CORAL REEF FISHES ATTRACTED BY RECREATIONAL FEEDING IN THAILAND

Phuket mar. biol. Cent. Res. Bull 74: 13 22 (2017) CORAL REEF FISHES ATTRACTED BY RECREATIONAL FEEDING IN THAILAND Suebpong Sa-nguansil 1 *, Pitiwong Tantichodok 1, Udomsak Darumas 1, Vachira Lheknim 2 and Beverly Pi Lee Goh 3 1 School of Science, Walailak University, Nakhon Si Thammarat, Thailand 2 Department of Biology, Faculty of Science, Prince of Songkla University, Songkhla, Thailand 3 Natural Sciences & Science Education, National Institute of Education, Nanyang Technological University, Singapore Deceased 1 st December 2014 *Corresponding author: s.sanguansil@gmail.com ABSTRACT: Recreational fish feeding is an attractive activity for marine tourism. Although many possible adverse impacts of this activity such as trophic alteration, malnutrition, habitat degradation, etc. have been suggested, proof of most of these impacts is still lacking. In order to investigate the impacts further, the species of coral reef fishes attracted by recreational feeding (also called bread feeder fishes ), as well as their abundance and composition need to be determined. This study aims to determine the species of bread feeder fishes in Thailand, and their relative abundance in the Gulf of Thailand and the Andaman Sea. There were 20 species of bread feeder fishes from 11 families recorded in this study (Pomacentridae, Siganidae, Labridae, Scaridae, Caesionidae, Carangidae, Hemiramphidae, Lutjanidae, Echeneidae, Nemipteridae and Terapontidae). Quantitative assessment revealed that Pomacentridae was the dominant bread feeder fishes, comprising 70 96% of the aggregations. The species that dominated the bread feeder fish assemblages in both the Gulf of Thailand and the Andaman Sea was the Indo-Pacific sergeant, Abudefduf vaigiensis, which comprised 56 73% of the aggregations. In addition, the results from this study indicated that most of the bread feeder fishes were omnivores. Therefore, the omnivores that exhibited high relative abundance, including A. vaigiensis, A. bengalensis and A. sexfasciatus, were appropriately targeted for further studies on the impacts of recreational feeding on bread feeder fishes. Key words: Coral reef fishes, Recreational feeding, Bread feeder fishes, Thailand INTRODUCTION Recreational feeding of coral reef fishes is a popular activity for marine tourism throughout the world (Orams, 2002; Alevizon, 2004; Hémery and McClanahan, 2005; Milazzo et al., 2005; Ilarri et al., 2008; Vignon et al., 2010; Feitosa et al., 2012; Brookhouse et al., 2013). This activity helps to provide a recreational service to tourists and good profit to the local tourism industry (Seenprachawong, 2003; Brander et al., 2007; Asafu-Adjaye and Tapsuwan, 2008). However, this activity may also cause adverse impacts at the individual, population, community and ecosystem levels (Milazzo et al., 2002; Orams, 2002; Alevizon, 2004). Although many adverse impacts of recreational fish feeding have been suggested, there are few studies to support such impacts. Some literature have proposed that this activity has altered coral reef fish behavior, negatively affected health of fishes, and slightly affected community composition of coral reef fishes (Hémery and McClanahan, 2005; Milazzo et al., 2005; Milazzo et al., 2006; Ilarri et al., 2008; Vignon et al., 2010; Feitosa et al., 2012; Brookhouse et al., 2013). Other possible impacts reported were on fish biology and ecology, e.g. trophic alteration, malnutrition, the alteration of growth and reproductive characters of the feeders. Habitat degradation has also been suggested. However these impacts were proposed based on information from terrestrial wildlife recreational feeding (Orams, 2002). The data for such impacts of marine recreational feeding remain limited. This has made marine tourism management difficult. In order to provide data to support these impacts, basic information including coral reef fish species attracted by recreational feeding, ( bread feeder

14 Phuket mar. biol. Cent. Res. Bull fishes ), is necessary. Therefore, the aims of this study were to provide a species list of bread feeder fishes in the coral reefs of Thailand, both in the Andaman Sea and in the Gulf of Thailand, and determine their quantitative composition, as well as trophic representation. Such information could be useful as baseline data to assess the impact of recreational feeding, and to help select target species for further studies on the impact of recreational feeding in Thailand. MATERIALS AND METHODS This study was carried out on the coral reefs that were utilized for tourism in the Gulf of Thailand and the Andaman Sea. The Gulf of Thailand surveys were conducted at Samae San Island (Chonburi Province) on 6 th February 2016, and Tan Island (Hat Khanom-Mu Ko Thale Tai National Park, Nakhon Si Thammarat Province and Surat Thani Province) on 21 st January 2012. The Andaman Sea surveys were conducted at Hae Island (Phuket Province) on 14 th May 2013 and on 13 th February 2016, and Cheuk Island (Haad Chao Mai National Park, Trang Province) on 26 th February 2012 (Fig. 1). As bread is generally used for this activity in Thailand, particularly in the selected study sites, we also used bread in this study. Feeding experiments were conducted by feeding bread to fishes on the recreational reef sites and in areas where regular fish feeding activity is known. For each site, 2 loaves of bread were fed around midday, slice by slice, continuously until all the bread was fed (within a half an hour). Fishes that consumed the bread were observed and identified based on Allen (2000), and later classified into feeding guilds, based on a review of existing literature. A Canon PowerShot G11 camera with waterproof housing was used to take underwater photographs of bread feeder fish assemblages while the feeding experiments were taking place. The camera was kept at a distance of about 1 meter away from the fish assemblages in order to cover the entire assemblage, for fish identification and enumeration. A total of 10 photographs were sampled randomly, using a random number table, for data collection on bread feeder fish communities at each site. For the image analysis, bread feeder fishes observed in the photographs of each site were identified (by species) and enumerated. Subsequently, the percent relative abundance of each bread feeder fish species, and their respective feeding guild was calculated (as a percentage of the total number of bread feeder fishes within a site). RESULTS This study identified 20 species of coral reef fish belonging to 11 families as bread feeder fishes in Thailand (Table 1). The families Pomacentridae and Siganidae were the most abundant, showing the highest numbers of bread feeder species (5 and 3 species, respectively). Labridae, Scaridae and Carangidae were fewer in species number (each represented by 2 species). The remaining families, including Caesionidae, Hemiramphidae, Lutjanidae, Echeneidae, Nemipteridae and Terapontidae were all represented by only one species each. These bread feeder fishes were represented in three primary feeding guilds according to the review of the literature: herbivores, carnivores and omnivores (Table 2). Although many coral reef fish families were observed to consume bread at the study sites, few families dominated the aggregations. Data on the relative abundance clearly showed that pomacentrids were the main bread feeder fishes in Thai waters. These fishes exhibited the highest abundances in the bread feeder assemblages, comprising 95 96 and 70 77 percent relative abundance in the Gulf of Thailand and in the Andaman Sea, respectively. The second and the third ranked bread feeder fish families were siganids and labrids which made up only 0 27% of bread feeder fishes. The remaining families comprised less than 2% of the aggregations (Fig. 2). The Indo-Pacific sergeant, Abudefduf vaigiensis, dominated the bread feeder fish aggregation (Fig. 3) both in the Gulf of Thailand (47 56 percent relative abundance), and in the Andaman Sea (70 73 percent relative abundance). However the minor components of bread feeder fish aggregations differed between the two areas. In the Gulf of Thailand A. sexfasciatus and A. bengalensis were the second and the third most abundant species, whereas in the Andaman Sea, Siganus canaliculatus, Thalassoma lunare and S. javus took those positions.

15 Check list of coral reef fishes attracted The composition of bread feeder aggregations also showed differences in relative abundance among feeding guilds (Fig. 4). The highest (70 97%) relative abundance represented in the bread feeder fish aggregations were omnivores in both seas. However, the second most abundant feeding guild varied between areas. They were carnivores or herbivores, indicated by 1 18% and 1 28% relative abundance, respectively. Table 1. Species list of bread feeder fishes observed in the recreational-feeding site in the Gulf of Thailand and the Andaman Sea: A. Samae San Island, Chonburi Province, B. Tan Island: Surat Thani Province, C. Hae Island, Phuket Province, D. Cheuk Island, Trang Province. Family No. Scientific Name Locations Gulf of Andaman Thailand Sea A B C D Pomacentridae 1 Abudefduf vaigiensis (Quoy and Gaimard, 1825) 2 Abudefduf sexfasciatus (Lacepède, 1802) 3 Abudefduf bengalensis (Bloch, 1787) 4 Abudefduf sordidus Forsskål, 1775 5 Chromis atripectoralis Welander and Schultz, 1951 Siganidae 6 Siganus javus (Linnaeus, 1766) 7 Siganus guttatus (Bloch, 1787) 8 Siganus canaliculatus (Park, 1797) Labridae 9 Thalassoma lunare (Linnaeus, 1758) 10 Halichoeres hortulanus (Lacepède, 1801) Scaridae 11 Scarus ghobban Forsskål, 1775 12 Scarus quoyi Valenciennes, 1840 Carangidae 13 Alepes vari (Cuvier, 1833) 14 Trachinotus baillonii (Lacepède, 1801) Caesionidae 15 Caesio cuning (Bloch, 1791) Hemiramphidae 16 Hemiramphus far (Forsskål, 1775) Lutjanidae 17 Lutjanus russelli (Bleeker, 1849) Echeneidae 18 Echeneis naucrates Linnaeus, 1758 Nemipteridae 19 Scolopsis ciliata (Lacepède, 1802) Terapontidae 20 Terapon jarbua (Forsskål, 1775)

16 Phuket mar. biol. Cent. Res. Bull Table 2. Feeding guilds of bread feeder fishes found in Thailand: H. Herbivores, C. Carnivores, O. Omnivores. Scientific Name Feeding guilds Food items Abudefduf vaigiensis O Mainly zooplankton and very small proportion of benthic algae, sessile invertebrates and detritus (Frédérich et al., 2009) Abudefduf sexfasciatus O Mainly zooplankton and very small proportion of benthic algae (Frédérich et al., 2009) Abudefduf bengalensis O Algae, small benthic invertebrates and sometimes coral spawn (Westneat and Resing, 1988) Abudefduf sordidus O Algae and small invertebrates, i.e., copepods (Russo, 1987) Chromis atripectoralis C Zooplankton (Hamner et al., 1988) Siganus javus H Benthic seaweed (Woodland, 2001; Cvitanovic and Bellwood, 2009) Siganus guttatus H Benthic algae (Woodland, 2001) Siganus canaliculatus H Benthic seaweed (Woodland, 2001; Cvitanovic and Bellwood, 2009) Thalassoma lunare C Benthic invertebrates and fish eggs (Westneat, 2001) Halichoeres hortulanus C Hard-shelled prey i.e. mollusks, crustaceans and sea urchin (Westneat, 2001) Scarus ghobban H Algae and associated material scraped from rocks or dead corals (Bellwood, 2001) Scarus quoyi H Algae and associated material scraped from rocks or dead corals (Bellwood, 2001) Alepes vari C Shrimps, copepods, decapods, other crustaceans and small fishes (Smith-Vaniz, 1999) Trachinotus baillonii C Crustaceans and worms (Smith-Vaniz, 1999) Caesio cuning C Zooplankton (Hamner et al., 1988) Hemiramphus far O Floating organic matter, crustaceans and small fishes (Collette, 1999a) Lutjanus russelli C Shrimps and fishes (Sheaves and Molony, 2000) Echeneis naucrates C Parasitic copepods attached to the host and pieces of food dropped by the host (Cressey and Lachner, 1970; Collette, 1999b) Scolopsis ciliata C Benthic invertebrates and small fishes (Russell, 2001) Terapon jarbua C Fishes (Whitfield, 1979)

17 Coral reef fishes attracted by recreational feeding in Thailand Figure 1. Study sites of the survey of bread feeder fishes in Thailand: A. Samae San Island, Chonburi Province, B. Tan Island, Surat Thani Province, C. Hae Island, Phuket Province, D. Cheuk Island, Trang Province.

18 Phuket mar. biol. Cent. Res. Bull Figure 2. The relative abundance of bread feeder fishes by families observed in the Gulf of Thailand and the Andaman Sea. Figure 3. The quantitative species composition of bread feeder fishes observed in the Gulf of Thailand and the Andaman Sea. A. Samae San Island, B. Tan Island, C. Hae Island, D. Cheuk Island.

19 Coral reef fishes attracted by recreational feeding in Thailand Figure 4. Feeding guild composition of bread feeder fishes observed in the Gulf of Thailand and the Andaman Sea: A. Samae San Island, B. Tan Island, C. Hae Island, D. Cheuk Island. Total bread feeder fishes count of site A, B, C and D were 632, 395, 398 and 509 fishes respectively (based on sampling images analysis) DISCUSSION This is the first published record of species composition of bread feeder fishes in Thailand, and provides useful baseline information for further studies on the impacts of recreational feeding (Table 1). The results of this study showed that a number of bread feeder fishes are common reef associated fishes living in coral reefs or adjacent waters (Allen, 2000; Satapoomin, 2000; Wilson et al., 2008). According to the data on relative abundance (Fig. 2), the most dominant bread feeder fishes observed were pomacentrids, the most dominant fish family in the Indo-Pacific and Thai reefs (Allen, 2001; Satapoomin, 2002; Satapoomin and Chansang, 2002). The present study found that Abudefduf vaigiensis (Pomacentridae) was the predominant bread feeder species in all assemblages studied (Fig. 3). This fish is a common species living in the reefs in the Gulf of Thailand and the Andaman Sea (Satapoomin and Chansang, 2002). Other species showing lower relative abundances included A. sexfasciatus, A. bengalensis, Siganus canaliculatus and Thasassoma lunare, suggesting that they may occur in lower abundance. The reef fish community structure also differed between sites. In addition, these species of fish were also observed to have a lower competitive ability to obtain bread compared to A. vaigiensis (personal observation). Our results from image analysis showed that omnivores were the predominant feeding guild of bread feeder fishes, comprising 70 97 percent relative abundance, followed by carnivores or herbivores (Table 2, Fig. 4). The reason why these omnivores respond to recreational feeding rather than carnivores and herbivores has not been documented. However, it is hypothesized that omnivores, who are opportunists which feed on a wide range of available prey items (Gerking, 1994), would have better trophic adaptability than carnivores or herbivores. They would therefore be more able to consume bread from recreational feeding.

20 Phuket mar. biol. Cent. Res. Bull It is noticeable that the proportion of omnivores in bread feeder fish compositions in the Gulf of Thailand (95 97 percent relative abundance) was greater than that of the Andaman Sea (70 77 percent relative abundance). This information agrees with Satapoomin (2002) who reported that coral reef fishes in Andaman Sea had higher species richness than that in the Gulf of Thailand. Therefore the higher diversity of coral reef fishes in the Andaman Sea provides a higher probability of the occurrence of bread feeder fish species there, compared to the Gulf of Thailand. It is interesting to note that during a preliminary study where some slices of bread were presented to coral reef fishes in a control site (with no prior recreational bread feeding activity) for 10 minutes, none of the fish attempted to consume the bread. This control site contained a number of fish species known to be bread feeder fishes at the experimental sites. In comparison, fishes in the study sites where recreational bread feeding activity is practiced would normally consume bread presented within 10 seconds (Sa-nguansil, 2015). This suggests that becoming a bread feeder fish involves some learning behavior as mentioned in Milazzo (2011). According to the results, omnivores were the predominant bread feeder fishes in Thai waters. The ecological role of omnivores in the coral reef community is not well demonstrated. Hence, it would be difficult to predict the effect of recreational feeding based on this information. It is recommended that the use of omnivores exhibiting high relative abundance, including Abudefduf vaigiensis, A. bengalensis and A. sexfasciatus as target species for further studies on coral reef recreational feeding will enable us to better understand the effect of this activity to their diet, growth and reproduction. ACKNOWLEDGEMENTS The authors would like to thank Thammasak Yeemin and Hansa Chansang for the perceptive comments and beneficial suggestions for improving this study. We also thank Phuket Marine Biological Center, Narainrit Chinfak and Sa-nguansil family for valuable assistance and support. This study was carried out with the financial support from The Development and Promotion of Scientific and Technology Talents Project (DPST), Walailak University Fund (fund number 24/2556), and National Research Council of Thailand (2014). REFERENCE Alevizon, W. 2004. Divers feeding fishes: A continuing issue in MPA management. MPA. News. 6(5): 4. Allen, G. 2000. Marine fishes of south-east Asia. Periplus Editions, Singapore. 292 p. Allen, G.R. 2001 Pomacentridae. In: K.E. Carpenter and V. Niem (eds.). FAO species identification guide for fishery purposes. The living marine resources of the Western Central Pacific (Vol. 5). FAO, Rome. pp. 3337 3356. Asafu-Adjaye, J. and S. Tapsuwan. 2008. A contingent valuation study of scuba diving benefits: Case study in Mu KoSimilan Marine National Park, Thailand. Tourism Manage 29(6): 1122 1130. Bellwood, D.R. 2001.Scaridae. In: K.E. Carpenter and V. Niem (eds.). FAO species identification guide for fishery purposes. The living marine resources of the Western Central Pacific (Vol. 6). FAO, Rome. pp. 3468 3492. Brander, L.M., P.V. Beukering and H.S.J. Cesar. 2007. The recreational value of coral reefs: A meta-analysis. Ecol. Econ. 63(1): 209 218. Brookhouse, N., D.J. Bucher, K. Rose, I. Kerr and S. Gudge. 2013. Impacts, risks and management of fish feeding at Neds Beach, Lord Howe Island Marine Park, Australia: a case study of how a seemingly innocuous activity can become a serious problem. J. Ecotour. 12(3): 165 181. Collette, B.B. 1999a. Hemiramphidae. In: K.E. Carpenter and V. Niem (eds.). FAO species identification guide for fishery purposes. The living marine resources of the Western Central Pacific (Vol. 4). FAO, Rome. pp. 2180 2196. Collette, B.B. 1999b. Echeneidae. In: K.E. Carpenter and V. Niem (eds.). FAO species identification guide for fishery purposes. The living marine resources of the Western Central Pacific (Vol. 4). FAO, Rome. pp. 2652 2654.

21 Coral reef fishes attracted by recreational feeding in Thailand Cressey, R.F. and E.A. Lachner. 1970. The parasitic copepod diet and life history of diskfishes (Echeneidae). Copeia 1970(2): 310 318. Cvitanovic, C. and D.R. Bellwood. 2009. Local variation in herbivore feeding activity on an inshore reef of the Great Barrier Reef. Coral Reefs 28(1): 127 133. Feitosa, C.V., L.D.C.T. Chaves, B.P. Ferreira and M.E. De Araújo. 2012. Recreational fish feeding inside Brazilian MPAs: impacts on reef fish community structure. J. Mar. Biol. Assoc. U. K. 92(7): 1525 1533. Frédérich, B., G. Fabri., G. Lepoint, P. Vandewalle and E. Parmentier. 2009. Trophic niches of thirteen damselfishes (Pomacentridae) at the Grand Récif of Toliara, Madagascar. Ichthyol. Res. 56(1): 10 17. Gerk, S.D. 1994. Feeding ecology of fish. Academic Press, San Diego. 416 p. Hamner, W.M., M.S. Jones, J.H. Carleton, I.R. Hauri and D. McB. Williams. 1988. Zooplankton, planktivorous fish, and water currents on a windward reef face: Great Barrier Reef, Australia. Bull. Mar. Sci. 42(3): 459 479. Hémery, G. and T.R. McClanahan. 2005. Effect of recreational fish feeding on reef fish community composition and behavior. West. Indian Ocean J. Mar. Sci. 4(2): 123 133. Ilarri, M.I., A.T. Souza, P.R. Medeiros, R.G. Grempel and I.M. Lucena Rosa. 2008. Effects of tourist visitation and supplementary feeding on fish assemblage composition on a tropical reef in the Southwestern Atlantic. Neotrop. Ichthyol. 6: 651 656. Milazzo, M. 2011. Evaluation of a behavioral response of Mediterranean coastal fishes to novel recreational feeding situation. Environ. Biol. Fish. 91(1): 127 132. Milazzo, M., R. Chemello, F. Badalamenti, R. Camarda and S. Riggio. 2002. The impact of human recreational activities in marine protected areas: What lessons should be learnt in the Mediterranean Sea?. Mar. Ecol. 23: 280 290. Milazzo, M.,F. Badalamenti, T. Vega Fernández and R. Chemello. 2005. Effects of fish feeding by snorkellers on the density and size distribution of fishes in a Mediterranean marine protected area. Mar. Biol. 146(6): 1213 1222. Milazzo, M., I. Anastasi and T.J. Willis. 2006. Recreational fish feeding affects coastal fish behavior and increases frequency of predation on damselfish Chromis chromis nests. Mar. Ecol. Prog. Ser. 310: 165 172. Orams, M.B. 2002. Feeding wildlife as a tourism attraction: a review of issues and impacts. Tourism Manage 23(3): 281 293. Russell, B.C. 2001. Nemipteridae. In: K.E. Carpenter and V. Niem (eds.). FAO species identification guide for fishery purposes. The living marine resources of the Western Central Pacific (Vol. 5). FAO, Rome. pp. 3051 3089. Russo, A.R. 1987. Role of habitat complexity in mediating predation by the gray damselfish Abudefduf sordidus on epiphytal amphipods. Mar. Ecol. Prog. Ser. 36(2): 101 105. Sa-nguansil, S. 2015. The effects of recreational feeding on diet, growth and reproduction of a coral reef-fish, Abudefduf bengalensis (Bloch, 1787), in the Gulf of Thailand. Ph.D., Walailak University, Nakhon Si Thammarat. 93 p. Satapoomin, U. 2000. A preliminary checklist of coral reef fishes of the Gulf of Thailand, South China Sea. Raffles Bull. Zool. 18(1): 31 53. Satapoomin, U. 2002. Comparative study of reef fish fauna in Thai waters: the Gulf of Thailand versus the Andaman Sea: Phuket Marine Biological Center. Technical Paper. 1/2002. Satapoomin, U. and H. Chansang. 2002. Structure of reef fish communities of Phuket Island, the Andaman Sea. Phuket mar. biol. Cent. Res. Bull. 64: 25 52. Seenprachawong, U. 2003. Economic valuation of coral reefs at Phi Phi Islands, Thailand. Int. J. Global Environ. 3(1): 104 114. Sheaves, M. and B. Molony. 2000. Short-circuit in the mangrove food chain. Mar. Ecol. Prog. Ser. 199: 97 109.

22 Phuket mar. biol. Cent. Res. Bull Smith-Vaniz, W.F. 1999. Carangidae. In: K.E. Carpenter and V. Niem (eds.). FAO species identification guide for fishery purposes. The living marine resources of the Western Central Pacific (Vol. 4). FAO, Rome. pp. 2659 2756. Vignon, M., P.Sasal, R.L. Johnson and R.Galzin. 2010. Impact of shark-feeding tourism on surrounding fish populations off Moorea Island (French Polynesia). Mar. Freshwater Res. 61(2): 163 169. Westneat, M. 2001. Labridae. In: K.E. Carpenter and V. Niem (eds.). FAO species identification guide for fishery purposes. The living marine resources of the Western Central Pacific (Vol. 6). FAO, Rome. pp. 3381 3467. Westneat, M. and J. Resing. 1988. Predation on coral spawn by planktivorous fish. Coral Reefs. 7(2): 89 92. Whitfield, A.K. 1979. Field observations on the lepidophagous teleost Teraponjarbua (Forskål). Environ. Biol. Fish. 4(2): 171 172. Wilson, S.K., S.C. Burgess, A.J. Cheal, M. Emslie, R. Fisher, I. Miller, N.V.C. Polunin and H.P.A. Sweatman. 2008. Habitat utilization by coral reef fish: implications for specialists vs. generalists in a changing environment. J. Anim. Ecol. 77(2): 220 228. Woodland, D.J. 2001. Siganidae. In: K.E. Carpenter and V. Niem (eds.). FAO species identification guide for fishery purposes. The living marine resources of the Western Central Pacific (Vol. 6). FAO, Rome. pp. 3627 3650. Manuscript received: 21 April 2016 Accepted: 17 November 2016