Abundance and diversity of anemonefishes and their host sea ...

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May 29, 2012 - sea anemones at two mesophotic sites on the Great. Barrier Reef ... A total of 37 host sea anemones (31 Entacmaea quadricolor and 6.

Coral Reefs (2012) 31:1057–1062 DOI 10.1007/s00338-012-0916-x


Abundance and diversity of anemonefishes and their host sea anemones at two mesophotic sites on the Great Barrier Reef, Australia T. Bridge • A. Scott • D. Steinberg

Received: 22 November 2011 / Accepted: 14 May 2012 / Published online: 29 May 2012 Ó Springer-Verlag 2012

Abstract Anemonefishes and their host sea anemones are iconic inhabitants of coral reef ecosystems. While studies have documented their abundance in shallow-water reef habitats in parts of the Indo-Pacific, none have examined these species on mesophotic reefs. In this study, we used autonomous underwater vehicle imagery to examine the abundance and diversity of anemones and anemonefishes at Viper Reef and Hydrographers Passage in the central Great Barrier Reef at depths between 50 and 65 m. A total of 37 host sea anemones (31 Entacmaea quadricolor and 6 Heteractis crispa) and 24 anemonefishes (23 Amphiprion akindynos and 1 A. perideraion) were observed. Densities were highest at Viper Reef, with 8.48 E. quadricolor and A. akindynos per 100 m2 of reef substratum. These results support the hypothesis that mesophotic reefs have many

T. Bridge and A. Scott contributed equally to this work. Communicated by Biology Editor Dr. Hugh Sweatman T. Bridge School of Earth and Environmental Sciences, James Cook University, Townsville, QLD 4811, Australia Present Address: T. Bridge (&) ARC Centre of Excellence for Coral Reef Studies, James Cook University, Townsville, QLD 4811, Australia e-mail: [email protected] A. Scott National Marine Science Centre, School of Environment, Science and Engineering, Southern Cross University, PO Box 4321, Coffs Harbour, NSW 2450, Australia D. Steinberg Australian Centre for Field Robotics, University of Sydney, Sydney, NSW 2006, Australia

species common to shallow-water coral reefs and that many taxa may occur at depths greater than currently recognised. Keywords Amphiprion  Entacmaea quadricolor  Heteractis crispa  Depth range  Mesophotic  Autonomous underwater vehicle

Introduction Ten species of sea anemone provide essential habitat for 26 species of ectosymbiotic anemonefish (Fautin and Allen 1997; Ollerton et al. 2007). These associations are often found on or near coral reefs throughout the Indo-Pacific (Dunn 1981; Fautin and Allen 1997). All host anemones also have endosymbiotic zooxanthellae, which translocate photosynthetically fixed carbon to the host. This contributes to their nutrition and restricts them to depths that receive sufficient sunlight (Dunn 1981; Fautin and Allen 1997; Muller-Parker and Davy 2001). Baseline studies on the distribution and abundance of host sea anemones and their resident fish are important, given that pressures such as aquarium collecting, bleaching events, storm swells and land reclamation have been found to reduce their abundance (Hattori 2002; Shuman et al. 2005; Hill and Scott 2012). Although anemones and anemonefishes have been studied at a variety of locations, for example, the Philippines (Shuman et al. 2005), Red Sea (Brolund et al. 2004; Chadwick and Arvedlund 2005), Japan (Hirose 1985; Hattori 2002, 2006) and Australia (Richardson et al. 1997; Jones et al. 2008; Scott et al. 2011), only populations in relatively shallow water (\40 m) have been investigated. Technological advances in recent years have resulted in greater awareness of the importance of deeper reef habitats



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Fig. 1 Great Barrier Reef bathymetry (data from Beaman 2010) showing location of study sites at Viper Reef and Hydrographers Passage

to coral reef function and biodiversity (Hinderstein et al. 2010). These habitats, referred to as mesophotic coral ecosystems (MCEs), occur in the middle to lower photic zone, but still contain many zooxanthellate taxa common to shallow-water reef habitats (Kahng et al. 2010; Bare et al. 2010; Bridge et al. 2012). Most studies characterising MCEs have focussed on either fish (Thresher and Colin 1986; Parrish and Bolland 2004; Brokovich et al. 2008) or the dominant habitat-forming benthos (Armstrong et al. 2006; Kahng and Kelley 2007; Bridge et al. 2011a, b; Bongaerts et al. 2011). To date, the abundance and diversity of sea anemones and anemonefishes in the mesophotic zone has not been investigated. Accordingly, this study utilised autonomous underwater vehicle (AUV) imagery to document the abundance of anemonefishes and their host anemones in the mesophotic zone (50–65 m depth) at two sites (*200 km apart) along the shelf-edge of the central Great Barrier Reef (GBR), Australia.

Materials and methods Georeferenced stereo images were collected by the AUV ‘Sirius’ in September–October 2007 (Williams et al. 2010). Images were collected at a rate of 2 Hz, and each image


covered an area of approximately 1.5 9 1.2 m. Anemones and anemonefishes were observed in four AUV missions: two at Viper Reef (18.83°S, 148.45°E) and two at Hydrographers Passage (19.70°S, 150.25°E) in the central GBR (Fig. 1). Although some AUV images were collected as deep as 150 m, phototrophic taxa are uncommon at depths [65 m at both Viper Reef and Hydrographers Passage (Bridge et al. 2011a, b), and therefore, only images \65 m depth were included in this study. All anemones and anemonefishes observed in AUV images were identified following Dunn (1981) and Fautin and Allen (1997). Their location and density (per 100 m2) were calculated using georeferenced tracks of the AUV missions in ArcMap 9.3. Two estimates of density are presented: one for the combined area of all AUV images and the second for ‘reef’ substrata only. This was done because the vast majority of images, particularly at Viper Reef, cover non-reef substratum that supports very few visible sessile benthic organisms (Bridge et al. 2011b). The total area surveyed at Viper Reef was 5,390 m2, with 165 m2 being ‘reef’ substratum. The surveys at Hydrographers Passage covered 1,910 m2 and included 956 m2 of ‘reef’ substratum. Reef substratum was identified using automatic clustering performed using a data-driven approach based on a

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Fig. 2 Autonomous underwater vehicle images showing a clustering Entacmaea quadricolor hosting two Amphiprion akindynos at 53 m depth, Hydrographers Passage; and b Heteractis crispa hosting four A. akindynos at 58 m, Viper Reef

Bayesian non-parametric variational Dirichlet process (Steinberg et al. 2011). This method uses descriptors for colour, texture and three-dimensional structure obtained from stereo images and has the advantage of not requiring knowledge of the number of clusters a priori, and therefore enables truly autonomous data extraction. Automatic classification of images allowed rapid identification of reef substratum ([50 % limestone reef) from a large pool of images (n = 59864)

Results and discussion Visual inspection of AUV images found two species of host sea anemones: Entacmaea quadricolor (both solitary and clustering forms) and Heteractis crispa, as well as two species of anemonefishes: Amphiprion akindynos and A. perideraion (Fig. 2; Table 1). Heteractis crispa and

Table 1 Density of sea anemones and anemonefish at Viper Reef and Hydrographers Passage E. quadricolor

H. crispa

A. akindynos

A. perideraion





All substrata





Reef only








All substrata




Reef only




Viper Reef No. individuals Density (100 m-2)

Hydrographers Passage No. individuals Density (100 m-2)



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Fig. 3 Bathymetry of submerged reefs at a Viper Reef; and b Hydrographers Passage. Stars and circles indicate the locations where Entacmaea quadricolor and Heteractis crispa, respectively, were observed in AUV images

A. akindynos were found at a maximum depth of 60 m, while E. quadricolor was found at a maximum depth of 58 m. A. akindynos was observed utilising both species of anemone. One A. perideraion was recorded during the surveys at 52 m residing in H. crispa. These findings represent the deepest known records for these species. A total of 37 anemones and 24 anemonefishes were observed across the two sites (Table 1). All anemones were


found on ‘reef’ substratum, except for one H. crispa that was observed on rubble substratum at Viper Reef. Hydrographers Passage contained more ‘reef’ substratum than Viper Reef; however, the density of anemones on ‘reef’ substratum was substantially greater at Viper Reef (Table 1). Likewise, the density of anemonefishes was also higher at this site. Due to the obligate nature of the symbiosis between the two partners, densities of anemonefishes are often higher in areas that

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have more sea anemones (Chadwick and Arvedlund 2005; Scott et al. 2011). It should be noted that the number of anemonefishes may have been underestimated in the current study, as fishes could have potentially been out of the image frame at the time of capture. The Viper Reef region consists primarily of an extensive Halimeda field punctuated by a series reef pinnacles, generally 20–80 m in diameter and up to 5 m high (Fig. 3a). Anemones generally occurred on the tops of these reef pinnacles, which also support high cover of scleractinian corals (Bridge et al. 2011b). In contrast, the Hydrographers Passage site consisted primarily of parallel lines of submerged reefs with the tops in *50 m water depth (Bridge et al. 2011a). The sizes of the reefs at this site are variable, with some being over 1 km in length and *150 m wide (Fig. 3b). Anemones and anemonefishes were less common at this site than at Viper Reef, even though the tops of these shoals are composed primarily of hard substratum and support a diverse assemblage of sessile benthic megafauna (Bridge et al. 2011a, b). Entacmaea quadricolor densities were higher than those of H. crispa. Solitary and clustering forms of E. quadricolor were found at both sites. The solitary anemones are most likely to have originated from sexually produced propagules, whereas the clusters probably resulted from asexual reproduction via longitudinal fission (Dunn 1981; Scott and Harrison 2007, 2009). All of the anemones, or clusters, except for one E. quadricolor were occupied by anemonefishes. Most anemones in shallow-water tropical reefs are also typically occupied (Dunn 1981). At Viper Reef, 80.0 % of the anemonefishes were observed in pairs or social groups, whereas at Hydrographers Passage, 55.6 % were observed in pairs or social groups. The findings of this study: (1) indicate that at least some species of host sea anemones and anemonefishes occur across a broad bathymetric range, extending from reef flats and slopes (Hirose 1985; Chadwick and Arvedlund 2005; Hattori 2006) well into the mesophotic zone; and, (2) reinforce the importance of studying mesophotic reefs when determining patterns of biodiversity and connectivity both within the GBR and elsewhere in the Indo-Pacific. Although only two host anemone and anemonefish species were observed in this study, Heteractis magnifica and Amphiprion bicinctus have been observed at *40 and 65 m, respectively (Brolund et al. 2004; Brokovich et al. 2008). Dedicated research effort would likely yield further information on the diversity and abundance of anemones and anemonefishes on mesophotic reefs. The densities of the most abundant species of anemone found in this study, E. quadricolor, are by no means the highest recorded (Scott et al. 2011), but are similar to some shallow-water habitats (see Richardson et al. 1997 for a review of E. quadricolor densities).


The ability of these species to exist across broad bathymetric ranges may be advantageous to anemone and anemonefish populations. Deep-reef habitats may be less susceptible to disturbance events such as warm-water bleaching and tropical storms (Glynn 1996; Riegl and Piller 2003; Bongaerts et al. 2010), and therefore, species that are able to exist over broad bathymetric ranges are less likely to be affected by predicted increases in the frequency and severity of these disturbances associated with climate change. Furthermore, host sea anemones and anemonefishes are highly sought after by aquarium collectors (Shuman et al. 2005), and the remote and inaccessible nature of MCEs makes this threat unlikely to affect their abundance in these habitats. Acknowledgments We would like to thank crew of RV Southern Surveyor, J. Webster and R. Beaman for their work in coordinating the expedition. This project was supported by the Integrated Marine Observing System (IMOS), Australia’s Marine National Facility, the National Geographic Society and the Natural Environment Research Council. We would also like to thank S. Williams and O. Pizarro for their assistance with the AUV data and two anonymous reviewers for their helpful suggestions for improving the manuscript.

References Armstrong RA, Singh H, Torres J, Nemeth RS, Can A, Roman C, Eustice R, Riggs L, Garcia-Moliner G (2006) Characterizing the deep insular shelf coral reef habitat of the Hind Bank Marine Conservation District (US Virgin Islands) using the Seabed autonomous underwater vehicle. Cont Shelf Res 26:194–205 Bare AY, Grimshaw KL, Rooney JJ, Sabater MG, Fenner D, Carroll B (2010) Mesophotic communities of the insular shelf at Tutuila, American Samoa. Coral Reefs 29:369–377 Beaman RJ (2010) Project 3DGBR: a high-resolution depth model for the Great Barrier Reef and Coral Sea. Marine and Tropical Sciences Research Facility (MTSRF) Project 2.5i.1a Final Report, MTSRF, Cairns, Australia, p12 plus Appendix 1 (accessible at http://www.deepreef.org/images/stories/publications/reports/ Project3DGBRFinal_RRRC2010.pdf) Bongaerts P, Ridgway T, Sampayo EM, Hoegh-Guldberg O (2010) Assessing the ‘deep reef refugia’ hypothesis: focus on Caribbean reefs. Coral Reefs 29:309–327 Bongaerts P, Bridge TCL, Kline DR, Muir PR, Wallace CC, Beaman RJ, Hoegh-Guldberg O (2011) Mesophotic coral ecosystems on the walls of Coral Sea atolls. Coral Reefs 30:335 Bridge TCL, Done TJ, Beaman RJ, Friedman A, Williams SB, Pizarro O, Webster JM (2011a) Topography, substratum and benthic macrofaunal relationships on the tropical mesophotic shelf margin, central Great Barrier Reef, Australia. Coral Reefs 30:143–153 Bridge TCL, Done TJ, Friedman A, Beaman RJ, Williams SB, Pizarro O, Webster JM (2011b) Variability in mesophotic coral reef communities along the Great Barrier Reef, Australia. Mar Ecol Prog Ser 428:63–75 Bridge TCL, Fabricius KE, Bongaerts P, Wallace CC, Muir PR, Done TJ, Webster JM (2012) Diversity of scleractinia and Octocorallia in the mesophotic zone of the Great Barrier Reef, Australia. Coral Reefs 31:179–189 Brokovich E, Einbinder S, Shashar N, Kiflawi M, Kark S (2008) Descending to the twilight-zone: changes in coral reef fish


1062 assemblages along a depth gradient down to 65 m. Mar Ecol Prog Ser 371:253–262 Brolund TM, Anders T, Nielsen EL, Arvedlund M (2004) An assemblage of the host anemone Heteractis magnifica in the northern Red Sea, and distribution of the resident anemonefish. J Mar Biol Assoc UK 84:671–674 Chadwick NE, Arvedlund M (2005) Abundance of giant sea anemones and patterns of association with anemonefish in the northern Red Sea. J Mar Biol Assoc UK 85:1287–1292 Dunn DF (1981) The clownfish sea anemones: Stichodactylidae (Coelenterata: Actiniaria) and other sea anemones symbiotic with pomacentrid fishes. Trans Am Philos Soc 71:1–115 Fautin DG, Allen GR (1997) Anemonefishes and their host sea anemones: a guide for aquarists and divers. Western Australian Museum, Perth Glynn PW (1996) Coral reef bleaching: facts, hypotheses and implications. Global Change Biol 2:495–509 Hattori A (2002) Small and large anemonefishes can coexist using the same patchy resources on a coral reef, before habitat destruction. J Anim Ecol 71:824–831 Hattori A (2006) Vertical and horizontal distribution patterns of the giant sea anemone Heteractis crispa with symbiotic anemonefish on a fringing coral reef. J Ethol 24:51–57 Hill R, Scott A (2012) The influence of irradiance on the severity of thermal bleaching in sea anemones that host anemonefish. Coral Reefs 31:273–284 Hinderstein LM, Marr JCA, Martinez FA, Dowgiallo MJ, Puglise KA, Pyle RL, Zawada DG, Appeldoorn R (2010) Theme section on ‘‘Mesophotic coral ecosystems: characterization, ecology and management’’. Coral Reefs 29:247–251 Hirose Y (1985) Habitat, distribution and abundance of coral reef seaanemones (Actiniidea and Stichodactylidae) in Sesoko Island, Okinawa, with notes on expansion and contraction behavior. Galaxea 4:113–127 Jones AM, Gardner S, Sinclair W (2008) Losing ‘Nemo’: bleaching and collection appear to reduce inshore populations of anemonefishes. J Fish Biol 73:753–761 Kahng SE, Kelley CD (2007) Vertical zonation of megabenthic taxa on a deep photosynthetic reef (50–140 m) in the Au0 au Channel, Hawaii. Coral Reefs 26:679–687 Kahng SE, Garcia-Sais JR, Spalding HL, Brokovich E, Wagner D, Weil E, Hinderstein L, Toonen RJ (2010) Community ecology of mesophotic coral reef ecosystems. Coral Reefs 29:255–275


Coral Reefs (2012) 31:1057–1062 Muller-Parker G, Davy SK (2001) Temperate and tropical algal sea anemone symbiosis. Invertebr Biol 120:104–123 Ollerton J, McCollin D, Fautin D, Allen G (2007) Finding NEMO: nestedness engendered by mutualistic organization in anemonefish and their hosts. Proc R Soc B 274:591–598 Parrish FA, Bolland RC (2004) Habitat and reef-fish assemblages of banks in the Northwestern Hawaiian Islands. Mar Biol 144:1065–1073 Richardson DL, Harriott VJ, Harrison PL (1997) Distribution and abundance of giant sea anemones (Actiniaria) in subtropical eastern Australian waters. Mar Freshw Res 48:59–66 Riegl B, Piller WE (2003) Possible refugia for reefs in times of environmental stress. International Journal of Earth Sciences 92:520–531 Scott A, Harrison PL (2007) Broadcast spawning of two species of sea anemone, Entacmaea quadricolor and Heteractis crispa, that host anemonefish. Invertebr Reprod Dev 50:163–171 Scott A, Harrison PL (2009) Gametogenic and reproductive cycles of the sea anemone, Entacmaea quadricolor. Mar Biol 156: 1659–1671 Scott A, Malcolm H, Damiano C, Richardson D (2011) Long-term increases in abundance of anemonefish and their host sea anemones in an Australian marine protected area. Mar Freshw Res 62:187–196 Shuman CS, Hodgson G, Ambrose RF (2005) Population impacts of collecting sea anemones and anemonefish for the marine aquarium trade in the Philippines. Coral Reefs 24:564–573 Steinberg D, Friedman A, Pizarro O, Williams SB (2011) A Bayesian nonparametric approach to clustering data from underwater robotic surveys. International Symposium on Robotics Research, Flagstaff, Arizona, USA (accessible at http://www.isrr-2011.org/ ISRR-2011/Program_files/Papers/Williams-ISRR-2011.pdf) Thresher RE, Colin PL (1986) Trophic structure, diversity and abundance of fishes of the deep reef (30–300 m) at Enewetak, Marshall Islands. Bull Mar Sci 38:253–272 Williams SB, Pizarro O, Webster JM, Beaman RJ, Mahon I, JohnsonRoberson M, Bridge TCL (2010) AUV-assisted surveying of drowned reefs on the shelf-edge of the Great Barrier Reef, Australia. J Field Robot 27:675–697

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