ICES Journal of Marine Science, 59: S324–S329. 2002 doi:10.1006/jmsc.2002.1208, available online at http://www.idealibrary.com on
Short communication An application of artificial reefs to reduce organic enrichment caused by net-cage fish farming: preliminary results Dror L. Angel and Ehud Spanier Angel, D. L., and Spanier, E. 2002. An application of artificial reefs to reduce organic enrichment caused by net-cage fish farming: preliminary results. – ICES Journal of Marine Science, 59: S324–S329. Two artificial reefs made of porous recycled high-density polyethylene fence material were moored on the sea floor (20-m depth) off the North Beach of Eilat (Gulf of Aqaba, Red Sea) in April 1999. One reef was situated below a commercial net-cage fish farm, and a control reef was deployed outside the area of direct influence of the farm. The objective was to determine if a reef below farm cages could alleviate organic loading of the environment by serving as a biological filter. To examine this question in both qualitative and quantitative terms, the two reefs were compared with regard to organic matter in the sediment close by, abundance of fish and invertebrates, particle filtration (retention) efficiency, and change in biomass of fouling organisms. In addition, control sites situated near the two reefs were also monitored to compare the status of the sediment and of associated biota with those of the reefs. The differences in organic matter content of the sediment between each reef and its respective control site were not significant. Also, fish community metrics did not differ significantly, although the total number of fish was 30% higher at the farm site. Biomass of fouling organisms (particularly tunicates and bryozoans) varied inconsistently between sites over time. Particle retention efficiency of the reefs was estimated at 240 g C d 1, based on the reduction in particulate Chl a in water samples taken downstream of the reefs compared with samples taken upstream. 2002 International Council for the Exploration of the Sea. Published by Elsevier Science Ltd. All rights reserved.
Keywords: artificial reef, biofilter, environmental impact, mariculture, Red Sea. Accepted 27 November 2001 D. L. Angel: Israel Oceanographic and Limnological Research, National Center for Mariculture, PO Box 1212, Eilat 88112, Israel; tel: +1 617 258 6835; fax: +1 617 253 7475; e-mail:
[email protected]. E. Spanier: The Leon Recanati Center for Maritime Studies and Department of Maritime Civilizations, University of Haifa, Mount Carmel, Haifa 31905, Israel.
Introduction One of the main concerns regarding net-cage fish mariculture in coastal waters is their impact on the marine environment. Generally, large populations of wild fish congregate around the fish cages to benefit from the unique conditions created by farms (Beveridge, 1996). The constant flux of faeces and uneaten food falling from the cages leads to organic matter (OM) accumulation on the seafloor and eventually to anoxia and build-up of hydrogen sulphide in the sediments (Holby, 1991). Such geochemical changes usually cause substantial alteration in the composition of benthic and 1054–3139/02/0S0324+06 $35.00/0
epibenthic biota below fish farms (Weston, 1990). Although organic matter does not accumulate under all fish farms, it will do so when supply rate exceeds decomposition rate (Hall et al., 1990). Various solutions have been proposed to reduce organic sediment enrichment below net cages (reviewed in Beveridge, 1996), e.g. collection of particles falling from the cages, collection of detritus from the seafloor using submersible pumps, harrowing the sediments, etc. However, most of these solutions are impractical. An alternative option might be to construct artificial reefs below fish farms to enhance take up and mineralization of organic and inorganic matter released from the cages and thereby reduce
2002 International Council for the Exploration of the Sea. Published by Elsevier Science Ltd. All rights reserved.
An application of artificial reefs to reduce organic enrichment caused by net-cage fish farming environmental enrichment. For example, Laihonen et al. (1996) described the possible use of artificial reefs as a means of nutrient removal in the Baltic Sea. Artificial reefs below fish farms should facilitate aerobic breakdown of OM released by providing a large surface area for microbial colonization in the oxygenated water above the seafloor. OM decomposition is largely a function of microbial processes and aerobic micro-organisms appear to be more efficient than anaerobic ones (Cowie and Hedges, 1992). Thus, a substantial part of the particulate and dissolved OM absorbed by reef organisms might be metabolized (respired) to CO2 and H2O and thereby naturally removed from the system. Moreover, by reducing OM flux from the farm to the sediment, the reef should enable macrofauna to re-colonize the surrounding sediments, and eventually enable demersal fish and other invertebrates to return to the region as well (for similar examples, see Porter et al., 1996; Angel et al., 1998a). We constructed reefs with a large surface area for settlement of sessile organisms, and with many openings to allow ample flow of oxygenated water through the structures. Our objective was to test the hypothesis that such reefs can reduce OM flux from net-cage fish farms to the environment by capturing and metabolizing some of these effluents. The study involved four treatments: at the farm site with (RC) and without (CC) a reef, and at a control site with (RN) and without (CN) a reef. We formulated the following three questions to detect qualitative and quantitative differences among RC, CC, RN, and CN: (1) Do reefs remove suspended particles from the water, and, if so, at what rates? (2) Do patterns of sessile invertebrate and fish recruitment differ between treatments? (3) Do biogeochemical variables (e.g. OM in the sediment) differ between treatments?
Study site The Ardag farm (in operation since 1988) is located near the city of Eilat, Israel at the northern end of the Gulf of Aqaba (Red Sea), about 300 m offshore and adjacent to the Israel–Jordan border (3458 40 E 2932 45 N). Gulf waters are generally oligotrophic and clear (visibility often exceeding 20 m) and sea surface temperatures range seasonally from 21C to 27C. In 1999, the farm consisted of three parallel 100–150-m-long steel pontoons, approximately 100 m apart and moored in a northeast–southwest orientation. The pontoons support a series of round net cages (mostly 13 m diameter and 10 m deep; 1327 m3) for production of gilthead seabream (Sparus aurata) (stocking density 20–25 kg m 3). During our study in 1999, fish were fed Matmor extruded fish food pellets (composition in g kg 1: dry matter, 925; protein, 450; digestible protein, 380; lipids, 190 lipids; N, 72; P, 15; ash, 120; energy equivalents in
S325
Figure 1. A sketch of the artificial reef showing the triangular reef structure made of 28 cylinders (numbered for reference in census work).
MJ kg 1: gross, 21; digestible, 18). The flux of particulate matter and organic carbon, as measured by sediment traps near the seafloor below the farm, generally did not exceed 40 (range 8–70) and 20 (range 2–30) g m 2 d 1, respectively (Angel et al., 1998b). The control site was situated 500 m west of the fish farm, outside its sphere of influence. The depth at both sites was 20 m.
Materials and methods Two reef units were constructed from 4-mm-thick white, high-density polyethylene sheets, which were rolled and tied to create 40 cm diameter cylinders. Each reef consisted of 28 cylinders arranged in a 240-cm high triangular shape with a 280240 cm base (Figure 1). The total surface area of reef material within each structure was 115 m2. Seventy-two 3045 cm sampling plates of the same high-density polyethylene material were labelled and weighed. These were bent and attached by tie wraps in a convex position on the outer sides of the external cylinders to resemble the reef surface (36 plates per reef), so that these could be sampled for sessile biomass without affecting the integrity of the reefs. The artificial reefs were deployed and moored to the sea floor on 25 March 1999. Control sites encompassing an area of sediment equal to that of the reefs (240280 cm) and situated 10 m south of the two reefs were marked by ropes. Sediments were sampled by scuba divers at 3-monthly intervals. Four sampling stations were located 3 m from the edge of the reefs on each side or from the
S326
D. L. Angel and E. Spanier Table 1. Parameter measurements at different times after reef deployment (ARD; in months) at the farm site (RC: reef; CC: nearby sediment) and control site (RN: reef; CN: nearby sediment). Within/outside refers to number of fish recorded within the reef cylinders and outside of, yet adjacent to the reef, respectively. (LOI: loss-on-ignition).
ARD
0 3 0 3 1 2 3 3 3 3 1 3 1 3 4 4
Variable Sediment geochemistry LOI (%) LOI (%) Water content (%) Water content (%) Fouling biomass (total reef surface) Dry weight (kg) Dry weight (kg) Dry weight (kg) Visual census (fish) No. of species Diversity (H ) No. individuals, within/outside Video census (fish) No. of species No. of species No. of individuals (within) No. of individuals (within) Macrofauna (total reef surface) No. of tunicates (within) No. of bryozoans (within)
240280 cm rectangle marked for the controls. In the laboratory, the top 1-cm slice from each sediment core was removed and analysed for percent water and losson-ignition (LOI; Angel et al., 1995). Three sampling plates were removed from each reef once every 2 months for detailed quantitative assessment of the micro and macro-fouling communities on the reef surface. The plates removed were weighed and photographed. Fish occupying the two reef structures were enumerated by a pair of divers during morning hours by in situ identification and counting (3 months after reef deployment) and by analysis of underwater video recordings and still photography of reef and control areas (after 1 and 3 months). Visual counts were conducted cylinderby-cylinder to assess the 3-dimensional distribution of the different fish species in the reef, as well as their orientation. Counts were also made of fish in the immediate vicinity of the reefs. In addition, macroinvertebrates and all visible organisms within the outermost 50 cm of representative cylinders of the reefs and in the control areas were enumerated. Fish species diversity (Shannon–Wiener, H ) at the two sites was calculated. Water samples were taken to assess the filtration efficiency of these structures and associated biota (Yahel et al., 1998). Prior to sampling, current direction and velocity were determined by releasing a fluorescent dye (sodium fluorescein) into the water and following its
Farm site RC CC
Control site RN CN
4.16 3.95 38.4 40.1
4.41 4.06 40.2 39.7
1.09 2.25 23.3 28.9
2.17 2.34 27.0 28.4
194 292 821
— — —
123 586 402
— — —
28 2.08 529/147
0 — 0
27 2.05 480/40
0 — 0
8 23 47 186
0 0 — —
12 10 27 181
0 0 — —
1649 1051
— —
5806 602
— —
flow. Water samples were collected by holding clean PVC tubes (30 cm long; 4.5 cm inner diameter) long enough in the direction of the current to allow complete flushing of the tubes and subsequently inserting rubber stoppers at each end. Five tubes were collected both downstream and upstream of the reef at each sampling date and the downstream side was always sampled first to minimize bias caused by re-suspension. Tubes were held 1 m away from the reef and samples were taken at different parts of the cross-section to represent the integrated reef filtration activity as best possible. The water samples were filtered onto 25 mm GFF filters for Chl a determination. Filters were extracted in 90% acetone at 4C for 24 h in darkness (Parsons et al., 1985). Chl a was measured by the non-acidification method of Welschmeyer (1994) using a Turner Designs TD-700 fluorometer, and used as a proxy for microalgal biomass. Pair-wise Student t-tests were used to evaluate significant differences.
Results Quantitative results are summarized in Table 1. Comparisons between LOI and pore-water content of sediments adjacent to and further away from the reefs indicated no significant differences. However, both LOI and water content were substantially higher in sediments at the farm site than at the control site. Biomass of
An application of artificial reefs to reduce organic enrichment caused by net-cage fish farming 0.3
–1
Mean Chl a (µg l )
(a)
0.2
0.1
0 2.0 (b)
–1
Mean Chl a (µg l )
fouling organisms (invertebrates, algae, bacteria) on the reefs increased rapidly at both sites. After 1 month, the farm site had a higher biomass, but was overtaken by the control site after 2 months. While biomass increased further at the farm site reef until an all-time high after 3 months, biomass at the control site became reduced. Visual observations confirmed that the reefs attracted wild fish within hours after deployment. However, a census was not conducted at that time. Number of species and Shannon–Wiener diversity index (H ) were similar for the two reef sites, but more fish were seen at the farm site than at the control, both within the reef and outside the reef. On both reefs, the damselfish (Neopomacentrus miryae) dominated numerically, followed by the goldfish (Pseudoanthias squamipinnis). Although numbers were considerably less, the most conspicuous species in both reefs was the lionfish (Pterois miles). Fish were not observed in the control areas near the two reefs (CC and CN). Analysis of the video recordings revealed fewer fish specimens than the in situ census. The dominant species were domino damselfish (Dascyllus trimaculatus), pennantfish (Heniochus diphreutes) and P. miles. There were no consistent differences between reef sites. Four months after reef deployment, the dominant organisms at both RC and RN were solitary tunicates and bryozoa. Tunicate distribution in the cylinders was preferentially on the upper inside part of each cylinder and on the outer and upper parts of the reefs. Tunicate abundance at the control site was fourfold higher than at the fish farm site. However, 1 month later the tunicate populations in both reefs crashed, dropping to less than 50 individuals in each. Peak abundance of bryozoa occurred in the inner cylinders. Only arborescent colonies were counted (mostly Bugula spp.). In this case, abundance was about twice as high at RC than at RN. Other macro-benthic taxa observed within the reefs included sea urchins, anemones, crinoids, sponges, bivalves, gastropods, polychaetes, and crustaceans. Among the gastropods, Fusinus polygonoides was the most abundant species, with peak abundance in the bottommost row of cylinders. In comparison to the thriving communities associated with the reefs, the nearby control areas were barren. At the control area of the farm site, the sediment was covered with microbial mats dominated by the sulphideoxidizing bacterium Beggiatoa sp. and various gliding, filamentous cyanobacteria. Apart from mud snails (Nassarius sp.), no other macrofauna species were observed. The control reef was situated within beds of seagrass (Halophila stipulacea) and no microbial mats were present. The dominant macrofauna at the nearby control site included auger shells (tentatively identified as belonging to Terebridae), Nassarius sp., small hermit crabs, and sea cucumbers.
S327
1.6
1.2
0.8
RC Up
RC Down RN Up Station
RN Down
Figure 2. Summary of mean Chl a concentration (error bars: s.d.) at upstream (Up) and downstream (Down) stations relative to the RC and RN artificial reefs in (a) June and (b) September 1999 (all differences between Up and Down: p
