biofiltracion in situ

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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.

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In situ biofiltration: a means to limit the dispersal of effluents from marinefinfish cage aquaculture

Dror L. Angel1

, Noa Eden1

, Stephen Breitstein2

, Amir Yurman2

, Timor Katz1

& Ehud Spanier2

1Israel Oceanographic & Limnological Research, National Center for Mariculture, P.O.B. 1212, Eilat 88112,

Israel

E-mail: [email protected] [email protected] Leon Recanati Institute for Maritime Studies and Department of Maritime Civilizations, University of Haifa,

Mount Carmel, Haifa 31905, Israel

Key words: artificial reef, fish farm, mariculture, environmental impact, Red Sea

Abstract

Net pen fish 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 biofiltration by artificial reefs for reducing the negative environmental

impacts surrounding fish farms in the Gulf of Aqaba, Red Sea. Two triangular-shaped artificial reefs (reef volume

8.2 m3) constructed from porous durable polyethylene were deployed at 20 m; one below a commercial fish 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 fish farm effluents 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 first year of this study fish 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 artificial reefs in

order to assess the biofiltration capacity of the associated fauna. Chlorophyll a was significantly reduced to a level

1535% lower than ambient concentrations. This reduction was greatest at intermediate current speeds (310 cms1), but was not influenced by current direction. The reef structures served as a successful base for colonization

by natural fauna and flora, thereby boosting the local benthic biodiversity, and also served as effective biofilters of

phytoplankton.

Abbreviations: SAR Salmon Aquaculture Report; HDPE high density polyethylene; RC reef at fish farm; RN

control reef at North Beach; PVC polyvinyl chloride; GFF glass fiber filter; Chl a chlorophyll a; SCUBA

self-contained underwater breathing apparatus

Introduction

Marine aquaculture is a booming industry that is rap-idly spreading throughout the worlds coastal regions

(Naylor et al., 2000). One of the current major con-

cerns related to mariculture is the impact that this

activity has on the surrounding environment. In in-

tensive sea-cage aquaculture, which focuses mainly

on carnivorous species, more than half of the nitro-

gen and phosphorus delivered to the fish is released

to the marine environment as dissolved and particulate

compounds (Handy & Poxton, 1993; Enell, 1995; Lu-

patsch & Kissil, 1998) and this nutrient-rich dischargemay lead to various environmental impacts.

The most common types of impact that occur

around intensively-managed fish farms include: (a)

eutrophication and increased turbidity in the water

column around the fish cages (Gowen & Bradbury,

1987; SAR, 1998), (b) organic enrichment of the un-

derlying sediments, followed by anoxia and hydrogen


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sulfide accumulation (Holmer & Kristensen, 1992;

Angel et al., 1995), (c) emigration or death of most of

the macrofauna and meiofauna and changes in the mi-

crobial flora 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 aquaculturesites and as a result, the marine environment is im-

pacted. Nonetheless, there are several ways in which

the impacts can be reduced and thereby increase the

environmental sustainability of aquaculture.

Recent technological advances in fish nutrition

and feed delivery systems have enabled farmers to

drastically reduce the discharge of effluents from fish

farms (Beveridge, 1996). However, despite the ever-

increasing nutritional efficiency of fish rearing, there

is always release of some dissolved and particulate

matter from fish cages to the surrounding environment.

Our goal was to examine the feasibility of building

structures around fish farms that would be colonized

by organisms that could serve as a biofilter to capture

effluents released from the fish cages in order to reduce

the effect on the ecosystem. The term biofiltration is

used here to denote the uptake of dissolved and partic-

ulate compounds by living organisms. We will present

findings from an ongoing study carried out adjacent

to a commercial fish farm (Ardag) in the northern

Gulf of Aqaba in order to demonstrate the potential of

a novel biofilter to reduce some of the impacts of fish

farm effluents on the marine environment.

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 oli-

gotrophic and sea surface temperatures range from 21

to 27 C (Reiss & Hottinger, 1984). The main current

direction in the region of the fish farm is perpendic-

ular to the prevailing northern winds; generally east

to west or west to east and the mean current velocity

at 17 m is 20 cm s

1

during winter, and 5 cm s

1

during summer (Brenner et al., 1988, 1989). The nat-

ural, unenriched sediments near the farm consist of

fine 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 asso-

ciated with the seagrass beds. The soft sediments in

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 pon-

toons situated approximately 100 m apart and moored

in a northeast-southwest orientation. The pontoons

supported a series of round net cages (most cages were13 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

fish were fed dry food pellets rich in protein and lipids.

The flux of particulate matter, as measured in 1998

by sediment traps near the seafloor below the Ardag

farm ranged between 8 and 70 g m2 d1 (most values

did not exceed 40 g m2 d1) and the flux 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 artificial reefs

Two artificial 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 vari-

ous 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 artificial reef was

115 m2. The two artificial 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 fish farm. Both reefs were

moored to the seafloor (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 encom-

passing an area of seafloor equal to that of the reefs

(240 280 cm) and situated 10 m south of, and at

same depth as, the two artificial reefs were marked byropes 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


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Figure 1. Sketch of the artificial 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 artificial 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 artificial reefs, 3 settling plates wereremoved 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 wa-

ter passing via the artificial 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 fluor-

escein dye into the water and following its flow. The

water samples were collected by holding 30 cm longPVC tubes (5 cm diameter) in the direction of the cur-

rent, 1 m from the reef, for a period of time sufficient

to allow at least 2 complete flushings of the tubes be-

fore 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 or-

der to represent the integrated reef filtration activity

as best possible. The water samples were filtered onto

25 mm GFF filters for chlorophyll (chl) a determina-

tion. 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-acidification method of

Welschmeyer (1994) using a Turner Designs TD-700

fluorometer.

Quantification of fish and invertebrates in the

artificial reefs

Once every two months, the fish 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 con-

ducted cylinder-by-cylinder in order to assess the 3-

dimensional distribution of the different fish speciesin the reef. Counts were also made of fish that were

associated with, yet situated outside the reef cylinders.

On two occasions, a pair of divers enumerated macro-

invertebrates within the outermost 50 cm of the reef

cylinders of the reefs. Counts were also conducted of

fish and macrofauna in the bare control areas, south of

the reefs.


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Table 1. Summary of reef filtration measurements conducted at both RC (artificial reef below the fish farm) and RN (artificial reef 500 m

west of the farm) from June 1999 to April 2000. Reef filtration was assessed by significance of the difference ( = significant (p


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Table 2. Summary of the fish species and abundances (# fish) in three censi carried out at both artificial reefs, RC (below

the fish farm) and RN (artificial 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 fish observed both within the reef cylinders and adjacent to the reefs

Latin name English name RC RN RC RN RC RN

7/99 7/99 10/99 10/99 3/00 3/00

# fish # fish # fish # fish # fish # fish

Acanthopagrus bifasciatus Doublebar bream 5 13 17Amblyglyphidon leucogaster Whitebelly damselfish 45 5 1

Apogon aureus Golden cardinalfish 35 534 337 267 380

Apogon cyanosoma Goldstriped cardinalfish 4 207 13 37

Apogon fleurieu Flower cardinalfish 50 25

Apogon fraenatus Bridled cardinalfish 2

Apogon nigripinnis Bullseye cardinalfish 13

Apogon pseudotaniatus Doublebar cardinalfish 15 28 3 49 7 460

Apolemichtys xanthotis Yellow-ear angelfish 2 4 1

Arothron diadematus Masked puffer 2 2

Arothron hispidus Bristly puffer 1 2 1

Bodianus anthioides Lyretail hogfish 2 1

Cantherhines pardalis Wire-net filefish

Canthigaster coronata Crown toby 1Canthigaster margaritata Pearl toby 2 1 1 1 7

Chaetodon auriga Threadfin butterflyfish 1 3 4

Chaetodon faciatus Striped butterflyfish 2 1 10

Chaetodon paucifasciatus Crown butterflyfish 2 5 3

Cheiladipterus macrodon Largetooth cardinalfish 7

Cheilinus lunulatus Broomtail wrasse 5

Cheilinus mentalis Mental wrasse 2

Cheilodipterus quinquelineatus Fiveline cardinalfish 4 85 2

Chilomycetrus spilostylus Yellowspotted burrfish 6 6 7 1 7 2

Corythoichthys schultzi Gilded pipefish 1 1

Dascyllus trimaculatus Domino 57 14 47 39 139 52

Dendrochirus brachypterus Shortfin lionfish 2 1 4 1 4

Diplodus noct Arabian pinfish 1 4Epinephelus chlorostigma Brownspotted grouper 1

Epinephelus faciatus Blacktip grouper 3 3 13 3 27 4

Escenius gravieri Red Sea mimic blenny 1 1

Gymnothorax javanicus Giant moray 1 1

Heniochus diphreutes False moorish idol 55 21 7 6 11

Heniochus intermedius Red Sea bannerfish 9 11 7

Labroides dimidiatus Cleaner wrasse 1 12 19 16

Lethrinus nebulosus Spangled emperor

Meiacanthus nigrolineatus Blackline blenny 1 45 20 2 3 5

Mulloides flavolineatus Yellowstripe goatfish 20 100

Myripristis murdjan Blotcheye soldierfish 2

Neopomacentrus miryae Mirys damselfish 282 165 168 195 103 72

Ostracion cubicus Cube trunkfish 10 4 19 1 24 5Parupeneus forsskali Forsskals goatfish 7 2

Parupeneus macronema Longbarbel goatfish 4 1

Pomacanthus imperator Emperor angelfish 1 2

Pomacentrus trichourus Reticulated damselfish 1 3 1 3 1

Pseudoanthias squamipinnis Scalefin goldfish 89 156 66 78 68 56

Pseudochromis dixurus Forktail dottyback 2

Pseudochromis fridmani King salmon fish 2

Continued on p. 6


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Table 2. Continued

Latin name English name RC RN RC RN RC RN

7/99 7/99 10/99 10/99 3/00 3/00

# fish # fish # fish # fish # fish # fish

Pseudochromis springeri Bluestriped dottyback 3

Pterois miles Devil firefish 29 18 18 1 25 7

Pygolites diacanthus Royal angelfish 2

Rhinecanthus assai Picasso triggerfish 1 3 1 3 2

Sargocentron diadema Crown squirrelfish 7 8 6

Scolopsis ghanam Dotted spinecheek 3 16 10 15

Scorpaenopsis diabolus Devil scorpionfish 1 2 1 1

Sepia pharaonis cuttlefish 1 2

Siderea grisea Grey moray 5 7 9 5 18 7

Siganus luridus Dusky spinefoot 12 4 50 50

Siganus rivulatus Rivulated rabbitfish 2

Sparus aurata Gilthead seabream 13

Stephanolepis diaspros Reticulated leatherjacket

Sufflamen albicaudatus Bluethroat triggerfish 1 1

Synodus variegatus Common lizardfish 2

Tetrosomus gibbosus Thornback trunkfish 1

Thalassoma klunzingeri Klunzingers wrasse 1 1

Torpedo sinus persici Electric ray 1

unknown 1 4

unknown 2 6

unknown 3 1

unknown 4 1

Total # of individuals 676 518 1116 1144 886 1185

Total # of species 28 25 37 26 42 31

Results

Increase in reef biomass

The change in biomass of small (


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Fish populations associated with the artificial reefs

The artificial reefs became colonized by wild fish

within hours after the structures were moored to the

seafloor, however a census was not conducted at that

time. Results of the July 1999 census showed that the

dominant species in both reefs were Neopomacentrusmiryae and Pseudoanthias squamipinnis. However,

the composition of the rest of the fish community at

RC was clearly different from RN (Table 2). By Octo-

ber 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 fish communities were

dominated (>50% of all individuals) by several dif-

ferent species of cardinalfish (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 fish at RC (mainly due to a 50% re-duction in the population ofApogon aureus), yet there

was another increase in the number of species, due

mostly to the additional fish species observed around

(but not inside) the reef. In comparison, there was not

much change in the total fish 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 artificial reefs

Sessile and motile macro-invertebrates in the artificialreefs 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 bryozoaobserved were two morphs of arborescent

colonies; probably of the genus Bugula, and a variety

of encrusting colonies. During August 1999, the tu-

nicate populations in both of the reefs collapsed quite

suddenly.

Another group of very abundant attached macro-

invertebrates was the bivalvia. These settled onto the

surfaces of the reefs soon after the reefs were de-

ployed, 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 num-

bers 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 first year. The tubes were calcareous

structures that ranged in length from several mm to

several cm. Among the gastropods, the most abundantspecies observed was Fusinus polygonoides which oc-

curred 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 unidentified invertebrates.

In comparisonto the thriving biological communit-

ies associated with the artificial 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 si-

nusigerus. The RN reef was situated within beds of the

seagrass Halophila stipulacea and microbial mats did

not occur on the seafloor there. The dominant mac-

rofauna 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 sed-

iments directly below RC and RN for macrofauna or

for geochemistry because the bottom row of cylinders

in each reef entirely covered the seafloor.

An additional census, conducted at the end of

March 2000, revealed that the invertebrate communitywas still dominated by arborescent and encrusting

bryozoaand 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 Dia-

dema 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 numbersof gastropods associated with the artificial

reefs and most of the bivalves were dead.


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Discussion

Several studies have shown the combined economic

and environmental advantage in cultivation of bivalves

and macroalgae at sites adjacent to net cage fish

farms (Folke & Kautsky, 1989; Chopin & Yarish,

1998) in order to absorb the elevated levels of nu-trients and particulate matter downstream of farms.

Although we did not attempt to cultivate a specific

organism, we nonetheless found that the triangular-

shaped artificial reefs served as suitable substrates for

development of a diverse community of fish and in-

vertebrates. Laihonen et al. (1996) suggested that such

reef-associated communities may have the potential to

remove both particulate and dissolved matter from fish

farm effluents.

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 several-

fold higher than at more pristine offshore stations.

These were likely due to nutrients excreted by the

fish 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 significant chl a re-

moval values that we measured (1535% reduction;

see Table 1) were similar to the mean value (21% re-

duction) 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 efficiency of chl

a removal, our data suggest that current speed plays a

role in the ability of the reefs to capture phytoplank-

ton (Table 1). On several occasions, current speeds

were slower than 3 cm s1 and although the filtering

invertebrates could surely capture particles and phyto-

plankton that entered the reef cylinders, no significant

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 upstreamside would suddenly become the downstream side

and vice versa or water motion might suddenly stop al-

together. On one occasion (5/4/2000) current velocity

exceeded 10 cm s1 and gusted to beyond 20 cm s1,

providing an exceptionally large flux of particles to the

biofiltering invertebrates, yet apparently not giving the

filter feeders the opportunity to capture the suspended

particles. Additional measurements of reef filtration

capacity must be made in order to determine the effect

of current speed and to elucidate other variables that

may influence 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 meas-

urements. 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 artificial reefs in

Sept. 1999 (Table 1) was 0.233 mg chl a m3), a car-

bon/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 car-

bon 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 fish farms, there are also large

communities of planktonic bacteria (Angel, unpubl.)

whose growth is likely stimulated by the enriched nu-

trient environment. The waters around fish 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 fish farm such as fish feces, uneaten fish feed

and detached invertebrates and macroalgae. Many of

these compounds and planktonic organisms have the

potential to be consumed by different members ofthe reef community we found in our structures. Mac-

roalgae, bivalves (Manahan et al., 1982; Manahan,

1990) and sponges (Reiswig, 1985) are the main can-

didates for uptake of dissolved organic and inorganic

compounds. Macroalgae often covered considerable

portions of the reef surfaces and were generally pre-

valent 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 bi-

valves (Barnes, 1980). The detritivores in the reefs

include crustaceans, polychaetes, echinoderms, gast-

ropods, sponges, fish, bivalves and possibly tunicates

as well (Barnes, 1980).

Two of the abundant fish species, N. miryae and P.

squamipinnis as well as many of the other fish in the

reefs (e.g. damselfish and angelfish) were planktivores

or omnivores and thus may have played an important

role in the capture of organic particles released by the


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fish cages. Planktivorous fish can feed very efficiently,

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; Kiflawi &

Genin, 1997). There are indications that zooplankton

abundances are relatively high in the fish farm re-

gion in comparison to the natural coral reefs (Geninet al., 1995), though it is not clear whether this is

related to the enhanced phytoplankton community in

this area. At any rate, the artificial reefs can enhance

zooplankton removal by providing a habitat for both

zooplanktivorous invertebrates and fish.

Dynamics within the reef community will evid-

ently affect the capacity for removal. It is clear from

the data presented above and from the invertebratebio-

mass fluctuations (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 organ-

isms. Possible explanations for fluctuations 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 sol-

itary tunicates (3.5 fold more at RN than at RC) in

early summer 1999, followed by a dramatic disappear-

ance 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 specific pred-

ator or to natural life cycle changes, but it was more

likely due to the unusually high surface water temper-

atures (>28 C) that occurred in the Gulf of Aqaba

during August, as similar crashes of other benthic in-vertebrates, such as sponges, were observed (Yahel,

pers. comm.). In comparison to RN, there was a con-

tinuous increase in biomass of attached organisms on

RC during the first 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 bi-

valves on the artificial 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 inter-

actions with more-rapidly growing invertebrates, such

as bryozoans, polychaetes and sponges. Moreover, it

is likely that bivalves were also preyed on by fish and

invertebrates that occupied the reefs.

(3) Predatory fish, such as lionfish, groupers and

cardinalfish were among the first fish that colonized

the reef structures and are likely to have exerted top-

down pressure on some of the smaller species and

juvenile fish. Between July and October 1999, there

was an impressive increase in some of the cardinalfish

populations and a concurrent decrease in the abund-

ances ofH. diphreutes and N. miryae. We propose that

these changes in community composition were related

to fish predation and/or migration away from the reef

structures.One of the well-established impacts of fish 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 deploy-

ment, within less than 6 months there was a consid-

erable increase in the abundances and biodiversity of

fish and invertebrates associated with the structures,

whereas the adjacent control areas remained practic-

ally barren. Despite their relatively small size, the

artificial reefs had 3-dimensional geometrical com-

plexity that provided numerous niches and shelter for

a wide variety and large numbers of invertebrates and

fishes. It is noteworthy that, aside from a drop in fish

abundances at RC in March 2000, there was a con-

tinuous increase throughout the first year of this study

in both abundances and number of species at both

reefs and that the RC fish community had consistently

higher species richness than RN. In a study conduc-

ted in the early 1990s at artificial reefs situated only a

few km west of the Ardag fish farm, Golani & Diamant

(1999) found a similar increase in fish species richness

within the first 7 months, followed thereafter by a re-

duction in the number of individuals and an increasein the species diversity. Whereas many of the fish 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 fish observed in RC

and RN were recruited from the Ardag fish farm which

serves as a haven for numerous fish species (Angel et

al., 1998).

At the conclusion of the first 12 months of this field

trial, it is clear that artificial reefs and other types of

biofilters, 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 fish 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 biofilter has been established,

removal capacity of dissolved organic and inorganic

nutrients, detritus, bacterioplankton and zooplankton

should be investigated.


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10

Acknowledgements

We acknowledge Avinoam Breitstein for his assistance

in construction and deployment of the reefs, the Ar-

dag staff who kindly assisted in deployment of the

reefs and in numerous small favors, Debbie Lindell

who helped with chl a determinations and commentson this manuscript and the NCM for constant financial

and logistical support for this important and innovative

research. This study was partially supported by grant

#2098 from the Israeli Ministry of Environment.

References

Angel, D. L., P. Krost & H. Gordin, 1995. Benthic implications

of net cage aquaculture in the oligotrophic Gulf of Aqaba. Eur.

Aquacult. Soc. Spec. Publ. 25: 129173.

Angel, D. L., A. Post, S. Brenner, N. Eden, T. Katz, A. Cicelsky

& I. Lupatsch, 1998. Environmental impact assessment of the

Ardag net cage fish farm on the northern Gulf of Aqaba. A reportprepared for the Ardag Fish Company, Israel: 95 pp. (in Hebrew).

Angel, D. L., S. Verghese, J. J. Lee, A. M. Saleh, D. Zuber, D.

Lindell & A. Symons, 2000. Impact of a net cage fish farm on

the distribution of benthic foraminifera in the northern Gulf of

Eilat (Aqaba, Red Sea). J. Foram. Res. 30: 5465.

Barnes, R. D., 1980. Invertebrate Zoology. 4th edn. Saunders

College, Philadelphia: 1089 pp.

Beveridge, M. C. M. 1996. Cage Aquaculture. 2nd edn. Fishing

News Books, Oxford: 346 pp.

Black, K. B., 1998. The environmental interactions associated with

fish culture. In Black, K. D. & A. D. Pickering (eds), Biology of

Farmed Fish. Publ, CRC Press, New York: 284326.

Brenner, S., Z. Rosentroub & Y. Bishop, 1988. Current measure-

ments in the Gulf of Elat. Israel Oceanographic & Limnological

Research (IOLR) Report H3/88: 38 pp.

Brenner, S., Z. Rosentroub & Y. Bishop, 1989. Current measure-

ments in the Gulf of Elat 1988/89. IOLR Report H8/89: 31

pp.

Chopin, T. & C. Yarish, 1998. Nutrients or not nutrients? World

Aquacult. 29: 3136.

Enell, M., 1995. Environmental impact of nutrients from Nordic fish

farming. Water Sci. Technol. 31: 6171.

Fishelson, L., 1971. Ecology and distribution of the benthic fauna

in the shallow waters of the Red Sea. Mar. Biol. 10: 113130.

Folke, C. & N. Kautsky, 1989. The role of ecosystems for a

sustainable development of aquaculture. Ambio 18: 234243.

Genin, A., G. Gal & L. Haury, 1995. Copepod carcasses in the

ocean. II. Near coral reefs. Mar. Ecol. Prog. Ser. 123: 6571.

Glynn, P. W., 1973. Ecology of a Caribbean coral reef. The Porites

reef-flat biotop: Part II. Plankton community with evidence for

depletion. Mar. Biol. 22: 121.Golani, D. & A. Diamant, 1999. Fish colonization of an artificial

reef in the Gulf of Elat, northern Red Sea. Envir. Biol. Fish. 54:

275282.

Gowen, R. J. & N. B. Bradbury, 1987. The ecological impact of

salmonid farming in coastal waters: a review. Oceanogr. mar.

biol. Ann. Rev. 25: 563575.

Gowen, R. J., D. P. Weston & A. Ervik, 1991. Aquaculture and the

benthic environment: a review. In Cowey, C. B. & C. Y. Cho

(eds), Nutritional Strategies and Aquaculture Waste. University

of Guelph Press, Guelph, Canada: 187205.

Greene, L. E. & W. S. Alevison, 1989. Comparative accuracies of

visual assessment methods for coral reef fishes. Bull. mar. Sci.

44: 988912.

Hamner, W. M., M. S. Jones, J. H. Carleton, I. R. Hauri & D.

McB. Williams, 1988. Zooplankton, planktivorous fish and watercurrents on a windward reef face: Great Barrier Reef, Australia.

Bull. mar. Sci. 42: 459479.

Handy, R. D. & M. G. Poxton, 1993. Nitrogen pollution in mari-

culture toxicity and excretion of nitrogenous compounds by

marine fish. Rev. Fish Biol. Fisheries 3: 205241.

Holmer, M. & E. Kristensen, 1992. Impact of marine fish cage

farming on metabolism and sulfate reduction of underlying

sediments. Mar. Ecol. Prog. Ser. 80: 191201.

Kiflawi, M. & A. Genin, 1997. Prey flux manipulation and the

feeding rates of reef-dwelling planktivorous fish. Ecology 78:

10621077.

Laihonen, P., J. Hnnunen, J. Chojnacki & I. Vuorinen, 1996. Some

prospects of nutrient removal with artificial reefs. In Jensen, A.

C. (ed.), Proceedings of the 1st EARRN (European Artificial

Reef Research Network). Ancona, Italy: 8596.

Lupatch I. & G. W. Kissil, 1998. Predicting aquaculture waste from

gilthead seabream (Sparus aurata) culture using a nutritional

approach. Aquat. Living Resour. 11: 265268.

Manahan, D., 1990. Adaptations by invertebrate larvae for nutrient

acquisition from seawater. Am. Zool. 30: 147160.

Manahan, D., S. H. Wright, G. C. Stevens & M. A. Rice, 1982.

Transport of dissolved amino acides by the mussel, Mytilus

edulis: demonstration of net uptake from natural seawater. Sci-

ence 215: 12531255.

Naylor, R. L., R. J. Goldburg, J. H. Primavera, N. Kautsky, M. C.

M. Beveridge, J. Clay, C. Folke, J. Lubchenco, H. Mooney & M.

Troell, 2000. Effect of aquaculture on world fish supplies. Nature

405: 10171024.

Parsons, T. R., M. Takahashi & B. Hargrave, 1977. Biological

Oceanographic Processes. Pergamon Press, N.Y.: 332 pp.

Parsons, T. R., Y. Maita & C. M. Lalli, 1985. A Manual of Chemicaland Biological Methods for Seawater Analysis. Pergamon Press,

N.Y.: 173 pp.

Reiss Z. & L. Hottinger, 1984. The Gulf of Aqaba: Ecological

Micropaleontology, Springer-Verlag, Berlin: 354 pp.

Reiswig, H. M., 1985. In situ feeding in two shallow-water hex-

actinellid sponges. In Rutzler, K. (ed.), New Perspectives in

Sponge Biology. Smithsonian Institution Press, Washington, DC:

504510.

Salmon Aquaculture Review, 1998. Environmental Assessment

Office, British Columbia, Canada: 1500 pp.

Welschmeyer, N. A., 1994. Fluorometric analysis of chlorophyll

a in the presence of chlorophyll b and phaeopigments. Limnol.

Oceanogr. 39: 19851992.

Weston, D. P., 1990. Quantitative examination of macrobenthic

community changes along an organic enrichment gradient. Mar.

Ecol. Prog. Ser. 61: 23324.Yahel, G., A. F. Post, K. Fabricius, M. Dominique, D. Vaulot & A.

Genin, 1998. Phytoplankton distribution and grazing near coral

reefs. Limnol. Oceanogr. 43: 551563.

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