Natural cleaning of the black-lip pearl oyster Pinctada margaritifera by butterflyfishes (Chaetodon) in French Polynesia
Introduction
In French Polynesia, the large-scale culture of the black-lip pearl oyster, Pinctada margaritifera (L. 1758), has occurred since the 1970s with the development of modern production methods alongside targeted commercial policies making ‘Tahitian cultured Pearls’ an internationally recognized luxury product (Southgate, 2007). However, a constant issue during pearl production is biofouling, the settlement and growth of unwanted sessile plants or animals on the oyster's shell (Wahl, 1989). Biofouling can cause high mortality rates in large oysters (Fitridge et al., 2012) and induce sub-lethal effects on growth and yield (Che et al., 1996, Taylor et al., 1997, Lodeiros et al., 2002). Control measures represent a substantial financial investment with prevention and cleaning costs estimated at between 25 and 30% of the total operational costs of the pearl oyster industry in French Polynesia (Lewis, 1994, Lacoste and Gaertner-Mazouni, 2014).
Prevention techniques can include the use of antifouling compounds such as heavy metals or biocides (Yebra et al., 2004, Chambers et al., 2006). However, as these treatments are detrimental to both the survival and growth of bivalves and the surrounding aquatic environment, pearl farmers more often clear oysters of epibionts using air exposure, freshwater or high-salinity baths, and high-temperature treatments (Taylor et al., 1997). In French Polynesia, manual cleaning using knives, brushes or high-pressured water is also commonplace (Che et al., 1996). However, when conducted repeatedly, this weakens the shell and facilitates the settlement of fouling organisms (Guenther et al., 2006) leading to decreased survival (Pit and Southgate, 2003).
Foraging by mobile marine organisms on shell-associated epibionts could reduce the amount of additional effort required to control biofouling. However, current studies on this topic have largely focused on grazing invertebrates (e.g. sea urchins) and have presented conflicting results concerning the efficiency of these organisms at removing epibiont communities (Lodeiros and Garcia, 2004, Ng et al., 2014). To our knowledge, few empirical studies have investigated the potential for foraging by fishes to reduce biofouling on commercially important bivalves. In French Polynesia, as well as other South Pacific islands, pearl farmers have reported butterflyfishes (Chaetodon) approaching pearl oysters and feeding on their shells (pers. obs.). With this in mind, we examined foraging on pearl oysters by Chaetodon butterflyfishes at Rangiroa Atoll, French Polynesia to determine if these fishes will remove epibionts, what epibionts are consumed or avoided, and if different species are equally effective at reducing biofouling.
Section snippets
Material & methods
Rangiroa Atoll (S 15°14′, W 147°60′) is located in the Tuamotu Archipelago, French Polynesia. Experiments were performed on the north coast, adjacent to the marine and mining resources management organization (Direction des Ressources Marines et Minières, DRMM) outpost.
Chaetodon butterflyfishes are a widely dispersed group of coral reef-associated fishes that often form heterosexual pairs (Yabuta and Berumen, 2013). While a wide degree of dietary specialisation is observed within this genus a
Results
All six species of Chaetodon removed epibionts from oysters during trials with the percentage removed ranging from 40 ± 7% (mean ± SE) in Chaetodon ephippium to 16 ± 4% in Chaetodon trifascialis. On average, epibionts covered 82 ± 2% of the surface of the oyster prior to trials and, only 65 ± 1% following 48 h. C. ephippium (40 ± 7%), Chaetodon ulietensis (34 ± 3%), and Chaetodon auriga (31 ± 3%) removed significantly more epibionts than both Chaetodon lunulatus (17 ± 6%) and C. trifascialis
Discussion
All Chaetodon species examined at Rangiroa Atoll removed epibionts from the surface of P. margaritifera with algae, anemones, tunicates, and sponges most often targeted. C. ephippium was the most efficient cleaner (i.e. it removed the most epibiont biomass ∼40%) while C. trifascialis was the least efficient cleaner (i.e. it removed the least epibiont biomass ∼16%). C. trifascialis, along with C. citrinellus, also removed the most limited range of epibiont types (algae plus either tunicates or
Conclusion
The present study evaluated natural cleaning of black-lip pearl oysters, P. Margaritifera, by Chaetodon butterflyfishes. Targeted removal of epibionts by these fishes could potentially reduce the supplementary effort needed to prevent oyster biofouling. Generalist species should be the focus of future experiments as these fishes removed the greatest amount and range of epibionts. Investment in identifying and developing natural methods of biofouling control would benefit the French Polynesian
Acknowledgments
This study was funded by the ANR Polyperl project (Integrated management and adaptation of pearl culture in French Polynesia in the context of global change: an environmental, economic and social approach, ANR-11-AGRO-0006). We thank the staff of DRMM at Rangiroa for their help during these experiments.
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