Vol. 23: 129–137, 2015 AQUATIC BIOLOGY Published online January 22 doi: 10.3354/ab00614 Aquat Biol OPENPEN ACCESSCCESS Chemical versus structural defense against fish predation in two dominant soft coral species (Xeniidae) in the Red Sea Ben Xuan Hoang1,2,*, Yvonne Sawall1, Abdulmohsin Al-Sofyani3, Martin Wahl1 1Helmholtz Centre for Ocean Research, GEOMAR, Wischhofstrasse 1-3, 24148 Kiel, Germany 2Institute of Oceanography, Vietnam Academy of Science and Technology, 01 Cada, Nha Trang, Vietnam 3Faculty of Marine Science, King Abdulaziz University, PO Box 80207, Jeddah 21589, Saudi Arabia ABSTRACT: Soft corals of the family Xeniidae are particularly abundant in Red Sea coral reefs. Their success may be partly due to a strong defense mechanism against fish predation. To test this, we conducted field and aquarium experiments in which we assessed the anti-feeding effect of sec- ondary metabolites of 2 common xeniid species, Ovabunda crenata and Heteroxenia ghardaqen- sis. In the field experiment, the metabolites of both investigated species reduced feeding on exper- imental food pellets in the natural population of Red Sea reef fishes by 86 and 92% for O. crenata and H. ghardaqensis, respectively. In the aquarium experiment, natural concentration of soft coral crude extract reduced feeding on experimental food pellets in the moon wrasse Thalassoma lunare (a common reef fish) by 83 and 85% for O. crenata and H. ghardaqensis, respectively. Moon wrasse feeding was even reduced at extract concentrations as low as 12.5% of the natural crude extract concentration in living soft coral tissues. To assess the potential of a structural anti- feeding defense, sclerites of O. crenata (H. ghardaqensis lacks sclerites) were extracted and mixed into food pellets at natural, doubled and reduced concentration without and in combination with crude extract at 25% of natural concentration, and tested in an aquarium experiment. The sclerites did not show any effect on the feeding behavior of the moon wrasse, indicating that scle- rites provide structural support rather than anti-feeding defense. We conclude that the conspicu- ous abundance of xeniid soft coral species in the Red Sea is likely a consequence of a strong chem- ical defense, rather than physical defenses, against potential predators. KEY WORDS: Chemical defense · Feeding deterrence · Sclerites · Soft coral · Xeniidae · Ovabunda · Heteroxenia · Red Sea INTRODUCTION protection (La Barre et al. 1986), allelopathy (Sam- marco et al. 1983, 1985) and anti-fouling activity Soft corals (Cnidaria, Alcyonacea) are a major (Changyun et al. 2008, Limna Mol et al. 2010). component of the sessile coral reef benthos and These chemical defenses may be as effective as are highly diverse in tropical Indo-Pacific coral reefs biomineralized skeletons in that they protect herma - (Dinesen 1983, Fabricius & Alderslade 2001), includ- typic corals from predation by most reef fishes (Sam- ing the Red Sea (Benayahu & Loya 1977, 1981, marco & Coll 1992). For example, some Alcyoniidae Benayahu 1985, Reinicke 1997). Some soft corals of species (e.g. Sinularia polydactyla, Rhytisma fulvum the families Xeniidae and Alcyoniidae contribute to fulvum) were shown to possess secondary metabo- the diet of coral reef fishes (Gohar 1940). Secondary lites, which protected the soft corals against predation metabolites of some soft corals have been shown to by carnivorous fish (Wylie & Paul 1989, Van Alstyne possess ecological functions including anti-predatory et al.1994, Kelman et al. 1999). A survey by Coll et al. © The authors 2015. Open Access under Creative Commons by *Corresponding author: [email protected] Attribution Licence. Use, distribution and reproduction are un - restricted. Authors and original publication must be credited. Publisher: Inter-Research · www.int-res.com 130 Aquat Biol 23: 129–137, 2015 (1982) showed a high prevalence of toxic species areas (~4 m depth), forming extensive carpets (Be- among the soft coral order Alcyonacea (>50% of the nayahu & Loya 1981, Reinicke 1997). Xeniid ‘colonies’ species) in the central Great Barrier Reef, suggesting consist of numerous conspecific individuals occurring that secondary metabolites, which are active against side by side (Gohar 1940). The family differs from all predators, are common in the Alcyonacea. In an other Octocorallia due to the soft, fleshy consistency extensive study by La Barre et al. (1986), it was found of the colony and its non-retractile polyps (Ashworth that the majority of soft coral taxa in the Great Barrier 1899). Some xeniid species lack stinging nematocysts Reef possess defense mechanisms against fish preda- (Janes 2008), which might reduce their capacity for tion, although toxicity and repellence are not always protection against predators (Vermeij 1978, Bakus related to each other. 1981, McIlwain & Jones 1997). Nevertheless, their Chemical defense against predation may already competitiveness is high, presumably due to their mot - be present in eggs, embryos or larvae of some soft ility as adults, their rapid asexual reproduction (Be- corals (Coll et al. 1989, Kelman et al. 1999, Slattery et nayahu & Loya 1981), and the widespread allelopathy al. 1999, Lindquist 2002) indicating the importance against space competitors and hard coral recruitment of chemical anti-feeding defense throughout the life (Sammarco et al. 1983, Atri genio & Alino 1996). Sec- history of soft corals. In addition to their well-studied ondary metabolites with anti microbial (Kelman et al. anti-feeding role, secondary metabolites of soft corals 1998, 2006) and anti-fouling activity (König et al. may also serve to combat fouling on the surface 1989) also seem to be common in xeniid soft corals. (Bhosale et al. 2002, Limna Mol et al. 2010) and may Indeed, xeniids, like many other soft coral taxa, are protect corals against viral infections (Ahmed et al. remarkably rich in bioactive secondary metabolites 2013). The conspicuous richness of chemical defenses (König et al. 1989, El-Gamal et al. 2005). Some chem- in soft corals (Rocha et al. 2011) may therefore con- ical compounds that have been isolated from xeniid tribute to their remarkable invasion potential (Lages species are considered to be useful candidates in the et al. 2006, Fleury et al. 2008). field of medicine, particularly against cancer cells. In soft corals, chemical defense can be supple- These include the compounds blumiolide A, B and C mented by mechanical defense such as mucus secre- of the species Xenia blumi (El-Gamal et al. 2005), dif- tion (La Barre et al. 1986, Sammarco et al. 1987, ferent umbellacins of the species X. umbellata (El- Harvell & Fenical 1989) or elevated spicule concentra- Gamal et al. 2006) and different xeniolide of the spe- tion (Van Alstyne et al. 1992). Calcium carbonate spic- cies X. blumi, X. novaebrittanniae and X. umbellata ules are common attributes in Octocorallia, as well as (Bishara et al. 2006). To the best of our knowledge, in Porifera, Echinodermata and Ascidiacea (Kingsley their potential chemical defense against fish preda- 1984). The size and shape of the spicules are often tion, which could contribute to their high abundance species-specific and can be used as taxonomic tools in the Red Sea, has not been investigated so far. (e.g. Bayer et al. 1983). In soft corals, they are assum- In this study, we investigated the chemical defense ed to mainly function as structural support for the against fish predation of 2 particularly abundant polyps and colonies (Lewis & Von Wallis 1991, Van xeniid species in the Red Sea, Ovabunda crenata Alstyne et al. 1992, O’Neal & Pawlik 2002), however, and Heteroxenia ghardaqensis. We further studied they can also function as defensive structures. This whether or not chemical defense is enhanced by the was demonstrated for some soft coral species, where presence of sclerites. To this purpose, artificial food fishes rejected sclerites containing artificial food (Van was prepared and charged with crude extract of soft Alstyne et al. 1992, 1994), but not for others (Kelman coral (1) at natural concentration and fed to the reef et al. 1999, O’Neal & Pawlik 2002). The anti-feeding fish community in situ, and (2) at natural and reduced defense by sclerites may be effective only in those concen trations, with and without the addition of scle- parts of the colony where their concentration is partic- rites, and fed to the moon wrasse Thalassoma lunare ularly high (Puglisi et al. 2000). Where sclerites do in aquaria. play a defensive role, their shape, size and abundance de termine their protective efficiency, traits which may differ throughout a coral colony (Sammarco et al. MATERIALS AND METHODS 1987, Van Alstyne et al. 1992, Koh et al. 2000). The family Xeniidae is composed of 34 species and Sample collection and identification is one of the most common and widely distributed oc- tocoral families in the Red Sea (Reinicke 1997). It can Soft coral samples were collected near the city of cover up to 50% of the substrate in some shallow reef Jeddah, Saudi Arabia, in the central Red Sea. Coral Hoang et al.: Predation defense in soft coral 131 (hard and soft) cover in this area ranged from 36 to sodium hypochlorite to dissolve the tissue and leave 61%, of which the family Xeniidae comprised 7.5 to the sclerites. After 12 h, the supernatant was care- 14% (determined by line intercept transects at 3 to fully decanted and fresh sodium hypochlorite was 4 m depth). The 2 xeniid soft coral species were col- added. This process was repeated until the tissue lected by SCUBA diving in 3 to 6 m depth. Ovabunda was completely dissolved and the sclerites remained crenata was collected at off-shore reefs (10 km from on the bottom of the tube. Sclerites were collected the coast) while Heteroxenia ghardaqensis was col- and rinsed 3 times with distilled water, dried in an lected near-shore (50 m from the coast), where the oven at 80°C until completely dry, and weighed.