Hydrobiologia 469: 110, 2002. S.A. Ostroumov, S.C. McCutcheon & C.E.W.

Steinberg (eds), Ecological Processes and Ecosystems. 2002 Kluwer Academic Publishers. Printed in the Netherlands.

In situ bioltration: a means to limit the dispersal of efuents from marine nsh cage aquaculture
Dror L. Angel1 , Noa Eden1 , Stephen Breitstein2 , Amir Yurman2, Timor Katz1 & Ehud Spanier2
Oceanographic & Limnological Research, National Center for Mariculture, P.O.B. 1212, Eilat 88112, Israel E-mail: angel@agri.huji.ac.il dror@mit.edu 2 The Leon Recanati Institute for Maritime Studies and Department of Maritime Civilizations, University of Haifa, Mount Carmel, Haifa 31905, Israel Key words: articial reef, sh farm, mariculture, environmental impact, Red Sea
1 Israel

Abstract Net pen sh farms generally enrich the surrounding waters and the underlying sediments with nutrients and organic matter, and these loadings can cause a variety of environmental problems, such as algal blooms and sediment anoxia. In this study we test the potential of bioltration by articial reefs for reducing the negative environmental impacts surrounding sh farms in the Gulf of Aqaba, Red Sea. Two triangular-shaped articial reefs (reef volume 8.2 m3 ) constructed from porous durable polyethylene were deployed at 20 m; one below a commercial sh farm and the other 500 m west of this farm in order to monitor the colonization of these reefs by the local fauna and to determine whether the reef community can remove sh farm efuents from the water. Both reefs became rapidly colonized by a wide variety of organisms with potential for the removal of compounds released from the farms. Within the rst year of this study sh abundances and the number of species reached 5181185 individuals per reef and 2542 species per reef. Moreover, numerous benthic algae; small sessile invertebrates (bryozoa, tunicates, bivalves, polychaetes, sponges, anemones) and large motile macrofauna (crustaceans, sea urchins, gastropods) settled on the reef surfaces. Depletion of chlorophyll a was measured in the water traversing the articial reefs in order to assess the bioltration capacity of the associated fauna. Chlorophyll a was signicantly reduced to a level 1535% lower than ambient concentrations. This reduction was greatest at intermediate current speeds (310 cm s1 ), but was not inuenced by current direction. The reef structures served as a successful base for colonization by natural fauna and ora, thereby boosting the local benthic biodiversity, and also served as effective biolters of phytoplankton. Abbreviations: SAR Salmon Aquaculture Report; HDPE high density polyethylene; RC reef at sh farm; RN control reef at North Beach; PVC polyvinyl chloride; GFF glass ber lter; Chl a chlorophyll a; SCUBA self-contained underwater breathing apparatus Introduction Marine aquaculture is a booming industry that is rapidly spreading throughout the worlds coastal regions (Naylor et al., 2000). One of the current major concerns related to mariculture is the impact that this activity has on the surrounding environment. In intensive sea-cage aquaculture, which focuses mainly on carnivorous species, more than half of the nitrogen and phosphorus delivered to the sh is released to the marine environment as dissolved and particulate compounds (Handy & Poxton, 1993; Enell, 1995; Lupatsch & Kissil, 1998) and this nutrient-rich discharge may lead to various environmental impacts. The most common types of impact that occur around intensively-managed sh farms include: (a) eutrophication and increased turbidity in the water column around the sh cages (Gowen & Bradbury, 1987; SAR, 1998), (b) organic enrichment of the underlying sediments, followed by anoxia and hydrogen

2 sulde accumulation (Holmer & Kristensen, 1992; Angel et al., 1995), (c) emigration or death of most of the macrofauna and meiofauna and changes in the microbial ora in the sediments under the cages (Weston, 1990; SAR, 1998). Although some of these impacts may be reduced by proper a priori site selection, there are often constraints involved in choice of aquaculture sites and as a result, the marine environment is impacted. Nonetheless, there are several ways in which the impacts can be reduced and thereby increase the environmental sustainability of aquaculture. Recent technological advances in sh nutrition and feed delivery systems have enabled farmers to drastically reduce the discharge of efuents from sh farms (Beveridge, 1996). However, despite the everincreasing nutritional efciency of sh rearing, there is always release of some dissolved and particulate matter from sh cages to the surrounding environment. Our goal was to examine the feasibility of building structures around sh farms that would be colonized by organisms that could serve as a biolter to capture efuents released from the sh cages in order to reduce the effect on the ecosystem. The term bioltration is used here to denote the uptake of dissolved and particulate compounds by living organisms. We will present ndings from an ongoing study carried out adjacent to a commercial sh farm (Ardag) in the northern Gulf of Aqaba in order to demonstrate the potential of a novel biolter to reduce some of the impacts of sh farm efuents on the marine environment. this region contain abundant foraminiferal tests (Angel et al., 2000). The farm began operation in 1988 and in 1999 it consisted of three parallel 100150 m long steel pontoons situated approximately 100 m apart and moored in a northeast-southwest orientation. The pontoons supported a series of round net cages (most cages were 13 m diameter; 10 m deep) for production of gilthead seabream (Sparus aurata), stocked at between 20 and 25 kg m3 . During 1999, annual production at the Ardag farm was approximately 1200 tons. The caged sh were fed dry food pellets rich in protein and lipids. The ux of particulate matter, as measured in 1998 by sediment traps near the seaoor below the Ardag farm ranged between 8 and 70 g m2 d1 (most values did not exceed 40 g m2 d1 ) and the ux of organic carbon ranged from 2 to 30 g m2 d1 (most values did not exceed 20 g m2 d1 ) (Angel et al., 1998).

Materials and methods Deployment of the articial reefs Two articial reef units were constructed from 4 mm thick, 70 mm mesh white high-density polyethylene (HDPE) sheets rolled into cylinders. The cylinders were reinforced by attaching rectangular 40 mm mesh sheets as vertical and horizontal partitions. Plastic tie wraps were used to fasten the cylinders, to secure the partitions inside the cylinders and to connect the various parts of the reefs together. Each reef consisted of 28 40-cm diameter cylinders arranged in a triangular shape with a 280 240 cm base and 240 cm height (Fig. 1). The surface area of each articial reef was 115 m2 . The two articial reefs (RC and RN) were deployed on March 26, 1999; RC was placed below the northwestern side of the Ardag farm and RN was located 500 m west of the sh farm. Both reefs were moored to the seaoor (20 m depth) by means of ropes tied to four 50 mm PVC pipes that were inserted to a depth of 2.5 m into the sediment. Sites encompassing an area of seaoor equal to that of the reefs (240 280 cm) and situated 10 m south of, and at same depth as, the two articial reefs were marked by ropes and served as a control for comparison of faunal colonization. Changes in the biomass of attached organisms Seventy-two 30 45 cm plates were prepared with the same 70 mm HDPE used to construct the reefs

Description of sites studied The Ardag farm is located at the northern end of the Gulf of Aqaba (Red Sea), about 300 m offshore next to the Israel-Jordan border at 34 58 40 E, 29 32 45 N (Angel et al., 2000). The Gulf waters are generally oligotrophic and sea surface temperatures range from 21 to 27 C (Reiss & Hottinger, 1984). The main current direction in the region of the sh farm is perpendicular to the prevailing northern winds; generally east to west or west to east and the mean current velocity at 17 m is 20 cm s1 during winter, and 5 cm s1 during summer (Brenner et al., 1988, 1989). The natural, unenriched sediments near the farm consist of ne sand that support a wide variety of soft-bottom invertebrates (Fishelson, 1971), seagrasses (mainly Halophila stipulacea), benthic medusae (Cassiopeia andromeda) and demersal and epiphytic species associated with the seagrass beds. The soft sediments in

Figure 1. Sketch of the articial reef showing the elongated triangular structure made of 40 cm diameter plastic cylinders. Reef dimensions are: 240 cm length 280 cm width 240 cm height; both articial reefs, RC and RN, had identical dimensions. The cylinders were numbered for reference and to facilitate census work.

and were labelled and weighed. The plates were bent and attached in a convex shape on the outer sides of the external cylinders of the reefs in order to resemble the reef surfaces, so that these could be sampled to document change in reef biomass without affecting the integrity of the reefs. In order to monitor changes in the community of organisms associated with the surfaces of the articial reefs, 3 settling plates were removed from each of the reefs every other month and these were photographed, dried and weighed. Particulate matter removal rates In order to quantify the removal of algae from the water passing via the articial reefs, water samples were taken upstream and downstream of the reefs, after Yahel et al. (1998). Direction and speed of the current were determined before sampling by releasing uorescein dye into the water and following its ow. The water samples were collected by holding 30 cm long PVC tubes (5 cm diameter) in the direction of the current, 1 m from the reef, for a period of time sufcient to allow at least 2 complete ushings of the tubes before sealing these with rubber stoppers. Water samples were collected from 5 different positions at each side of the reef on each sampling date (see Table 1) in order to represent the integrated reef ltration activity

as best possible. The water samples were ltered onto 25 mm GFF lters for chlorophyll (chl) a determination. Filters were extracted in 90% acetone in the dark at 4 C for 24 h, following Parsons et al. (1985). Chl a was measured by the non-acidication method of Welschmeyer (1994) using a Turner Designs TD-700 uorometer.

Quantication of sh and invertebrates in the articial reefs Once every two months, the sh associated with the reefs were enumerated by both: (a) visual tallying by a pair of divers (Greene & Alevizon, 1989) and (b) video recordings of the reefs and the control areas. Both visual counts and video photography were conducted cylinder-by-cylinder in order to assess the 3dimensional distribution of the different sh species in the reef. Counts were also made of sh that were associated with, yet situated outside the reef cylinders. On two occasions, a pair of divers enumerated macroinvertebrates within the outermost 50 cm of the reef cylinders of the reefs. Counts were also conducted of sh and macrofauna in the bare control areas, south of the reefs.

4
Table 1. Summary of reef ltration measurements conducted at both RC (articial reef below the sh farm) and RN (articial reef 500 m west of the farm) from June 1999 to April 2000. Reef ltration was assessed by signicance of the difference ( = signicant (p<0.01); = highly signicant (p<0.001); ns = not signicant) between mean ( standard deviation) chlorophyll a concentrations (mg m3 ) upstream (up) versus downstream (dwn) of the reefs and the percent (%) reduction in chl a concentration. For each date, current direction and velocity (Vel) at each of the articial reefs is also presented Date RC Up Chl a (mg m3 ) 0.244 0.014 1.639 0.080 0.314 0.019 0.318 0.024 1.858 0.360 RC Dwn Chl a (mg m3 ) 0.193 0.022 1.376 0.123 0.234 0.021 0.322 0.015 1.723 0.521 RC % reduction 21 16 25 1ns 7ns 1.825 0.040 0.940 0.025 0.696 0.052 26 1.857 0.070 2ns 0.428 0.080 0.370 0.051 14ns RN Up Chl a (mg m3 ) 0.244 0.035 1.324 0.065 RN Dwn Chl a (mg m3 ) 0.157 0.024 1.121 0.104 RN % reduction 35 15 Current Direction Current Vel RC (cm s1 ) 6 5 6 <2 03 1020 4 5 Current Vel RN (cm s1 ) 3 10

13.6.99 9.9.99 21.11.99 27.2.00 4.4.00 5.4.00 10.4.00

W E W RC: variable RN: W variable W E

Figure 2. Summary of temporal changes in the biomass (kg) of attached organisms (mostly benthic invertebrates) on the surfaces of the two articial reefs, RC (below the sh farm) and RN (articial reef 500 m west of the farm). Biomasses were estimated for each of the reefs by extrapolating the mean weight increase recorded on three 35 40 cm pieces of reef material to the surface area of the entire reef.

5
Table 2. Summary of the sh species and abundances (# sh) in three censi carried out at both articial reefs, RC (below the sh farm) and RN (articial reef 500 m west of the farm), in July 1999 (7/99), October 1999 (10/99) and in March 2000 (3/00). The data include sh observed both within the reef cylinders and adjacent to the reefs Latin name English name RC 7/99 # sh RN 7/99 # sh RC 10/99 # sh 5 45 534 4 25 2 15 2 1 28 3 2 2 2 1 1 3 1 2 13 49 7 4 460 1 2 1 1 RN 10/99 # sh RC 3/00 # sh 13 1 267 13 RN 3/00 # sh 17 380 37

Acanthopagrus bifasciatus Amblyglyphidon leucogaster Apogon aureus Apogon cyanosoma Apogon eurieu Apogon fraenatus Apogon nigripinnis Apogon pseudotaniatus Apolemichtys xanthotis Arothron diadematus Arothron hispidus Bodianus anthioides Cantherhines pardalis Canthigaster coronata Canthigaster margaritata Chaetodon auriga Chaetodon faciatus Chaetodon paucifasciatus Cheiladipterus macrodon Cheilinus lunulatus Cheilinus mentalis Cheilodipterus quinquelineatus Chilomycetrus spilostylus Corythoichthys schultzi Dascyllus trimaculatus Dendrochirus brachypterus Diplodus noct Epinephelus chlorostigma Epinephelus faciatus Escenius gravieri Gymnothorax javanicus Heniochus diphreutes Heniochus intermedius Labroides dimidiatus Lethrinus nebulosus Meiacanthus nigrolineatus Mulloides avolineatus Myripristis murdjan Neopomacentrus miryae Ostracion cubicus Parupeneus forsskali Parupeneus macronema Pomacanthus imperator Pomacentrus trichourus Pseudoanthias squamipinnis Pseudochromis dixurus Pseudochromis fridmani

Doublebar bream Whitebelly damselsh Golden cardinalsh Goldstriped cardinalsh Flower cardinalsh Bridled cardinalsh Bullseye cardinalsh Doublebar cardinalsh Yellow-ear angelsh Masked puffer Bristly puffer Lyretail hogsh Wire-net lesh Crown toby Pearl toby Threadn butterysh Striped butterysh Crown butterysh Largetooth cardinalsh Broomtail wrasse Mental wrasse Fiveline cardinalsh Yellowspotted burrsh Gilded pipesh Domino Shortn lionsh Arabian pinsh Brownspotted grouper Blacktip grouper Red Sea mimic blenny Giant moray False moorish idol Red Sea bannersh Cleaner wrasse Spangled emperor Blackline blenny Yellowstripe goatsh Blotcheye soldiersh Mirys damselsh Cube trunksh Forsskals goatsh Longbarbel goatsh Emperor angelsh Reticulated damselsh Scalen goldsh Forktail dottyback King salmon sh

35 50

5 337 207

2 1 2

1 4 10

3 7 5 2 7 1 139 1 4 27 1 1 11 11 19 3

2 6 57 2 6 14 1 4 7 47 1 3 3 13 1 3 85 1 39 4 2 1 52 4

4 1 1 7 16 5

55 1 1 2 282 10

21

7 9 12 20 20 168 19 7 1 2 3 66

45

2 100 195 1

165 4 4

103 24 2

72 5

1 89 2 1 156

1 78

3 68 2

1 56

Continued on p. 6

6
Table 2. Continued Latin name English name RC 7/99 # sh RN 7/99 # sh RC 10/99 # sh 3 18 2 3 7 16 RN 10/99 # sh RC 3/00 # sh RN 3/00 # sh

Pseudochromis springeri Pterois miles Pygolites diacanthus Rhinecanthus assai Sargocentron diadema Scolopsis ghanam Scorpaenopsis diabolus Sepia pharaonis Siderea grisea Siganus luridus Siganus rivulatus Sparus aurata Stephanolepis diaspros Sufamen albicaudatus Synodus variegatus Tetrosomus gibbosus Thalassoma klunzingeri Torpedo sinus persici

Bluestriped dottyback Devil resh Royal angelsh Picasso triggersh Crown squirrelsh Dotted spinecheek Devil scorpionsh cuttlesh Grey moray Dusky spinefoot Rivulated rabbitsh Gilthead seabream Reticulated leatherjacket Bluethroat triggersh Common lizardsh Thornback trunksh Klunzingers wrasse Electric ray unknown 1 unknown 2 unknown 3 unknown 4

29 1

18

1 1

25 3 8 10 1 18 50 13

7 2 6 15

1 5 12

3 2 1 7 4 2

9 50

1 2 5

1 2 1 1 4 6 1 1 518 25

1 1

Total # of individuals Total # of species

676 28

1116 37

1144 26

886 42

1185 31

Results Increase in reef biomass The change in biomass of small (<5 cm), sessile organisms (invertebrates, algae, bacteria) on the reefs was assessed by weighing representative sampling plates and extrapolating this to calculate a weight gain for the entire reef (Fig. 2). Initially, there was a similar biomass increase in both reefs, yet within three months the biomass of attached organisms on RN was almost 2-fold greater than on RC. The biomass peak was mainly attributed to a solitary benthic tunicate that was considerably more abundant at RN than at RC (see below). However, in September 1999 there was a reversal in this pattern and the attached biomass on RC was double that on RN, as a result of the collapse of the tunicate population on both reefs and a large increase in the bivalve population on RC. This trend prevailed through November 1999, but by February 2000, the

estimated biomass of attached organisms on both reefs reached similar values, slightly less than 700 kg per reef.

Particulate matter removal rates The ltration efciency of the articial reefs was assessed by comparing microalgal pigment levels (estimated by chl a concentration) in the water mass upstream vs downstream of the reefs (Table 1). Chlorophyll a concentrations at the study sites were highest in September 1999 and in April 2000, but removal efciency was not affected by ambient chl a concentration. On dates when current speeds were intermediate (310 cm s1 ), irrespective of the current direction, removal was signicant and ranged between 15 and 35% (n=6). However, on occasions when the current speed was below 3 cm s1 and once, when the speed was greater than 10 cm s1 , removal was insignicant.

7 Fish populations associated with the articial reefs The articial reefs became colonized by wild sh within hours after the structures were moored to the seaoor, however a census was not conducted at that time. Results of the July 1999 census showed that the dominant species in both reefs were Neopomacentrus miryae and Pseudoanthias squamipinnis. However, the composition of the rest of the sh community at RC was clearly different from RN (Table 2). By October 1999 (6 months after reef deployment), there was a substantial increase in both the number of species and the number of individuals at both reefs with more species at RC. In both reefs, the sh communities were dominated (>50% of all individuals) by several different species of cardinalsh (Apogon spp.); with A. aureus the most common of the Apogon species. The census carried out at the end of March 2000 (1 year after the start of this study) indicated a clear drop in total abundance of sh at RC (mainly due to a 50% reduction in the population of Apogon aureus), yet there was another increase in the number of species, due mostly to the additional sh species observed around (but not inside) the reef. In comparison, there was not much change in the total sh abundance at RN, though there was also an increase in the number of species. Fish were seldom observed in the control areas near the two reefs. Invertebrate populations in the articial reefs Sessile and motile macro-invertebrates in the articial reefs were enumerated by SCUBA divers 3 months after reef deployment and the dominant organisms in both RC and RN were solitary tunicates and bryozoa. The bryozoa observed were two morphs of arborescent colonies; probably of the genus Bugula, and a variety of encrusting colonies. During August 1999, the tunicate populations in both of the reefs collapsed quite suddenly. Another group of very abundant attached macroinvertebrates was the bivalvia. These settled onto the surfaces of the reefs soon after the reefs were deployed, and by June 1999 large numbers of the small (12 mm) spat were recognizable, but these were too numerous to enumerate. By the end of August 1999, there were 100200 bivalves, ranging in size from 3 to 30 mm, on each of the settling plates that was sampled. If we assume similar abundances throughout the reef, there were several hundred thousand bivalves (mostly oysters) per reef. Tube-forming polychaetes settled on the surfaces of the reefs and their numbers exceeded several hundred individuals per settling plate within 6 months of reef deployment and in most cases reached 1000 individuals or more per plate by the end of the rst year. The tubes were calcareous structures that ranged in length from several mm to several cm. Among the gastropods, the most abundant species observed was Fusinus polygonoides which occurred mainly in the lower rows of cylinders in both reefs. In addition to the above, macroalgae and several other macro-benthic taxa were observed on and within the reef structures, including sea urchins, anemones, crinoids, sponges, gastropods, crustaceans and various cryptic and unidentied invertebrates. In comparison to the thriving biological communities associated with the articial reefs, the nearby control areas were practically barren. At the control area near RC the sediment was occasionally covered with microbial mats and the only macro-invertebrate observed there was the local mud snail, Nassarius sinusigerus. The RN reef was situated within beds of the seagrass Halophila stipulacea and microbial mats did not occur on the seaoor there. The dominant macrofauna on the sandy sediments surrounding RN and at the nearby control site consisted of auger shells, Nassarius spp., small hermit crabs, sea urchins and sea cucumbers. It was not possible to examine the sediments directly below RC and RN for macrofauna or for geochemistry because the bottom row of cylinders in each reef entirely covered the seaoor. An additional census, conducted at the end of March 2000, revealed that the invertebrate community was still dominated by arborescent and encrusting bryozoa and a variety of solitary tunicates, with similar abundances at both reefs. However, the coverage of arborescent bryozoa was greater on the western side than on the eastern side of each reef. The numbers and variety of sea urchins had increased at both reefs and these echinoderms were concentrated mostly on the eastern sides of the reefs. At RC the sea urchin population was almost exclusively composed of Diadema sp., whereas at RN there were roughly equal numbers of Tripneustes sp. and Diadema sp. There was a general increase in the abundances of sponges (mostly encrusting) at both reefs with greater numbers at RN than at RC and most of the sponges at RN on the eastern side. There was also a clear decrease in the numbers of gastropods associated with the articial reefs and most of the bivalves were dead.

8 Discussion Several studies have shown the combined economic and environmental advantage in cultivation of bivalves and macroalgae at sites adjacent to net cage sh farms (Folke & Kautsky, 1989; Chopin & Yarish, 1998) in order to absorb the elevated levels of nutrients and particulate matter downstream of farms. Although we did not attempt to cultivate a specic organism, we nonetheless found that the triangularshaped articial reefs served as suitable substrates for development of a diverse community of sh and invertebrates. Laihonen et al. (1996) suggested that such reef-associated communities may have the potential to remove both particulate and dissolved matter from sh farm efuents. Angel et al. (1998; unpublished) found that the waters immediately surrounding the Ardag farm (100 300 m radius) had levels of chl a that were severalfold higher than at more pristine offshore stations. These were likely due to nutrients excreted by the sh that were rapidly taken up by algae, leading to increased algal biomass. Therefore, algal uptake constitutes indirect removal of nutrients from these waters. Moreover, particulate chl a removal can serve as a proxy for removal of suspended particles from the water column. The range of signicant chl a removal values that we measured (1535% reduction; see Table 1) were similar to the mean value (21% reduction) reported by Yahel et al. (1998) who examined the uptake of chl a after passage of water via a natural perforated reef at the nearby Eilat Oil Terminal. Whereas neither ambient chl a concentrations nor current direction seemed to affect the efciency of chl a removal, our data suggest that current speed plays a role in the ability of the reefs to capture phytoplankton (Table 1). On several occasions, current speeds were slower than 3 cm s1 and although the ltering invertebrates could surely capture particles and phytoplankton that entered the reef cylinders, no signicant differences between chl a levels on the two sides of the reefs were observed. When currents were sluggish (1 2 cm s1 ), there were often shifts in current direction and velocity such that during sampling the upstream side would suddenly become the downstream side and vice versa or water motion might suddenly stop altogether. On one occasion (5/4/2000) current velocity exceeded 10 cm s1 and gusted to beyond 20 cm s1 , providing an exceptionally large ux of particles to the bioltering invertebrates, yet apparently not giving the lter feeders the opportunity to capture the suspended particles. Additional measurements of reef ltration capacity must be made in order to determine the effect of current speed and to elucidate other variables that may inuence chl a removal. Algal planktivores on the reefs likely to be responsible for chl a depletion include bivalves, tunicates, sponges, polychaetes and bryozoa (Barnes, 1980). The following is an example of a reef carbon uptake rate calculation based on chl a removal measurements. If we take the summer mean current velocity below the farm (5 cm s1 ), the amount of chl a taken up by the reef (mean uptake by the articial reefs in Sept. 1999 (Table 1) was 0.233 mg chl a m3 ), a carbon/chlorophyll a conversion ratio of 60 (Parsons et al., 1977) and the reef dimensions (length = 2.40 m, volume = 9.56 m3 ), the estimated uptake of algal carbon by the reef in summer is 240 g d1 . This is a conservative carbon removal estimate because algal carbon uptake is likely to be only part of the total carbon absorbed by the reef. In addition to high algal biomass in the waters around commercial sh farms, there are also large communities of planktonic bacteria (Angel, unpubl.) whose growth is likely stimulated by the enriched nutrient environment. The waters around sh farms are often also enriched in organic and inorganic nutrients and detritus (Black, 1998). Sources of detritus and particulate organic matter include materials released from the sh farm such as sh feces, uneaten sh feed and detached invertebrates and macroalgae. Many of these compounds and planktonic organisms have the potential to be consumed by different members of the reef community we found in our structures. Macroalgae, bivalves (Manahan et al., 1982; Manahan, 1990) and sponges (Reiswig, 1985) are the main candidates for uptake of dissolved organic and inorganic compounds. Macroalgae often covered considerable portions of the reef surfaces and were generally prevalent on the regions that received the most light, whereas sponges and bivalves were generally found on the inner sides of the cylinders. Bacterioplankton are consumed by sponges, tunicates, bryozoa and bivalves (Barnes, 1980). The detritivores in the reefs include crustaceans, polychaetes, echinoderms, gastropods, sponges, sh, bivalves and possibly tunicates as well (Barnes, 1980). Two of the abundant sh species, N. miryae and P. squamipinnis as well as many of the other sh in the reefs (e.g. damselsh and angelsh) were planktivores or omnivores and thus may have played an important role in the capture of organic particles released by the

9 sh cages. Planktivorous sh can feed very efciently, removing as much as 50% or more of the plankton reaching them if the current is neither too swift nor slow (Glynn, 1973; Hamner et al., 1988; Kiawi & Genin, 1997). There are indications that zooplankton abundances are relatively high in the sh farm region in comparison to the natural coral reefs (Genin et al., 1995), though it is not clear whether this is related to the enhanced phytoplankton community in this area. At any rate, the articial reefs can enhance zooplankton removal by providing a habitat for both zooplanktivorous invertebrates and sh. Dynamics within the reef community will evidently affect the capacity for removal. It is clear from the data presented above and from the invertebrate biomass uctuations (Fig. 2) that an equilibrium among the reef occupants has yet to be achieved. Many of the dramatic changes documented over the course of the year are likely to be due to interactions among organisms. Possible explanations for uctuations in the reef community are discussed below. (1) The sharp rise and fall in invertebrate biomass at RN (Fig. 2), was due to a massive buildup of solitary tunicates (3.5 fold more at RN than at RC) in early summer 1999, followed by a dramatic disappearance of this population toward the end of August. The collapse of the tunicate populations in both reefs may have been related to the appearance of a specic predator or to natural life cycle changes, but it was more likely due to the unusually high surface water temperatures (>28 C) that occurred in the Gulf of Aqaba during August, as similar crashes of other benthic invertebrates, such as sponges, were observed (Yahel, pers. comm.). In comparison to RN, there was a continuous increase in biomass of attached organisms on RC during the rst 6 months of this study because the dominant invertebrates were not tunicates but rather bivalves which persisted throughout the summer. (2) Despite rather impressive recruitment of bivalves on the articial reefs during the summer of 1999, very few grew beyond a length of 3 or 4 cm and by February 2000, most of the bivalves had died. Bivalve mortalities may have been affected by interactions with more-rapidly growing invertebrates, such as bryozoans, polychaetes and sponges. Moreover, it is likely that bivalves were also preyed on by sh and invertebrates that occupied the reefs. (3) Predatory sh, such as lionsh, groupers and cardinalsh were among the rst sh that colonized the reef structures and are likely to have exerted topdown pressure on some of the smaller species and juvenile sh. Between July and October 1999, there was an impressive increase in some of the cardinalsh populations and a concurrent decrease in the abundances of H. diphreutes and N. miryae. We propose that these changes in community composition were related to sh predation and/or migration away from the reef structures. One of the well-established impacts of sh farms is the reduction in biodiversity of fauna in and on the surrounding sediments (Weston, 1990; Gowen et al., 1991). Although it was not possible to examine the macrobenthos in the sediments below the reefs to establish whether this changed following reef deployment, within less than 6 months there was a considerable increase in the abundances and biodiversity of sh and invertebrates associated with the structures, whereas the adjacent control areas remained practically barren. Despite their relatively small size, the articial reefs had 3-dimensional geometrical complexity that provided numerous niches and shelter for a wide variety and large numbers of invertebrates and shes. It is noteworthy that, aside from a drop in sh abundances at RC in March 2000, there was a continuous increase throughout the rst year of this study in both abundances and number of species at both reefs and that the RC sh community had consistently higher species richness than RN. In a study conducted in the early 1990s at articial reefs situated only a few km west of the Ardag sh farm, Golani & Diamant (1999) found a similar increase in sh species richness within the rst 7 months, followed thereafter by a reduction in the number of individuals and an increase in the species diversity. Whereas many of the sh that appeared in the reefs described by Golani & Diamant (1999) were recruited from nearby natural reefs, it is likely that a large number of the sh observed in RC and RN were recruited from the Ardag sh farm which serves as a haven for numerous sh species (Angel et al., 1998). At the conclusion of the rst 12 months of this eld trial, it is clear that articial reefs and other types of biolters, such as structures for cultivation of bivalves or macroalgae (Laihonen et al., 1996), can be useful for reducing some of the environmental impacts of commercial marine sh farms. As discussed above, it is likely that the reefs remove much more carbon than was inferred from chl a removal. Now that the potential of the reefs as a biolter has been established, removal capacity of dissolved organic and inorganic nutrients, detritus, bacterioplankton and zooplankton should be investigated.

10 Acknowledgements We acknowledge Avinoam Breitstein for his assistance in construction and deployment of the reefs, the Ardag staff who kindly assisted in deployment of the reefs and in numerous small favors, Debbie Lindell who helped with chl a determinations and comments on this manuscript and the NCM for constant nancial and logistical support for this important and innovative research. This study was partially supported by grant #2098 from the Israeli Ministry of Environment.
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