., 1998, 2000, 2002). Both benthic meiofaunal and macrofaunal communities are negatively influenced by organic enrichments and have been used as sensitive indicators of aquaculture impact (Karakassis et al., 2000, 2002; La Rosa et al., 2001; Mirto et al., 2001). Possible effects on the larger benthic primary producers have only been addressed briefly (Delgado et al., 1997, 1999; Pergent et al., 1999; Dimech et al., 2000a,b; Ruiz et al., 2001), but the proliferation of macroalgae along shore lines adjacent to fish farms, as observed in Cyprus, has lead to environmental concerns (Argyrou et al., 1999). Also an increased frequency of invasive macroalgae species, such as Caulerpa racemosa and C. taxifolia has been linked to increased nutrient loading from fish farming. The transparency of Mediterranean waters is generally high, in particular in surroundings of the major islands away from urban developments, and most of the Mediterranean coastal waters are oligotrophic. Light may thus penetrate to the bottom at considerable water depths and allow growth of benthic primary producers, such as macroalgae and seagrasses to large depths. The seagrass Posidonia oceanica is a prominent component of the Mediterranean coast due to its ability to grow in low-nutrient environments. P. oceanica covers about 50,000 km2 in the Mediterranean (Bethoux and Copin-M ontegu, 1986) extending between 1 and 40 m depth, where it forms lush meadows that represent a major source of food and habitat for a wide range of organisms (Duarte and Chiscano, 1999). In addition, the reef-forming P. oceanica meadows are major sites of organic carbon burial, and their canopies dissipate wave energy and trap sediments (Gacia and Duarte, 2001; Gacia et al., 2002). Hence, P. oceanica meadows are valuable ecosystems contributing to preserve both the biodiversity and physical integrity of the Mediterranean coast (Hemminga and Duarte, 2000), and are, therefore protected under both national and European frameworks. Yet, these meadows are often found at locations suitable for fish farming since these sites are characterised by rapid water movements (Be-
1373
thoux and Copin-M ontegu, 1986), generating a conflict between the conservation of these meadows and the growth of aquaculture operations in the Mediterranean. In practice, however, many Mediterranean fish farms have been established over P. oceanica meadows, as there are no clear guidelines on a minimum protection zone and only a few studies have been undertaken to examine the effect of fish farming on benthic primary producers.
3. Negative effects on seagrass meadows Available information points to aquaculture practices as a growing threat to seagrass meadows (Duarte, 2002), with major negative effects of farming activities on the adjacent seagrass meadows extending from individual to ecosystem level (Fig. 1). The seagrass P. oceanica is severely impacted right beneath the cages, where light levels are significantly reduced due to the presence of net cages (Delgado et al., 1999; Dimech et al., 2000a,b) and where organic inputs deteriorate sediment conditions to support seagrass growth. The water transparency, however, is not a major limiting factor outside the cages, as there is only limited reduction in light penetration (Ruiz et al., 2001). Yet, the seagrass meadows are clearly affected by the farming activities both underneath and within the proximity of the fish cages, resulting in reduced seagrass biomass and density close to the cages and increased epiphytic cover and macroalgal invasion (Table 1). Loading of the seagrass leaves with settling particles and an increase in epiphytic growth may further affect the photosynthetic capacity of the seagrasses by reducing the incident light resulting in reduced leaf growth (Delgado et al., 1997, 1999). Reduced carbohydrate pools within rhizomes of impacted seagrasses indicate that the carbon balance of the plant is negatively affected by the operation of fish cages (Ruiz et al., 2001). The health of the seagrass is further affected by the deterioration of sediment conditions by the excess organic and nutrient inputs derived from the inputs of fish feed, which exceed by several fold the requirements of the
Fig. 1. A conceptual model on the effect of fish farm waste products on seagrass meadows.
1374
M. Holmer et al. / Marine Pollution Bulletin 46 (2003) 1372–1376
Table 1 Descriptors of seagrass (P. oceanica) meadow status under fish cages compared to control sites Location
Density (%)
Biomass (%)
Leaf growth (%)
Epiphyte cover (%)
Herbivory pressure (%)
Reference
Corsica 10 m
)80
n.a.
n.a.
+500
n.a.
Corsica 23 m
)45
n.a.
n.a.
+100
n.a.
Malta 12–16 m
)31
)54
n.a.
+200
n.a.
Murcia Spain 8 m Minorca 5.5 m (3 years after cessation) Cyprus 30 m
n.a. )93
)53 )97
)60 to 75 n.a.
+100–600 +56
+80–200 n.a.
Pergent et al. (1999) Pergent et al. (1999) Dimech et al. (2000a,b) Ruiz et al. (2001) Delgado et al. (1999)
)35
)50
n.a.
n.a.
n.a.
Sicily 20 m
)95
)84
)17
+217
+550
Perez et al. (unpublished) Perez et al. (unpublished)
n.a.––data not available.
cultured fish (Holmer and Kristensen, 1996; Ervik et al., 1997; Holmer, unpublished). The nutrient inputs derived from fish farms increase the nutrient contents within P. oceanica tissues, which is often nutrient-limited (Alcoverro et al., 1997). However, this change seems to attract herbivores to the seagrass meadows (Table 1) thereby increasing herbivory and burdens on the carbon budget of the plant. Sea-urchins are usually found in low numbers in seagrass meadows, but their numbers have been observed to increase tremendously near to fish cages, resulting in a high herbivore pressure. Overgrazing decrease the photosynthetic capacity by reducing shoot size and thus further enhance the carbon imbalance of the meadows (Ruiz et al., 2001). Rhizome growth and hence the expansion of the seagrass meadows has been found to decrease in vicinity of fish cages and this is particularly a problem during recolonization after cessation of the farms (Delgado et al., 1999), as seagrasses are clonal plants that reply heavily on rhizome extension for clonal growth (Marb a and Duarte, 1998). Delgado et al. (1999) found that the seagrass meadows impacted by aquaculture activities were still declining 3 years after cessation suggesting that recolonization was not initiated yet.
4. Focus on the slow-growing seagrass P. oceanica An ongoing comparative study assessing the impacts of fish farming on P. oceanica meadows across the Mediterranean (MedVeg project, www.medveg.dk) confirms the above findings, with the input of organic matter and nutrients having negative impact on P. oceanica beds surrounding fish farms installations in distances up to 200 m away from the operations (Table 1). At a location in Sicily negative impacts were inferred from changes in meadow spatial structure with up to 10fold decrease in cover and shoot density close to the cages and a 2-fold decrease 50 m away from the cages
(Table 1). The herbivore pressure increased near the fish farm, mainly due to high numbers of the sea-urchin Paracentrotus lividus below the cages, but also in the surroundings where it was hiding among the rhizomes (Table 1). The reasons for the increase are not clear, but it seems that the sea-urchins are attracted either due to enriched food sources as a result of increased nitrogen content in the plant–epiphyte complex or due to the organic matter settling from the farm. The increase in sea-urchin density involves an increase in herbivore pressure on P. oceanica leaves, causing important reduction in leaf shoot length and decreasing the capability of the plants to obtain energy. Fish farm effluents also cause a proliferation of macroalgae cover and shifts in community composition. Close to the cages, seagrass shoot density and cover were diminished due to plant mortality, creating bare space which was colonised by more opportunistic species such as the invasive species C. racemosa, whereas other species typical on P. oceanica rhizomes, such as Udotea spp. reduce their extent. Preliminary results also show reduced rhizome growth, along with physiological responses with increased nutrient concentrations and reduced carbon reserves in P. oceanica which may be critical for the increased mortality of the plants. The sediments were highly reduced in the affected areas with sulphide present in the pore waters indicating that the sediment conditions to support plant growth were severely impoverished close to the farm (Holmer, unpublished). The decline in seagrass density near fish farms appears to result from both increased shoot mortality and impared seagrass recruitment. Indeed, rhizome growth, the primary mechanism for clonal seagrass expansion (Hemminga and Duarte, 2000) has been observed to decline severely shortly after the establishment of fish farms, thereby impairing the recruitment of new seagrass shoots to compensate for losses. These results obtained within the MedVeg project provide evidence that deterioration of the adjacent P. oceanica meadows
M. Holmer et al. / Marine Pollution Bulletin 46 (2003) 1372–1376
occurs very shortly (months) after the onset of farming operation. The impacts to P. oceanica meadows derived from the spread of fish cage farming in the Mediterranean are particularly alarming, as this impact adds to stresses that are already resulting in seagrass loss across the Mediterranean (e.g. Marb a and Duarte, 1997; Duarte, 2002). Because P. oceanica is the slowestgrowing seagrass species and rarely reproduces sexually (Hemminga and Duarte, 2000), the recovery times of P. oceanica are very long, in the order of centuries (Duarte, 1995; Marb a et al., 2002), such that losses of this species should be considered irreversible at managerial time scales. It is, therefore, critical that reliable guidelines, based on solid scientific evidence, be produced to assist with site selection to establish new fish farms as to avoid damage to P. oceanica meadows. Moreover, a suite of best practices for fish farming in the Mediterranean must be developed to avoid the present excess supply of feed in the farms, which expands the impact of the operations. Lastly, remediation technologies to improve habitat (e.g. sediment) conditions to support seagrass growth and to improve seagrass health must be developed to prevent the loss of alreadyimpacted meadows. Whereas the MedVeg project represents an important step towards these goals, additional large-scale research efforts are necessary to underpin the sustainability of fish farming activities in the Mediterranean coast, as the demand for aquaculture products continue to increase.
Acknowledgements This work was partially funded by MedVeg (EU contract no. Q5RS-2001-02456) and Danish Research Council to MH (grant no. 21-02-0463).
References Alcoverro, T., Romero, J., Duarte, C.M., L opez, N.I., 1997. Spatial and temporal variations in nutrient limitation of seagrass Posidonia oceanica growth in the NW Mediterranean. Mar. Ecol. Prog. Ser. 146, 155–161. Argyrou, M., Demetropoulos, A., Hadjichristophorou, M., 1999. Expansion of the macroalga Caulerpa racemosa and changes in soft bottom macrofaunal assemblages in Moni Bay, Cyprus. Oceanol. Acta 22, 517–528. Bethoux, J.P., Copin-M ontegu, G., 1986. Biological fixation of atmospheric nitrogen in the Mediterranean Sea. Limnol. Oceanogr. 31, 1353–1358. Delgado, O., Grau, A., Pou, S., Riera, F., Massuti, C., Zabala, M., Ballesteros, E., 1997. Seagrass regression caused by fish cultures in Fornells Bay (Menorca, Western Mediterranean). Oceanol. Acta 20, 557–563. Delgado, O., Ruiz, J., Perez, M., Romero, J., Ballesteros, E., 1999. Effects of fish farming on seagrass (Posidonia oceanica) in a Mediterranean bay: seagrass decline after organic loading cessation. Oceanol. Acta 22, 109–117.
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Dimech, M., Borg, J.A., Schembri, P.J., 2000a. Structural changes in a Posidonia Oceanica meadow exposed to a pollution gradient from a marine fish farm in Malta (Central Mediterranean). Biol. Mar. Medit. 7, 361–364. Dimech, M., Borg, J.A., Schembri, P.J., 2000b. The effects of a marine fish farm on the species richness and abundance of molluscs,decapods and echinoderms associated with a Posidonia Oceanica meadow in Malta (Central Mediterranean). Biol. Mar. Medit. 7, 357–360. Duarte, C.M., 1995. Submerged aquatic vegetation in relation to different nutrient regimes. Ophelia 41, 87–112. Duarte, C.M., 2002. The future of seagrass meadows. Environ. Conserv. 29, 192–206. Duarte, C.M., Chiscano, C.L., 1999. Seagrass biomass and production: a reassessment. Aquat. Bot. 65, 159–174. Ervik, A., Hansen, P.K., Aure, J., Stigebrandt, A., Johannessen, P., Jahnsen, T., 1997. Regulating the local environmental impact of intensive marine fish farming I. The concept of the MOM system (Modelling-Ongrowing fish farms-Monitoring). Aquaculture 158, 85–94. FAO, 1997. Review of the state of world fishery resources: Marine fisheries. FAO Fisheries Circular no. 920 FIRM/C920, Rome. ISSN 0429-9329. Gacia, E., Duarte, C.M., 2001. Elucidating sediment retention by seagrasses: sediment deposition and resuspension in a Mediterranean (Posidonia oceanica) meadow. Estuar. Coast. Shelf Sci. 52, 505–514. Gacia, E., Duarte, C.M., Middelburg, J.J., 2002. Carbon and nutrient deposition in a Mediterranean seagrass (Posidonia oceanica) meadow. Limnol. Oceanogr. 47, 23–32. Hemminga, M.A., Duarte, C.M., 2000. Seagrass Ecology. Cambridge University Press, Cambridge. Holmer, M., Kristensen, E., 1996. Seasonality of sulfate reduction and pore water solutes in a marine fish farm sediment: the importance of temperature and sedimentary organic matter. Biogeochemistry 32, 15–39. Karakassis, I., 1998. Aquaculture and coastal marine biodiversity. Oceanis 24, 271–286. Karakassis, I., Tsapakis, M., Hatziyanni, E., 1998. Seasonal variability in sediment profiles beneath fish farm cages in the Mediterranean. Mar. Ecol. Prog. Ser. 162, 243–252. Karakassis, I., Tsapakis, M., Hatziyanni, E., Papadopoulou, K.N., Plaiti, W., 2000. Impact of cage farming of fish on the seabed in three Mediterranean coastal areas. Ices J. Mar. Sci. 57, 1462–1471. Karakassis, I., Tsapakis, M., Hatziyanni, E., Pitta, P., 2001. Diel variation of nutrients and chlorophyll in sea bream and sea bass cages in the Mediterranean. Fresen. Environ. Bull. 10, 278– 283. Karakassis, I., Tsapakis, M., Smith, C.J., Rumohr, H., 2002. Fish farming impacts in the Mediterranean studied through sediment profile imagery. Mar. Ecol. Prog. Ser. 227, 125–133. La Rosa, T., Mirto, S., Favaloro, E., Savona, B., Sara, G., Danovaro, R., Mazzola, A., 2002. Impact on the water column biogeochemistry of a Mediterranean mussel and fish farm. Water Res. 36, 713– 721. La Rosa, T., Mirto, S., Mazzola, A., Danovaro, R., 2001. Differential responses of benthic microbes and meiofauna to fish farm disturbance in coastal sediments. Environ. Pollut. 112, 427–434. Marba, N., Duarte, C.M., 1997. Interannual changes in seagrass (Posidonia oceanica) growth and environmental change in the Spanish Mediterranean littoral. Limnol. Oceanogr. 42, 800–810. Marba, N., Duarte, C.M., 1998. Rhizome elongation and seagrass clonal growth. Mar. Ecol. Prog. Ser. 174, 269–280. Marba, N., Duarte, C.M., Holmer, M., Martınez, R., Basterretxea, G., Orfila, A., Jordi, A., Tintore, J., 2002. Effectiveness of protection on (Posidonia oceanica) populations in the Cabrera National Park (Spain). Environ. Conserv. 29, 509–518.
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Mirto, S., La Rosa, T., Gambi, C., Danovaro, R., Mazzola, A., 2001. Nematode community response to fish farm impact in the western Mediterranean. Environ. Bull. 116, 203–214. Pergent, G., Mendez, S., Pergent-Martini, C., Pasqualini, V., 1999. Preliminary data on the impact of fish farming facilities on Posidonia oceanica meadows in the Mediterranean. Oceanol. Acta 22, 95–107. Pitta, P., Karakassis, I., Tsapakis, M., Zivanovic, S., 1999. Natural vs. mariculture induced variability in nutrients and plankton in the Eastern Mediterranean. Hydrobiologica 391, 181–194.
Ruiz, J.M., Perez, M., Romero, J., 2001. Effects of fish farm loadings on seagrass (Posidonia oceanica) distribution,growth and photosynthesis. Mar. Pollut. Bull. 42, 749–760. Vezzuli, L., Chelossi, E., Riccardi, G., Fabiano, M., 2002. Bacterial community structure and activity in fish farm sediments of the Ligurian Sea (Western Mediterranean). Aquacult. Int. 10, 123– 141. UNEP, 2002. Vital Water Graphics––An Overview of the State of the World’s Fresh and Marine Waters. UNEP, Nairobi, Kenya. ISBN: 92-807-2236-0.
Focus
Benthic primary producers––a neglected environmental problem in Mediterranean maricultures? Marianne Holmer
a,*
, Marta Perez b, Carlos M. Duarte
c
a Institute of Biology, University of Southern Denmark, Campusvej 55, DK5230 Odense M, Denmark Department d’Ecologıa, Facultad de Biologıa, Universitat de Barcelona, Avda. Diagonal 645, 08028 Barcelona, Spain Grupo de Oceanografia Interdisciplinar, Instituto Mediterr aneo de Estudios Avanzados (IMEDEA), CSIC-UiB, C/Miquel Marqu es 21, 07190 Esporles (Islas Baleares), Spain b
c
Abstract Marine fish farming is increasing rapidly in the Mediterranean and in contrast to the Atlantic the coastal zone in the Mediterranean is characterized by clear waters with high transparency. This allows benthic primary producers such as the slow-growing seagrass Posidonia oceanica to grow at large depths at locations suitable for fish farming and generating a conflict between the conservation of these meadows and the growth of aquaculture operations in the Mediterranean. In this paper we review the current knowledge on environmental interactions between fish farming and benthic primary producers with particular focus on P. oceanica, as this seagrass is a key component along Mediterranean coasts. The recovery times of P. oceanica are very long, in the order of centuries, and losses of this species are thus considered to be irreversible at managerial time scales. Ó 2003 Elsevier Ltd. All rights reserved. Keywords: Aquaculture; Posidonia; Seagrass; Mediterranean
1. Introduction During the last two decades culturing of marine fishes aquaculture has increased rapidly in the Mediterranean (UNEP, 2002) with an expected expansion rate of 4% annually over the next few years. The expansion of marine aquaculture in the Mediterranean basin is a necessary consequence of the collapse of overexploited wild fisheries (FAO, 1997) and the high demand for fish products in the diet of Mediterranean countries. The species cultured in the Mediterranean are primarily warm water species, such as seabream (Sparus auratus) and sea-bass (Dicentrarchus labrax), which target local markets. Several new species are being investigated, and recently culturing of tuna fish to market size has increased tremendously. Common for all these species is a demand for high water quality and rapid water exchange. To fulfill these requirements new farms are primarily installed in open coastal areas at large water depths in excess of >15 m, which enhances the disper-
*
Corresponding author. Tel.: +45-65-502605; fax: +45-65-930457. E-mail address: [email protected] (M. Holmer).
0025-326X/$ - see front matter Ó 2003 Elsevier Ltd. All rights reserved. doi:10.1016/S0025-326X(03)00396-5
sion of dissolved and particulate waste products and minimize the negative impacts on the local environment (Ervik et al., 1997).
2. Environmental impacts specific to fish farming in the Mediterranean The environmental impacts of marine fish farming in the Mediterranean are consistent with those in other parts of the world. Increased nutrient concentrations may stimulate phytoplanktonic and bacterial activity (Karakassis et al., 2001; La Rosa et al., 2002). However, due to the rapid water exchange in most Mediterranean fish farms the water quality appears to be relatively unaffected, with minor increases in nutrient concentrations close to the cages during feeding (Pitta et al., 1999; Karakassis et al., 2001). In contrast, impacts on the benthic ecosystem are far more severe, resulting in organic enrichment of the sediments (Vezzuli et al., 2002) with a consequent reduced biodiversity (Karakassis, 1998). Organic inputs increase by 2–3 fold below and adjacent to fish farms (Karakassis et al., 2000; Holmer, unpublished data). This organic enrichment enhances
M. Holmer et al. / Marine Pollution Bulletin 46 (2003) 1372–1376
bacterial activity (La Rosa et al., 2001) and in particular the anaerobic activity (Karakassis et al., 1998, 2000, 2002). Both benthic meiofaunal and macrofaunal communities are negatively influenced by organic enrichments and have been used as sensitive indicators of aquaculture impact (Karakassis et al., 2000, 2002; La Rosa et al., 2001; Mirto et al., 2001). Possible effects on the larger benthic primary producers have only been addressed briefly (Delgado et al., 1997, 1999; Pergent et al., 1999; Dimech et al., 2000a,b; Ruiz et al., 2001), but the proliferation of macroalgae along shore lines adjacent to fish farms, as observed in Cyprus, has lead to environmental concerns (Argyrou et al., 1999). Also an increased frequency of invasive macroalgae species, such as Caulerpa racemosa and C. taxifolia has been linked to increased nutrient loading from fish farming. The transparency of Mediterranean waters is generally high, in particular in surroundings of the major islands away from urban developments, and most of the Mediterranean coastal waters are oligotrophic. Light may thus penetrate to the bottom at considerable water depths and allow growth of benthic primary producers, such as macroalgae and seagrasses to large depths. The seagrass Posidonia oceanica is a prominent component of the Mediterranean coast due to its ability to grow in low-nutrient environments. P. oceanica covers about 50,000 km2 in the Mediterranean (Bethoux and Copin-M ontegu, 1986) extending between 1 and 40 m depth, where it forms lush meadows that represent a major source of food and habitat for a wide range of organisms (Duarte and Chiscano, 1999). In addition, the reef-forming P. oceanica meadows are major sites of organic carbon burial, and their canopies dissipate wave energy and trap sediments (Gacia and Duarte, 2001; Gacia et al., 2002). Hence, P. oceanica meadows are valuable ecosystems contributing to preserve both the biodiversity and physical integrity of the Mediterranean coast (Hemminga and Duarte, 2000), and are, therefore protected under both national and European frameworks. Yet, these meadows are often found at locations suitable for fish farming since these sites are characterised by rapid water movements (Be-
1373
thoux and Copin-M ontegu, 1986), generating a conflict between the conservation of these meadows and the growth of aquaculture operations in the Mediterranean. In practice, however, many Mediterranean fish farms have been established over P. oceanica meadows, as there are no clear guidelines on a minimum protection zone and only a few studies have been undertaken to examine the effect of fish farming on benthic primary producers.
3. Negative effects on seagrass meadows Available information points to aquaculture practices as a growing threat to seagrass meadows (Duarte, 2002), with major negative effects of farming activities on the adjacent seagrass meadows extending from individual to ecosystem level (Fig. 1). The seagrass P. oceanica is severely impacted right beneath the cages, where light levels are significantly reduced due to the presence of net cages (Delgado et al., 1999; Dimech et al., 2000a,b) and where organic inputs deteriorate sediment conditions to support seagrass growth. The water transparency, however, is not a major limiting factor outside the cages, as there is only limited reduction in light penetration (Ruiz et al., 2001). Yet, the seagrass meadows are clearly affected by the farming activities both underneath and within the proximity of the fish cages, resulting in reduced seagrass biomass and density close to the cages and increased epiphytic cover and macroalgal invasion (Table 1). Loading of the seagrass leaves with settling particles and an increase in epiphytic growth may further affect the photosynthetic capacity of the seagrasses by reducing the incident light resulting in reduced leaf growth (Delgado et al., 1997, 1999). Reduced carbohydrate pools within rhizomes of impacted seagrasses indicate that the carbon balance of the plant is negatively affected by the operation of fish cages (Ruiz et al., 2001). The health of the seagrass is further affected by the deterioration of sediment conditions by the excess organic and nutrient inputs derived from the inputs of fish feed, which exceed by several fold the requirements of the
Fig. 1. A conceptual model on the effect of fish farm waste products on seagrass meadows.
1374
M. Holmer et al. / Marine Pollution Bulletin 46 (2003) 1372–1376
Table 1 Descriptors of seagrass (P. oceanica) meadow status under fish cages compared to control sites Location
Density (%)
Biomass (%)
Leaf growth (%)
Epiphyte cover (%)
Herbivory pressure (%)
Reference
Corsica 10 m
)80
n.a.
n.a.
+500
n.a.
Corsica 23 m
)45
n.a.
n.a.
+100
n.a.
Malta 12–16 m
)31
)54
n.a.
+200
n.a.
Murcia Spain 8 m Minorca 5.5 m (3 years after cessation) Cyprus 30 m
n.a. )93
)53 )97
)60 to 75 n.a.
+100–600 +56
+80–200 n.a.
Pergent et al. (1999) Pergent et al. (1999) Dimech et al. (2000a,b) Ruiz et al. (2001) Delgado et al. (1999)
)35
)50
n.a.
n.a.
n.a.
Sicily 20 m
)95
)84
)17
+217
+550
Perez et al. (unpublished) Perez et al. (unpublished)
n.a.––data not available.
cultured fish (Holmer and Kristensen, 1996; Ervik et al., 1997; Holmer, unpublished). The nutrient inputs derived from fish farms increase the nutrient contents within P. oceanica tissues, which is often nutrient-limited (Alcoverro et al., 1997). However, this change seems to attract herbivores to the seagrass meadows (Table 1) thereby increasing herbivory and burdens on the carbon budget of the plant. Sea-urchins are usually found in low numbers in seagrass meadows, but their numbers have been observed to increase tremendously near to fish cages, resulting in a high herbivore pressure. Overgrazing decrease the photosynthetic capacity by reducing shoot size and thus further enhance the carbon imbalance of the meadows (Ruiz et al., 2001). Rhizome growth and hence the expansion of the seagrass meadows has been found to decrease in vicinity of fish cages and this is particularly a problem during recolonization after cessation of the farms (Delgado et al., 1999), as seagrasses are clonal plants that reply heavily on rhizome extension for clonal growth (Marb a and Duarte, 1998). Delgado et al. (1999) found that the seagrass meadows impacted by aquaculture activities were still declining 3 years after cessation suggesting that recolonization was not initiated yet.
4. Focus on the slow-growing seagrass P. oceanica An ongoing comparative study assessing the impacts of fish farming on P. oceanica meadows across the Mediterranean (MedVeg project, www.medveg.dk) confirms the above findings, with the input of organic matter and nutrients having negative impact on P. oceanica beds surrounding fish farms installations in distances up to 200 m away from the operations (Table 1). At a location in Sicily negative impacts were inferred from changes in meadow spatial structure with up to 10fold decrease in cover and shoot density close to the cages and a 2-fold decrease 50 m away from the cages
(Table 1). The herbivore pressure increased near the fish farm, mainly due to high numbers of the sea-urchin Paracentrotus lividus below the cages, but also in the surroundings where it was hiding among the rhizomes (Table 1). The reasons for the increase are not clear, but it seems that the sea-urchins are attracted either due to enriched food sources as a result of increased nitrogen content in the plant–epiphyte complex or due to the organic matter settling from the farm. The increase in sea-urchin density involves an increase in herbivore pressure on P. oceanica leaves, causing important reduction in leaf shoot length and decreasing the capability of the plants to obtain energy. Fish farm effluents also cause a proliferation of macroalgae cover and shifts in community composition. Close to the cages, seagrass shoot density and cover were diminished due to plant mortality, creating bare space which was colonised by more opportunistic species such as the invasive species C. racemosa, whereas other species typical on P. oceanica rhizomes, such as Udotea spp. reduce their extent. Preliminary results also show reduced rhizome growth, along with physiological responses with increased nutrient concentrations and reduced carbon reserves in P. oceanica which may be critical for the increased mortality of the plants. The sediments were highly reduced in the affected areas with sulphide present in the pore waters indicating that the sediment conditions to support plant growth were severely impoverished close to the farm (Holmer, unpublished). The decline in seagrass density near fish farms appears to result from both increased shoot mortality and impared seagrass recruitment. Indeed, rhizome growth, the primary mechanism for clonal seagrass expansion (Hemminga and Duarte, 2000) has been observed to decline severely shortly after the establishment of fish farms, thereby impairing the recruitment of new seagrass shoots to compensate for losses. These results obtained within the MedVeg project provide evidence that deterioration of the adjacent P. oceanica meadows
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occurs very shortly (months) after the onset of farming operation. The impacts to P. oceanica meadows derived from the spread of fish cage farming in the Mediterranean are particularly alarming, as this impact adds to stresses that are already resulting in seagrass loss across the Mediterranean (e.g. Marb a and Duarte, 1997; Duarte, 2002). Because P. oceanica is the slowestgrowing seagrass species and rarely reproduces sexually (Hemminga and Duarte, 2000), the recovery times of P. oceanica are very long, in the order of centuries (Duarte, 1995; Marb a et al., 2002), such that losses of this species should be considered irreversible at managerial time scales. It is, therefore, critical that reliable guidelines, based on solid scientific evidence, be produced to assist with site selection to establish new fish farms as to avoid damage to P. oceanica meadows. Moreover, a suite of best practices for fish farming in the Mediterranean must be developed to avoid the present excess supply of feed in the farms, which expands the impact of the operations. Lastly, remediation technologies to improve habitat (e.g. sediment) conditions to support seagrass growth and to improve seagrass health must be developed to prevent the loss of alreadyimpacted meadows. Whereas the MedVeg project represents an important step towards these goals, additional large-scale research efforts are necessary to underpin the sustainability of fish farming activities in the Mediterranean coast, as the demand for aquaculture products continue to increase.
Acknowledgements This work was partially funded by MedVeg (EU contract no. Q5RS-2001-02456) and Danish Research Council to MH (grant no. 21-02-0463).
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