REHABILITATION OF CORAL REEF-FISH

BULLETIN OF MARINE SCIENCE, 70(1): 185–197, 2002

CORAL REEF PAPER

REHABILITATION OF CORAL REEF-FISH COMMUNITIES: THE IMPORTANCE OF ARTIFICIAL-REEF RELIEF TO RECRUITMENT RATES Gil Rilov and Yehuda Benayahu ABSTRACT The present study demonstrates that, when considering artificial reefs as potential tools to assist restoration of degraded coral reefs, the construction of complex vertical structures is preferable over low-relief ones to achieve rapid recruitment of coral reef fish. Previous studies have demonstrated that the coral reef fish assemblage on unplanned vertical artificial structures in Eilat, Red Sea, have higher abundance and species richness than nearby natural reefs. In the present study, we tested the hypothesis that high relief artificial reefs had higher recruitment of coral reef fishes, mainly planktivores, than near-bottom low-relief artificial reefs. Indeed, recruitment was about two orders of magnitude higher to the experimental vertical installations than to the near-bottom ones. Most of the initial recruitment occurred at the upper sections of the vertical installations, which may indicate near surface movement of fish larvae as they approach the shore. Alternatively, it may result from preference by planktivorous species for areas with high water/ plankton flux. These results demonstrate that even small, simply-structured, installations with an appropriate orientation and shelter can attract a great number of coral reef fish recruits.

While marine reserves are strongly advocated by many managers and biologists as the main conservation management strategy (Allison et al., 1998; McClanahan, 1999), artificial reefs (ARs) have also been suggested as a potential tool to assist the restoration of marine habitats (e.g., Kenchington, 1988; Pratt, 1994). It is well established that many coral reef systems around the world suffer from extensive degradation due to anthropogenic stresses, such as destructive fishing methods, coral mining, coastal development, pollution, and tourist activity (Richmond, 1993; Wilkinson et al., 1997; McClanahan, 1999). Loss of habitat caused by tourist activity is one of the major problems in reef conservation (Van Treeck and Schuhmacher, 1998). Visitors to coral reefs worldwide break corals and disrupt sediment (Neil, 1990; Riegel and Velimirov, 1991; Hawkins and Roberts, 1992, 1993, 1997; Chadwick-Furman, 1997), leading to a decrease in reef spatial-complexity. This, in turn, reduces species richness and diversity of fishes on coral reefs (Sano et al., 1984; Dennis and Bright, 1988), since shelter is one of the major limiting factors for settlement of fish (Robertson et al., 1981; Hixon and Beets, 1993). The creation of well-planned artificial habitats may offer alternative shelters, which are expected to attract new recruits, increase their survival rate, and thus enlarge the overall pool of fish in the area (Alevizon and Gorham, 1989; Ambrose and Swarbrick, 1989). ARs of different types have been used for decades for a variety of purposes. Most research of ARs has focused primarily on their potential to enhance fishing grounds (e.g., Bohnsack et al., 1991; Liu et al., 1991; Naito, 1991; Bombace et al., 1994). Another approach has been to study their use for assisting the mitigation of environmental damage, as examined in temperate (e.g., Carter et al., 1985; Seaman and Sprague, 1991) and tropical waters (Campos and Gamboa, 1989). At present, the question of whether ARs merely redistribute fishes from surrounding natural habitats, or in fact increase produc185

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tion of fish is still under debate (Bohnsack et al., 1994; Carr and Hixon, 1997). Size, surface area, complexity and location have all been demonstrated to be important factors in influencing the success of an AR in attracting targeted species, and thus enhancing the fish community (Bohnsack et al., 1991; Kim et al., 1994). The importance of structural relief for fish recruitment to ARs, however, has not been addressed thoroughly in the literature. Nevertheless, it has been shown that the abundance of temperate (Kellison and Sedberry, 1998) and tropical (Beets, 1989) fish recruits increases in the presence of fish aggregating devices (FADs) found above or near low relief ARs. In the present study, we examine the importance of relief on the initial recruitment rates of coral reef fishes near the city of Eilat, Israel (Gulf of Eilat, Red Sea). Tourism impact on coral reefs was predicted to increase dramatically throughout the entire northern Red Sea region (Hawkins and Roberts, 1994). The coral reefs of Eilat were once considered among the more diverse reefs worldwide (Loya, 1972). At present, these reefs suffer mainly from the extensive nearby urban development and from damage caused by numerous visitors to the reef (Fishelson, 1995; Meshi and Ortal, 1995; Diamant, 1996, Zakai 1998, 2000; Epstein et al., 1999). Attraction of adult coral reef fish species has proved to be the general rule in low relief ARs (up to 2–3 m above the bottom) in Eilat, whereas recruitment and juvenile survival to these ARs were relatively low (Golani and Diamant, 1999). In contrast to low-relief ARs, the pillars of oil jetties near Eilat support high density of fish, including over 140 species (Rilov and Benayahu, 1998). Community indices (abundance, richness and diversity) along the pillars were affected positively by depth, proximity to the bottom and spatial complexity supplied by barbed wires that surround them. The main feature that differentiates the steel pillars supporting the jetties from the adjacent natural reefs is their orientation and inclination: i.e., vertical structures versus a moderate slope with lowrelief bottom. Pillars surrounded by barbed wires host a much richer and more abundant fish assemblage than the natural reefs in the area, including those in Eilat’s marine nature reserve (Rilov and Benayahu, 2000). These results led us to hypothesize that artificial reefs protruding into the water column may attract more recruits than low relief structures of similar size and structure. Thus, in the present study, we compared the initial recruitment stages of coral reef fishes to vertical high-relief versus near-bottom low-relief experimental AR installations. METHODS STUDY SITE AND EXPERIMENTAL DESIGN.—We conducted our study 100 m south of the Inter University Institute (IUI) of Eilat, ca 1 km south of the fringing reef of Eilat’s marine reserve (Fig. 1). We selected our study site based on three criteria: (1) it was far from the natural fringing reef, (2) it had low coral cover to reduce a possible influence of natural reef, and (3) it was sufficiently deep to deploy the vertical experimental installations. The experimental installations were anchored at 20 m depth on a moderately sloping sandy bottom with only a few scattered small coral heads. Hard bottom covered an average (± SD) of 12 ± 7.6% (both live and dead corals) of the substrate based on line transects placed near each of the four installations (6 parallel 10-m transects placed in 1 m intervals near each installation), following the methodology described in Loya (1972). The experimental installations used were modular (Fig. 2) and aimed at supplying shelter for fish of different sizes. They were each constructed of three units comprising 50 cm long PVC pipes (diameter detailed below), aligned parallel to the bottom, and arranged 2 m apart along two 5 mm stainless-steel galvanized wires (vertical installations), or along two iron rods 10 mm in diameter

RILOV AND BENAYAHU: REHABILITATION OF REEF FISH BY HIGH-RELIEF ARTIFICIAL REEFS

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Figure 1. Study area. Experimental installations were deployed ca 100 m south of the Interuniversity Institute of Eilat (IUI). The location of the nature reserve and the oil jetties are also indicated. (horizontal installations). Each unit consisted of two sub-units placed 50 cm apart as illustrated in Figure 2. One sub-unit consisted of two pairs of pipe groups, one with a diameter of 10 cm and the other 15 cm. The second sub-unit consisted of a group of six narrower pipes, 5 cm in diameter. The total height of a vertical installation above the bottom was 11 m, including floats. The horizontal installation was suspended by floats 1.5 m above the bottom (Fig. 2A) to avoid possible clogging by sediment. There were two replicates of each design, all anchored to the bottom by concrete weights (Fig. 2). The four installations were deployed 100 m from the shore, 40 m apart and aligned from north to south, in the following order: vertical north (VN), horizontal north (HN), vertical south (VS) and horizontal south (HS). VS and HS installations were deployed in early March 1992 and VN and HN, 3 wks later. FISH CENSUSES.—Fish censuses were conducted monthly from April 1992 to July 1993, except for February and June 1993. Fish in all four installations were censused visually during a single dive, first from a distance of 2–3 m to assess the number of individuals within schools, and then closer, examining the inside of the pipes with a flashlight. The contribution of each fish species observed during the study period to the fish abundance on an installation was described by its relative abundance, RA = (the pooled number of individuals of species i from all censuses/the total number of all individuals in all censuses) ¥ 100, and by its frequency of appearance, FA = (number of censuses in which species i was recorded/total number of censuses) ¥ 100. In addition, the fish were identified either as transients or residents. Transients were usually adult fishes that appeared once and seemed to visit the artificial reefs to feed. Residents were more stationary species that sheltered inside, or demonstrated close association with the structure and also appeared in ≥3 consecutive observations at a particular installation, or seen at least twice in two consecutive observations in a particular installation. Species that appeared in the last two censuses and sheltered in a specific installation were considered residents. Fish were also identified as juveniles or adults. Settlement period is usually referred to as the first few days after the larvae arrived to the reef and settled as a post-larvae or pre-juveniles (Victor, 1991). Because we did not census fish daily, we most probably did not observe fish immediately after settlement. Thus, we referred to all juveniles observed during each count as recruits. It should also be noted that we did not measure mortality or survival of fish, but because the ARs were isolated from each other and from the natural reef, we assumed that resident, benthic fishes, that disappeared from the ARs, suffered mortality.

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Figure 2. Experimental low-relief horizontal (a) and high relief vertical (b) installations. Each unit consisted of two sub-units. One sub-unit consisted of two pairs of pipe-groups differing in diameter.

RESULTS A total of forty-four fish species were observed at the experimental installations throughout the entire study period. Thirty-four of them were identified to the species level (Table 1). Frequency of appearance and relative abundance are given for the 15 most abundant ones, including two small, unidentified gobies. Two unidentified small fishes, one blenny and one goby, were observed sporadically and in low numbers on the ARs, five different juvenile wrasses were observed on one to two observations on the vertical ARs, and one

57.1 7.14 14.3 14.3 14.3

JA A A A A A 0.2 0.2 0.2 R R T

1.32 R 0.1 T A A A

JA A

A

R

21.4

A/J JA JA J JA JA A A 0.3

A/J JA JA J J JA

South FA RA T/R 85.7 55.6 R 57.1 19.6 R 21.4 8.84 R 7.14 6.3 T 100 6 R

Vertical AR

J A A JA A A A

A

15.4

61.5 26.9 R 76.9 11.2 R 15.4 30.6 T 30.8 5.22 R 46.2 4.48 R 61.5 5.97 R 30.8 2.99 R

23.1

2.24 R

A

4.48 R

FA

42.9 71.4 7.14 14.3 7.14 35.7 14.3 7.14 7.14 7.14

Horizontal AR North RA T/R A/J FA

Total # South of fish RA T/R A/J counted 1,509 395 122 108 85 23.5 R JA 54 29.4 R A 48 1.47 T A 42 2.94 R A 29 1.47 T A 18 7.35 R A 13 2.94 T A 10 1.47 T A 8 2.94 T A 7 1.47 T A 5

Holacanthus xanthotis, Chaetodon paucifasciatus, Cheilinus digrammus, Scarus fuscopurpureus, Haliochores scapularis, Pteragogus cryptus, Pseudochromis springeri, Zebrasoma xanthurum, Antennarius coccineus, Sufflamen albicaudatus, Cirrhitichthys oxycephalus, Arthodon hispidus, Fistularia commersonii, Stethojulis albovittata, Cantherhines pardatis, Tetrosomus gibbosus, Pomacanthus imperator, Epinephelus fasciatus, Variola luti, Siganus rivulatus, Chaetodon fasciatus

North FA RA T/R Neopomacentrus miryae 100 73 R Pseudanthias squamipinnis 46 14.9 R Scomberomorus lysa 15 2.66 R Pseudanthias taeniatus 7.7 3.49 R Petroscirtes mitratus 92 1.97 R Bodianus anthioides 15 0.15 T Goby sp. 1 54 0.76 R Paracheilinus octataenia Pomacentrus trichourus 54 0.53 R Meiacanthus nigrolineatus 31 0.76 R Pseudochromis olivaceus Goby sp. 2 15 8.67 R Pterois miles 23 0.38 R Scarus ferrugineus 23 0.23 T Escenius graviari 7.7 0.08 T

Species

Table 1. The 15 most abundant fish species that were observed in the experimental installations during the study period arranged from highest to lowest total # of fish counted on all installations together during the entire period. The frequency of appearance (FA) and relative abundance (RA) are shown. A species was designated as transient (T) or resident (R), and its individuals appeared either in a juvenile (J), or adult (A) form, or in both forms (JA). Twenty-one more species, listed under the table, occurred in low numbers and frequencies at the various installations, mainly as transients.


189

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Figure 3. The number of fish species that appeared either solely as juveniles, solely as adults or both as juveniles and adults in the four experimental installations.

juvenile could not be identified even at the family level. The total number of species observed at the four installations ranged as following: 24 in VN, 18 in VS, 17 in HN and 17 in HS. More species were observed as juveniles at the vertical installations than at the horizontal ones (VN-11, VS-8, HN-2 and HS-2 species, Fig. 3). The damselfish Neopomacentrus miryae was observed in all censuses and was the most abundant fish on the vertical structures (Table 1). This fish recruited to the ARs and later developed into adults (Table 1). The second most abundant fish at the vertical structures was Pseudanthias squamipinnis, but it had only an intermediate frequency of appearance. It was observed in large numbers only 1 yr after deployment and was also occasionally seen in small numbers at the horizontal installations (Table 1). Juveniles of the congeneric P. taeniatus settled in March 1993 on both VS and VN in numbers >10 individuals, but most were no longer observed within 2 mo. Similarly, the pelagic species Scomberoides lysan appeared as schools of juveniles around the upper unit and the floats of VN (May 1993), but was no longer observed two months later. In VS juveniles of this species had two settlement episodes (March and May 1993), after each of which they were no longer present. The blenny Petroscirtes mitratus was also frequently observed at the vertical structures. It was observed in small groups at the upper sections of the installations; first only adults were seen and later juveniles as well. N. miryae and the last three fish species mentioned above were absent from the horizontal structures. Several juveniles of the damselfish Pomacentrus trichourus recruited to both vertical installations and were later observed as adults at intermediate frequency and abundance (Table 1). During April-July 1993, towards the end of the study, adult lionfish Pterois miles appeared at the lower unit of the installations as a pair (VN) or solitary (VS). The grouper Epinephelus fasciatus was seen inside one of the large pipes of VS in two successive days in May 1993. The only species


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Fig. 4. Fish abundance at the experimental installations along the study period shown for the vertical installations (VN and VS) in their upper, middle and bottom units. * = no data.

that recruited to the horizontal installations was the wrasse Bodianus anthioides, which appeared in small numbers several times throughout the study period (Table 1). The species with the highest frequency of appearance at the horizontal ARs was a small transparent unidentified goby. The average number of fish was 81.9 ± 25.6 per census (mean ± SD, n = 14) at the vertical ARs and an order of magnitude lower (7.1 ± 2 fish) at the horizontal ARs. This difference was evident in 13 of the 14 censuses in both installations throughout the entire study period, and especially during the recruitment period in April–May of both 1992 and 1993, when the difference in fish numbers between the horizontal and vertical installations increased by one, or even two orders of magnitude (Fig. 4). During the recruitment episode of April–May 1993 most recruits, primarily N. miryae, P. squamipinnis, P. taeniatus and S. lysan, were observed in the upper units of the installation, 5–6 and 8–9 m above the bottom (Fig. 4). In July 1993 the number of fish diminished, mainly in the upper units, partially because the juvenile S. lysan were no longer present. The two most abundant fishes, N. miryae and P. squamipinnis, were scored into three size classes: 1–2 cm (recent recruits), 3–5 cm (juveniles), >5 cm (sub-adults or adults). Most of the April 1992 recruits of N. miryae were no longer seen on VN by July (Fig. 5), but those that remained increased in size and had changed their tail color from gray to orange by December of the same year. We also noticed a minor recruitment episode in October 1992. After the major recruitment of more than 300 fish in May 1993 the number of N. miryae declined by three to seven fold in VN and VS, respectively, in July 1993. Most individuals that remained in the installations were >5 cm. P. squamipinnis recruited sporadically in both vertical installations from October-December 1992, and again in

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Figure 5. Abundance of Neopomacentrus miryae and Pseudanthias squamipinnis at the two vertical southern (VS) and vertical northern (VN) installations along the study period. Values are given for three fish size classes. * = no data.

April and May 1993. By July 1993 more than 50% of the individuals were >5 cm in length (Fig. 5) and had changed their color to orange. Notably 70–90% of the individuals of these species remained on the installation in July 1993. By this time the recruits of late 1992 became adults with full coloration of females and males (deep orange and purple, respectively, see Shapiro, 1981). DISCUSSION Although the number of replicates for each relief type was limited to two in the present study, the results present a much greater recruitment rate to the vertical installations compared to the horizontal ones, thus confirming our working hypothesis. High-relief ARs were more effective at attracting recruits than low relief ones for at least some of the numerically dominant coral reef fishes. Fish Aggregating Devices (FADs) located several meters above the bottom have been shown to improve the recruitment of post-larval coral reef fish to low relief benthic structures (Beets, 1989). However, those FADs attracted juvenile and adult pelagic species, whereas juvenile coral reef fish were found only on the relatively more complex but low-relief nearby benthic reef. Because the effect of relief, structure, and complexity were confounded in Beets’ study, it is impossible to determine, in this case, the effect of relief alone. In our study, both structure and complexity of the vertical high-relief and horizontal low-relief ARs were identical. Consequently, it was possible to evaluate the importance of the AR’s relief to the recruitment of


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coral reef fish. We attribute the persistence of many recruits on these midwater structures and their survival to adulthood to the available shelter at the AR. Pelagic fish, mainly S. lysan, seemed to have settled to the vertical installations (some were seen in two successive censuses at exactly the same spot), but later probably migrated to pelagic waters or were preyed upon. Similarly, Stephan and Lindquist (1989) demonstrated that pelagic species are found on FADs only as juveniles. The Miri’s damselfish N. miryae and the scalefin anthias P. squamipinnis were dominant both as recruits and later as adults on the high relief installations. Both fish are planktivores that were also very abundant around the oil jetties of Eilat (Rilov and Benayahu, 1998), and to a much lesser extent on low relief artificial reefs (Golani and Diamant, 1999). There is evidence of net southerly currents around the oil jetties and the IUI during the fish main reproductive season (April-June, Genin A., pers. comm., IUI, Eilat 88103, Israel, and see also Abelson et al., 1999, for evidence of a southward longshore current in the region). This may suggest that the fish community at the oil jetties could have served as a source for larvae for adjacent more southern artificial structures, such as the installations in our study, and probably also for the nearby denuded natural reefs, as suggested by Rilov and Benayahu (1998, 2000). Recruitment was not observed in VS during April–May 1992, probably because this AR was deployed after the breeding season of N. miryae, whose juveniles were observed in VN that was deployed 3 ws earlier (Fig. 4). Juveniles of P. taeniatus, which is an inhabitant of deep reef-waters (Fishelson 1981), settled in spring 1993, but rapidly disappeared thereafter. This may have resulted either from unsuitability of the vertical structures for its adults, or due to competitive exclusion by its congeneric P. squamipinnis that settled at the installations during the same period. In later stages of the study, we observed two adult piscivore species in the lower units of the vertical ARs, that probably fed on the planktivore recruits (mainly N. miryae and P. squamipinnis). This may indicate that such ARs can, eventually, support higher trophic levels. However, more shelter than that provided by the small experimental installations is probably needed to support stable populations of predators. The high numbers of recruits of N. miryae and P. squamipinnis on the vertical ARs and the rarity or absence of other fish species that were abundant on the oil jetties (Rilov and Benayahu, 1998) may reflect differences in availability of larvae in the water during the study period. High variability in the recruitment rates of coral reef fishes has been observed among seasons, years and locations (Planes et al., 1993). Furthermore, fish survival and recruitment are greatly influenced by the behavior of their late larval stages, which is complex and can differ among taxa (Leis and Carson-Ewart, 1998). Rarity, or even absence, of abundant species from the vertical experimental installations may also reflect differences in habitat requirements for settlers and adults among species. For example, it is possible that planktivores like P. trichourus, with a less hydrodynamic body-shape than that of N. miryae and P. squamipinnis, and therefore much lower feeding efficiency in strong currents (see, Kiflawi and Genin, 1997), usually avoid high relief structures, where exposure to strong currents is extensive. Recruitment and persistence patterns were similar in both vertical ARs (Fig. 4). Most recruitment occurred at the upper sections, between 5–9 m above the bottom. This suggests that the larvae were at least several meters above the bottom as they approached the shore and subsequently settled on shallower portions of vertical structures. Recruitment of N. miryae and P. squamipinnis to the higher portions of the ARs may also have resulted from settlement preference of these planktivore species for areas with high water move-

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ment and plankton flux (see Hobson, 1991). Shapiro (1987) suggested that P. squamipinnis optimize for rapid settlement, and thus recruitment rates in Eilat are higher for this fish on deep, small coral aggregates than on large shallow coral aggregates. It is clear that reaching the shallow-water corals on the gently sloping reefs typical for this area requires further travel in open water, and thus greater risk of predation. However, it is apparent that when given the choice these larvae recruit first in shallower waters on high relief structures and not on deeper low relief ones (Rilov and Benayahu, 1998, this study). Evidence for active behavioral choice of settling larvae also exists for Neopomacentrus spp. in the Great Barrier Reef, Australia (Milicich and Doherty, 1994). It appears that, once delivered to a site, settlers or new recruits distribute themselves along the reef based on habitat preferences (Caselle and Warner, 1996). It seems that larvae of non-planktivore species either move closer to the bottom as they approach the shore, or actively select near-bottom habitats, and therefore usually settle around low-relief structures. This may explain the recruitment of juvenile B. anthioides only to the horizontal ARs. The disappearance of ca. 70% of the recruits (mostly N. miryae) from the installations by July 1993 (Fig. 4), mainly in the upper sections of the structures (8–9 m above the bottom), is probably related to post-settlement mortality, possibly due to predation by transient pelagic fish (see Beukers and Jones, 1988; Hixon, 1998). Alternatively, mortality may be relatively even along the vertical structures but, as recruits grow in size, they move closer to the bottom. This latter possibility fits well with Beet’s (1989) hypothesis that new settlers on FADs move later to bottom structures. Tagging of individuals would be necessary to elucidate the dynamics, survival rates and movement of juveniles on vertical structures. To conclude, evidence now suggests that vertical complex ARs is superior to low-relief ARs, for achieving rapid recruitment (this study) and high biodiversity (Rilov and Benayahu, 1998, 2000) of coral reef fishes. Well-designed vertical structures can attract recruits, offer shelter for juveniles and adults and supply habitat for both shallow and deep-water coral reef fishes (Rilov and Benayahu, 2000). They are also expected to become a source of recruits for nearby deteriorated regions. All these are highly valuable for conservation practices. High relief ARs occupy less bottom surface area than low relief ARs for a similar volume of reef. This aspect may be important for practical reasons in space-limited coastal regions such as the Eilat’s coastal area. Finally, due to the high diversity of fish and invertebrates on vertical artificial reefs (Goren, 1992; Rilov and Benayahu, 1998, 2000) they can become popular diving sites, thus reducing the pressure off the natural reef and allowing for a faster recovery. Vertical, complex ARs are suggested only as an additional means for coral reef fish community rehabilitation. They will be successful in facilitating recovery only if protection from human effects (i.e., marine protected areas) is provided at the same site. ACKNOWLEDGMENTS We would like to thank the Israeli Diving Federation for a grant funding part of this research. We acknowledge the Interuniversity Institute of Eilat for assistance and use of facilities, and M. Goren for useful suggestions. Special thanks to G. Nissel, I. Nehoran, N. Shiloah, R. Ben-David-Zaslow, and many others for helpful diving assistance. We would like to thank the anonymous reviewers who greatly improved this paper.


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DATE ACCEPTED: August 10, 2001.

ADDRESSES: CORRESPONDING AUTHOR: (G.R.) Duke University Marine Laboratory, Nicholas School of the Environment and Earth Sciences, Duke University, 135, Duke Marine Lab, Beaufort 28516, North Carolina. E-mail: . (Y.B.) Department of Zoology, George S. Wise Faculty of Life Sciences, Tel-Aviv University, Ramat-Aviv, Tel-Aviv 69978, Israel. E-mail: .