Community structure of coral reef fishes in El Quadim Bay (El Quseir, Egyptian Red Sea coast)

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1 Community structure of coral reef fishes in El Quadim Bay (El Quseir, Egyptian Red Sea coast) by Marc Kochzius Abstract. This study investigates the fish community structure of fishes on the coral reef in El Quadim Bay in order to obtain baseline data for a regular monitoring programme. A total of 16,683 fishes, representing 111 shallow-water species belonging to 47 genera and 31 families, were counted at 12 transects. Multivariate analysis indicates significant differences between the fish communities of the left side and right side of bay, as well as depth. This might be due to different exposure to wave action. The fish community in El Quadim Bay is very similar to undisturbed reefs and marine reserves in the Red Sea. Zusammenfassung. Diese Studie untersucht die Gemeinschaftsstruktur von Fischen des Korallenriffs in der El Quadim-Bucht im ägyptischen Roten Meer, um Basisdaten für eine regelmäßige Umweltüberwachung zur Verfügung zu stellen. Insgesamt wurden in 12 Transekten Fische erfaßt, die zu 111 Flachwasserarten aus 47 Gattungen und 31 Familien gehören. Eine multivariate Analyse deutet darauf hin, dass es signifikante Unterschiede zwischen den Fischgemeinschaften auf der linken und rechten Seite der Bucht, sowie in unterschiedlichen Tiefen gibt. Dieses könnte durch die unterschiedliche Exposition zur Brandung bedingt sein. Die Fischgemeinschaft in der El Quadim-Bucht ist denen von ungestörten Korallenriffen und marinen Schutzgebieten im Roten Meer sehr ähnlich. Key words. Multivariate statistics, species composition, ichthyofauna, reef fauna, biodiversity. Introduction Coral reefs are under high human impact in the northern Red Sea, caused by shipping, port activities and pollution as well as tourism (KHALAF & KOCHZIUS 2002a, KOCHZIUS 2002). At the beginning of the 1990s about 19% of Egypt s, 100% of Israel s and 50% of Jordan s coast containing coral reefs were affected by tourism (HAWKINS & ROBERTS, 1994) approximately 5.7 million tourists visited the Red Sea Riviera (NOAA 1997). Due to the growing tourism it is likely that the percentage of coral reef affected by tourisms increased. SCUBA diving has been identified as a major factor which may influence the underwater fauna of coral reefs. We investigate here the fish community structure of fishes on the coral reef in El Quadim Bay at the Egyptian Red Sea coast close to El Quseir in order to obtain baseline data for a regular monitoring programme. This future monitoring programme aims to evaluate whether the current management practice of the recreational SCUBA diving is sufficient to prevent a negative impact on El Quadim Bay. The main objectives of the study are to describe the community structure of fishes, and to compare this structure with other fish communities of the Red Sea. Zoology in the Middle East Vol.42, 2007 ISSN Kasparek Verlag, Heidelberg

2 90 Zoology in the Middle East Vol.42, 2007 Material and methods Study area. At El Quadim Bay, fringing reefs are distributed along the coast, interrupted by bays that are usually located at the mouth of wadis (dry river valleys). The bay is utilised for SCUBA diving by a single dive centre and for swimming by a hotel that is build beside the bay. Therefore, it is possible to manage the number of recreational SCUBA divers by the dive centre. Following the concept of a carrying capacity of a maximum of 6,000 dives per site and year (DIXON et al. 1993, HAWKINS & ROBERTS 1997), the number of dives per year is limited to about 20,000 dives at 5 dive sites. There is a gradient in diving pressure, with more dives in the inner than in the outer part of the bay. Due to the very steep reef slope it was not possible to lay out transects in the inner part of the bay. Therefore, conclusions about the fish community structure refer only to the outer part of the bay. Visual census. The fish community on a fringing coral reef at El Quadim Bay was surveyed in October 2005 by the visual census technique using SCUBA as described in ENGLISH et al. (1994). Transects of 50 m length and width (250 m 2 ) were marked at the study site. At each site visual censuses were conducted along three transects at the shallow slope () and deep slope (), respectively. The distance between transects at one site was about. The observer waited five minutes after laying the transect line to allow fishes to resume their normal behaviour. Subsequently, the diver swam along the transect and recorded all fishes encountered 2. on each site of the line and above the transect. All observed fishes were identified and recorded on a plastic slate. The duration for the count of each transect was 40-4inutes. The visual census technique is widely applied and accepted for fish ecological studies on coral reefs (ENGLISH et al. 1994). However, all conclusions are restricted to day active and non-cryptic species (BROCK 1982). Statistical analysis. Abundance of fishes was described by relative abundance (RA) and frequency of appearance (FA), calculated as follows: RA = (the pooled average abundance of species i from each depth and site/the pooled average abundance of all species from each depth and site) x 100 and FA = (number of transects in which species i was present/total number of all transects) x 100. Hence, RA describes the percentage of each species of the total abundance of all fishes. FA gives the information, on how many percent of transects a species is observed. Community indices such as Shannon-Wiener diversity (H ; ln basis), species richness (number of species), and fish abundance were compared among sites and depths. A one-way ANOVA was carried out with STATISTICA 5.1 (StatSoft, 1993). Multivariate analysis of the data such as MDS (multi-dimensional scaling) and ANOSIM (analysis of similarities) significance test were performed with PRIMER-5 software (Primer-E, 2000). MDS was based on Bray Curtis similarities of abundance data. Highly abundant species in contrast to species with very low abundance can disturb the analysis. Therefore, a log(1+x) transformation of data was conducted. ANOSIM significance test compares similarities of species compositions between the samples and can give evidence for differences. A two-way crossed layout of ANOSIM was performed with the transformed data (CLARKE & WARWICK 1994). Results Fish assemblages and community indices In this study a total of 16,683 fishes were counted on 12 visual census transects at and depth, representing 111 shallow-water species belonging to 47 genera and 31 families (Appendix). Most individuals observed on the visual census transects belonged to the families Pomacentridae (56.6%; 15 species), Anthiinae (32.5%; 1 species, subfamily of Serrani-

3 Coral reefs 91 dae), Acanthuridae (2.3%; 9 species), Labridae (2.3%; 27 species), Chaetodontidae (1.3%; 8 species), Scaridae (0.7%; 8 species), and Serranidae (0.6%; 14 species (Fig. 2). In terms of species richness per family the ichthyofauna showed the following ranking: Labridae (17.5%), Pomacentridae (9.7%), Serranidae (9.1%), Acanthuridae (5.8%), Chaetodontidae (5.2%), and Scaridae (5.2%) (Table 1). The most abundant species were Chromis dimidiata (44.9%), Pseudanthias squamipinnis (32.5%), Chromis ternatensis (5.8%), Chromis viridis (3.6%), and Amblyglyphidodon flavilatus (0.8%), representing 87.6% of all individuals (Table 2). In terms of frequency of appearance the most common species were Chromis dimidiata, Pseudanthias squamipinnis, Chromis ternatensis, Ctenochaetus striatus, Chaetodon austriacus, Siganus luridus, and Zebrasoma xanthurum (all 100%). Shannon-Wiener diversity (ln basis) ranged from 1.3 to 1.8, species richness from 33 to 49 species, and total abundance from 701 to ANOVA did not show significant differences between different depth and sites. Multivariate analysis of the fish community MDS analysis based on Bray-Curtis similarity of log(1+x) transformed data showed two main groups (Fig. 3): left (transects 1-6) and right (transects 7-12) side of El Quadim bay with subgroups at and depth on the right side of the bay. An ANOSIM significance test with a two-way crossed layout confirmed the difference between the left and right side of El Quadim Bay (p=0.01) as well as and depth (p=0.05). Discussion Dominant taxa and fish community parameters Chromis dimidiata and Pseudanthias squamipinnis are the most abundant species in El Quadim Bay. In reserves at the Marine Science Station (Jordan; KHALAF & KOCHZIUS 2002b) and Sanganeb atoll (Sudan; KRUPP et al. 1993) (Table 2), as well as at the Japanese gardens, off Eilat (Israel; RILOV & BENAYAHU 2000), and at Nuweiba (Egypt; BEN-TUVIA et al. 1983) P. squamipinnis is the most abundant species. At Sanganeb atoll C. dimidiata is the second most abundant species (Table 2) and is also found in high numbers at the Marine Science Station, Japanese gardens, and Nuweiba. Comparison of the relative abundance of the most common species at El Quadim Bay with the reserves at the Marine Science Station in Jordan and at Sanganeb atoll in Sudan shows a high similarity. The only exception is the very high abundance of C. dimidiata at El Quadim Bay. On Red Sea coral reefs Labridae contribute the highest percentage of species, followed by Pomacentridae (KHALAF & KOCHZIUS 2002b). This pattern could also be observed at El Quadim Bay. Compared to other coral reefs, El Quadim Bay shows a very high number of serranids. The number of acanthurids, chaetodontids and scarids at El Quadim Bay is within the same range of other fish assemblages in the Red Sea (Table 1). In terms of relative abundance of families, the ichthyofauna at El Quadim Bay is dominated by Pomacentridae, followed by Anthiinae (subfamily of Serranidae), Acanthuridae and Labridae. Almost the same pattern is found along the Jordanian coast in the Gulf of Aqaba, with the only difference that Labridae are more abundant than Acanthuridae (KHALAF & KOCHZIUS 2002b). The dominance of Pomacentridae was also revealed by visual censuses of fish assemblages on coral reefs in New Caledonia (ROSSIER & KULBICKI 2000) and on the Great Barrier Reef (ACKERMAN & BELLWOOD 2000).

4 92 Zoology in the Middle East Vol.42, 2007 Shannon-Wiener diversity (H ) did not differ between sites and depths. Regarding depth, the influence on diversity (H ) is not clear: KHALF & KOCHZIUS (2002b) as well as ÖHMAN & RAJASURIYA (1998) did not find a significant correlation between diversity (H ) and depth in Jordan and Sri Lanka, respectively. However, FRIEDLANDER & PARRISH (1998) pointed out a weak positive correlation in Hawaii, resulting in a higher diversity at larger depth. It seems that changes in diversity with depth are caused by environmental factor that differ between reefs. Therefore, a general trend of increasing diversity with depth is not evident. Species richness was rather similar in the two depths. This is in contrast to the general trend of species richness increasing with depth, shown for the Red Sea (EDWARDS & ROSEWELL 1981, ROBERTS & ORMOND 1987), in Hawaii (FRIEDLANDER & PARRISH 1998), and Sri Lanka (ÖHMAN & RAJASURIYA 1998). However, this trend is most pronounced between 1 m and 6 m depth, with a smaller or no difference between 6 m and 12 m depth (ROBERTS & ORMOND 1987). Since this study did not record fishes in the shallow water on the reef flat, this trend could not be detected. The mean value shows a higher abundance of fishes at depth than at depth, but an ANOVA analysis did not reveal a significant difference. KHALAF & KOCHZIUS (2002b) found a higher abundance of fishes in depth than in depth in the Gulf of Aqaba. A study on herbivorous fishes, such as Acanthuridae (Surgeonfishes), Scaridae (Parrotfishes), and Siganidae (Rabbitfishes) in the Gulf of Aqaba also suggests a higher abundance in than in depth (BOUCHON-NAVARO & HARMELIN-VIVIEN 1981). However, this might be due to regional differences, such as reef morphology and coral cover. In Hawaii, FRIED- LANDER & PARRISH (1998) did not reveal a connection of total fish abundance to depth. Multivariate analysis of the fish community Multi-dimensional scaling (MDS) as well as ANOSIM analysis indicate significant differences between the fish communities of the left and right side of bay as well as depths (Fig. 3). Such habitat and depth specific differences in fish communities of coral reefs are supported by other studies in Jordan (KHALAF & KOCHZIUS 2002b), Sri Lanka (ÖHMAN & RA- JASURIYA 1998), and Hawaii (FRIEDLANDER & PARRISH 1998). These differences can be due to changes in the benthic coral cover, current pattern and wave action. The differences between the left and right side of El Quadim Bay might be due to different exposure to wave action. At the left side, transects 3-6 are protected from the northerly winds and waves, whereas all transects on the right side are completely exposed. Conclusions The analysis of the dominant taxa and fish community parameters revealed the following pattern: (1) Labridae and Pomacentridae were the dominant families in terms of species richness of the ichthyofauna at El Quadim Bay as well as on other Red Sea coral reefs, (2) in terms of relative abundance Pomacentridae were the dominant family, (3) fish diversity, species richness, and abundance at El Quadim Bay were not correlated to depth in the observed range of and. Comparison of the dominant taxa and fish community parameters did not show major differences to other coral reef fish assemblages in the Red Sea. The percentage of species of the most abundant families was very similar to other reefs in the Red Sea and the percentage of serranid species was remarkable high in El Quadim Bay (Table 1). Since Serranidae are valuable food fishes, the high number of serranid species present might be due to the exclu-

5 Coral reefs 93 sion of fishing in El Quadim Bay. The relative abundance of the most abundant species at El Quadim Bay was also quite similar to marine reserves in Jordan (KHALAF & KOCHZIUS 2002b) and Sudan (KRUPP et al. 1993) (Table 2). As shown above, the fish communities of El Quadim Bay are very similar to undisturbed reefs and marine reserves in the Red Sea. A positive side effect for the fish fauna of the exclusive utilisation of El Quadim Bay for recreational SCUBA diving is the exclusion of fishermen. Acknowledgements. This study was supported by SUBEX Red Sea Diving Centers and Mövenpick Resort El Quseir. I would like to thank the staff of the SUBEX Red Sea Diving Center in El Quseir, especially Hans- Jürgen SCHERP, for assistance in diving. I am also grateful to Georg HEISS and anonymous reviewers for valuable comments on the manuscript. References ACKERMAN, J. L.& D. R. BELLWOOD (2000): Reef fish assemblages: a re-evaluation using enclosed rotenone stations. Marine Ecology, Progress Series 206: BEN-TUVIA, A., A. DIAMANT, A. BARANES & D. GOLANI (1983): Analysis of a coral reef fish community in shallow-waters of Nuweiba, Gulf of Aqaba, Red Sea. Bulletin of the Institute of Oceanography and Fisheries 9: BOUCHON-NAVARO, Y. & M. L. HARMELIN-VIVIEN (1981): Quantitative distribution of herbivorous reef fishes in the Gulf of Aqaba. Red Sea. Marine Biology 63: BROCK, R. E. (1982): A critique of the visual census method for assessing coral reef fish populations. Bulletin of Marine Science 32: CLARKE, K. R. & R. M. WARWICK (1994): Changes in marine communities: An approach to statistical analysis and interpretation. Natural Environment Research Council. DIXON, J. A., L. F. SCURA & T. VAN T HOF (1993): Meeting ecological and economic goals. Marine parks in the Caribbean. Ambio 22: EDWARDS, A. & J. ROSEWELL (1981): Vertical zonation of coral reef fishes in the Sudanese Red Sea. Hydrobiologia 79: ENGLISH, C., C. WILKINSON & V. BAKER (1994): Survey manual for tropical marine resources. Australian Institute of Marine Science, Townsville. FISHBASE (2005) FishBase: a global information system on fishes. FRIEDLANDER, A. M. & J. D. PARRISH (1998): Habitat characteristics affecting fish assemblages on a Hawaiian coral reef. Journal of Experimental Marine Biology and Ecology 224: HAWKINS, J. P. & C. M. ROBERTS (1994): The growth of coastal tourism in the Red Sea: present and future effects on coral reefs. Ambio 23: HAWKINS, J. P. & C. M. ROBERTS (1997): Estimating the carrying capacity of coral reefs for SCUBA diving. Proceeding of the 8 th International Coral Reef Symposium 2: KHALAF, M. A. & M. KOCHZIUS (2002a): Changes in trophic community structure of shore fishes at an industrial site in the Gulf of Aqaba, Red Sea. Marine Ecology Progress Series 239: KHALAF, M. A. & M. KOCHZIUS (2002b): Community structure and biogeography of shore fishes in the Gulf of Aqaba, Red Sea. Helgoland Marine Research 55: KOCHZIUS, M. (2002): Coral reefs in the Gulf of Aqaba. p. 62. In: C. WILKINSON (Ed.), Status of coral reefs of the world: Australian Institute of Marine Science, Townsville. KRUPP, F., T. PAULUS & D. NASR (1993): Coral reef fish survey.p In: F. KRUPP, M. TÜRKAY, A. G. D. EL HAG & D. NASR (Eds.), Comparative ecological analysis of biota and habitats in littoral and shallow sublittoral waters of the Sudanese Red Sea. Project report. Forschungsinstitut Senckenberg, Frankfurt and Faculty of Marine Science and Fisheries, Port Sudan.

6 94 Zoology in the Middle East Vol.42, 2007 NOAA (1997): Report of the Middle East Seas Regional Strategy Workshop for the International Coral Reef Initiative. Aqaba, Jordan, September National Oceanic and Atmospheric Administration, Silver Springs (USA). ÖHMAN, M. C. & A. RAJASURIYA (1998): Relationships between structure and fish communities on coral and sandstone reefs. Environmental Biology of Fishes 53: PRIMER-E (2000): PRIMER 5. Plymouth Routines in Multivariate Ecological Research. PRIMER-E Ltd, Plymouth Marine Laboratory. RILOV, G. & Y. BENAYAHU (2000): Fish assemblages on natural versus vertical artificial reefs: the rehabilitation perspective. Marine Biology 136: ROBERTS, C. M. & R. F. G. ORMOND (1987): Habitat complexity and coral reef fish diversity and abundance on Red Sea fringing reefs. Marine Ecology Progress Series 41: 1 8. ROSSIER, O. & M. KULBICKI (2000): A comparison of fish assemblages from two types of algal beds and coral reefs in the south-west lagoon of New Caledonia. Cybium 24: SCHRAUT, G. (1995): Dokumentation, Zonierung und ökologische Untersuchungen der Ichthyofauna eines Riffabschnittes im nördlichen Roten Meer bei Sharm El Sheikh. südlicher Sinai, Ägypten. Diploma Thesis, University of Marburg. STATSOFT (1993): STATISTICA for Windows StatSoft, Inc. Author s address: Marc Kochzius, Reef Check e.v., Bremen, Germany Centre for Environmental Research and Technology (UFT), University of Bremen, Leobenerstrasse UFT, Bremen. kochzius@uni-bremen.de. Table 1. Percentage of species of the most abundant fish families at El Quadim Bay, El Quseir, Egyptian Red Sea coast in comparison to other fish assemblages on Red Sea coral reefs. 1 this study (VC), 2 KHALAF & KOCHZIUS 2002b (VC), 3 RILOV & BENAYAHU 2000 (VC), 4 ZAJONZ et al. unpubl. report (VC), 5 SCHRAUT 1995 (VC), 6 KRUPP et al (VC+F). VC: visual census, F: fishing Labridae Pomacentridathuridadontidae Serranidae Acan- Chaeto- Scaridae El Quadim Bay(Egypt) Aqaba (Jordan) Eilat (Israel) Dahab (Egypt) Sharm El Sheikh (Egypt) Sanganeb atoll (Sudan) Table 2. Relative abundance (%) of the most abundant fish species at El Quadim Bay, El Quseir (Egyptian Red Sea) coast in comparison to other fish assemblages of marine reserves in the Red Sea. 1 this study (VC), 2 KHALAF & KOCHZIUS (2002b) (VC), 3 KRUPP et al (VC+F). VC: visual census, F: fishing. Species El Quadim Bay (Egypt) 1 Marine Science Station (Jordan) 2 Sanganeb atoll (Sudan) 3 Chromis dimidiata Pseudanthias squamipinnis Chromis ternatensis Chromis viridis Amblyglyphidodon flavilatus

7 Coral reefs 95 Fig. 1 Map of the northern Red Sea with the study site El Quseir (for a detailed map of El Quadim Bay see Fig. 4). Fig. 2. Dominant families of the ichthyofauna on visual census transects (250 m 2 ) at El Quadim Bay, El Quseir, Egyptian Red Sea coast.

96 Zoology in the Middle East Vol.42, 2007 Fig. 3. MDS plot (a) of relationships between fish assemblages (Bray-Curtis similarity, log(1+x) transformation of data, group average, stress = 0.

8 96 Zoology in the Middle East Vol.42, 2007 Fig. 3. MDS plot (a) of relationships between fish assemblages (Bray-Curtis similarity, log(1+x) transformation of data, group average, stress = 0.05) and map (b) of El Quadim Bay, Quseir, Egyptian Red Sea coast with approximate location of the 12 transects (even transect numbers: depth; odd transect numbers: depth). Appendix Average fish abundance per transect (250 m 2 ) at El Quadim Bay, Quseir, Egyptian Red Sea coast. For details regarding location of transects see Fig. 3. Nomenclature according to FishBase (2005). Transect number Depth Dasyatididae (Stingrays) Taeniura lymma Synodontidae (Lizardfishes) Synodontidae Holocentridae (Squirrelfishes) Holocentridae Myripristis murdjan Neoniphon sammara Sargocentron caudimaculatum Fistulariidae (Cornetfishes) Fistularia commersonii Scorpaenidae (Scorpionfishes) Pterois miles Pterois radiata Serranidae (Groupers, Anthiases) Aethaloperca rogaa Cephalopholis argus Cephalopholis hemistiktos Cephalopholis miniata Cephalopholis sexmaculata Diploprion drachi Grammistes sexlineatus Total

9 Coral reefs 97 Transect number Depth Plectropomus sp Pseudanthias squamipinnis Serranidae Variola louti Cirrhithidae (Hawkfishes) Paracirrhites forsteri Pseudochromidae (Dottybacks) Pseudochromis fridmani Priacanthidae (Bigeyes) Priacanthus hamrur Apogonidae (Cardinalfishes) Apogon quinquelineatus Apogonidae Carangidae (Jacks) Carangidae Carangoides bajad Lutjanidae (Snappers) Lutjanus ehrenbergi Macolor niger Caesionodae (Fusliers) Caesio lunaris Caesio striatus Caesio suevicus Haemulidae (Sweetlips) Plectorhynchus gaterinus Lethrinidae (Emperors) Lethrinus sp Monotaxis grandoculis Khyphosidae (Sea Chubs) Kyphosus sp Mullidae (Goatfishes) Mullidae Mulloidichthys vanicolensis Parupeneus macronema Chaetodontidae (Butterflyfishes) Chaetodon auriga Chaetodon austriacus Chaetodon fasciatus Chaetodon lineolatus Chaetodon melannotus Chaetodon paucifasciatus Chaetodon semilarvatus Heniochus intermedius Pomacanthidae (Anglefishes) Centropyge multispinis Pomacanthus imperator Pygoplites diacanthus Pomacentridae (Damselfishes) Abudefduf vaigiensis Amblyglyphidodon flavilatus Amphiprion bicinctus Chromis dimidiata Chromis ternatensis Chromis viridis Neopomacentrus miryae Pomacentridae Pomacentrus sulfureus Pomacentrus trichourus Labridae (Wrasses) Anampses lineatus Anampses meleagrides Total

10 98 Zoology in the Middle East Vol.42, 2007 Transect number Depth Anampses twistii Bodianus anthioides Cheilinus diagrammus Cheilinus fasciatus Cheilinus lunulatus Cheilinus sp Cheilinus trilobatus Coris aygula Epibulus insidiator Gomphosus caeruleus klunzingeri Halichoeres sp Hologymnus annulatus Labridae Labroides dimidiatus Larabicus quadrilineatus Pseudocheilinus octotaenia Pseudodax moluccanus Thalassoma rueppellii Scaridae (Parrotfishes) Cetoscarus bicolor Chlorurus sordidus Hipposcarus harid Scaridae Scarus niger Scarus sordidus Blenniidae (Blennies) Blenniidae Meiacanthus sp Plagiotremus sp Acanthuridae (Surgeonfishes) Acanthuridae Acanthurus nigricans Acanthurus sohal Ctenochaetus striatus Naso lituratus Naso unicornis Zebrasoma veliferum Zebrasoma xanthurum Siganidae (Rabbitfishes) Siganus luridus Scombridae (Mackerels) Rastrelliger kanagurta Balsistidae (Triggerfishes) Balistapus undulatus Balistidae Balistoides viridescens Pseudobalistes fuscus Rhinecanthus assasi Sufflamen albicaudatus Monacanthidae (Filefishes) Aluterus scriptus Amanses scopas Cantherhines pardalis Monacanthidae Ostraciidae (Boxfishes) Ostracion cyanurus Tetraodontidae (Pufferfishes) Arothron diadematus Total Total

Guidelines for Ornamental Fish Sampling, Data Collection and Analysis of the Aquarium Fish Trade

The Regional Organization for the Conservation of the Environment of the Red Sea and Gulf of Aden (PERSGA) Guidelines for Ornamental Fish Sampling, Data Collection and Analysis of the Aquarium Fish Trade