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The co-occurrence of the demosponge Hymeniacidon perlevis and the edible mussel Mytilus galloprovincialis as a new tool for bacterial load mitigation in aquaculture

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Abstract

Pollutants in marine coastal areas are mainly a consequence of anthropogenic inputs, and microorganisms often play a major role in determining the extent of this pollution. Thus, practical and eco-friendly techniques are urgently required in order to control or minimise the pathogenic bacterial problem. The bacterial accumulation of Mytilus galloprovincialis (Lamarck 1919) in the presence or absence of another filter feeder, the demosponge Hymeniacidon perlevis (Montagu 1818) on sewage flowing into the Northern Ionian Sea has been estimated in a laboratory study. On account of the interesting results obtained, we also evaluated the bioremediation capability of the sponges when reared in co-culture with mussels. Specimens of M. galloprovincialis and H. perlevis were collected from the Mar Grande and from the Second Inlet of the Mar Piccolo of Taranto (Northern Ionian Sea, Italy), respectively. In the laboratory, we detected the bacterial abundances in the sewage, in sponge homogenates (both sponges alone and sponges that have been added to sewage with mussels) and in mussel homogenates (both mussels alone and mussels that have been added to sewage with sponges). In the field, we estimated the bacterial concentration in both the seawater within the mussels culture and the seawater collected where mussels were reared in co-culture with sponges. The bacteriological analyses were performed analysing the following parameters: the density of culturable heterotrophic bacteria by spread plate on marine agar, total culturable bacteria at 37 °C on plate count agar and vibrios on thiosulphate–citrate–bile–sucrose–salt (TCBS) agar. Total coliforms, Escherichia coli and intestinal streptococci concentrations were detected by the MPN method. The study demonstrates a higher efficiency of the sponges in removing all the considered bacterial groups compared to the mussels. Due to the conspicuous bacterial accumulation by the sponge, we can conclude that the co-occurrence of the filter-feeder H. perlevis with M. galloprovincialis is a powerful tool in reducing the bacterial load in shellfish culture areas thus playing a role in mitigating the health hazard related to the consumption of edible mussels.

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References

  • Angulo FJ (2000) Antimicrobial agents in aquaculture: potential impact on health. APUA Newsletter 18:1–6

    Google Scholar 

  • Angulo FJ, Nargund VN, Chiller TC (2004) Evidence of an association between use of antimicrobial agents in food animals and antimicrobial resistance and health consequences of such resistance. J Vet Med 51(8–9):374–379

    Article  CAS  Google Scholar 

  • APHA, AWWA, WEF (1998) Standard Methods for the examination of water and wastewater, 20th edn. American Public Health Association/American Water Works Association/Water Environment Federation, Washington, DC

    Google Scholar 

  • ASQAP (Australian Shellfish Quality Assurance Program) Operations Manual (2004) Australian Shellfish Quality Assurance Advisory Committee, Australia

  • Berberovic RJ (2001) Possibilities and limits of wastewater-fed aquaculture. In: Werner C, Schlick J, Witte G. and Hildebrandt A (eds) Ecosan—closing the loop in wastewater management and sanitation. Proceedings of the International Symposium, 30–31 October 2000, Bonn, Germany, pp 113–122

  • Boxall AB, Fogg LA, Blackwell PA, Kay P, Pemberton EJ, Croxford A (2004) Veterinary medicines in the environment. Rev Environ Contam T 180:1–91

    CAS  Google Scholar 

  • Cabello FC (2004) Antibiotics and aquaculture in Chile: implications for human and animal health. Rev Med Chile 132:1001–1006

    Article  CAS  Google Scholar 

  • Caroppo C, Stabili L, Aresta M, Corinaldesi C, Danovaro R (2006) Impact of heavy metals and PCBs on marine picoplankton. Environ Toxicol 21(6):541–551

    Article  CAS  Google Scholar 

  • Cavallo RA, Stabili L (2002) Presence of vibrios in seawater and Mytilus galloprovincialis (Lam.) from the Mar Piccolo of Taranto (Ionian Sea). Wat Res 36:3719–3726

    Article  CAS  Google Scholar 

  • Corriero G, Longo C, Mercurio M, Nonnis Marzano C, Lembo G, Spedicato MT (2004) Rearing performance of Spongia officinalis on suspended ropes off the Southern Italian coast (Central Mediterranean Sea). Aquaculture 238:195–205

    Article  Google Scholar 

  • Danulat E, Muniz P, García-Alonso J, Yannicelli B (2002) Fist assessment of the highly contaminated harbour of Montevideo, Uruguay. Mar Pollut Bull 44:554–565

    Article  CAS  Google Scholar 

  • Doering PH, Oviatt CA (1986) Application of filtration rate models to field populations of bivalves; an assessment using experimental mesocosms. Mar Ecol Prog Ser 31:265–275

    Article  Google Scholar 

  • Food and Agriculture Organization of the United Nations (2012) The state of world fisheries and aquaculture. FAO Fisheries and Aquaculture Department, Rome

    Google Scholar 

  • Frost TM (1980) Clearance rate determinations for the freshwater sponge Spongilla lacustris: effects of temperature, particle type and concentration, and sponge size. Arch Hydrobiol 90:330–356

    Google Scholar 

  • Fu W, Sun L, Zhang X, Zhang W (2006) Potential of the marine sponge Hymeniacidon perleve as biorimediator of pathogenic bacteria in integrated aquaculture ecosystems. Biotechnol Bioeng 93(6):1112–1122

    Article  CAS  Google Scholar 

  • Gaino E, Cardone F, Corriero G (2010) Reproduction of the intertidal sponge Hymeniacidon perlevis (Montagu) along a bathymetric gradient. Open Mar Biol J 4:47–56

    Article  Google Scholar 

  • Gifford S, Dunstan RH, O’Connor W, Koller CE, MacFarlane GR (2006) Aquatic zooremediation: deploying animals to remediate contaminated aquatic environments. Trends Biotechnol 25(2):60–65

    Article  Google Scholar 

  • GPA (2001) The global programme of action for the protection of the marine environment from landbased activities. Artoos Drukkerijen, Rijswijk, Netherlands

    Google Scholar 

  • Haya K, Burridge LE, Chang BD (2000) Environmental impact of chemical wastes produced by the salmon aquaculture industry. ICES J Mar Sci 58:492–496

    Article  Google Scholar 

  • International Organization for Standardization (1998) Water quality—detection and enumeration of intestinal enterococci—part 1: miniaturized method (most probable number) for surface and waste water. International Organization for Standardization, ISO 7899–1

  • Jorgensen CB, Kiorboe T, Mohlenberg F, Riisgård HU (1984) Ciliary and mucus net filter feeding, with special reference to fluid mechanical characteristics. Mar Ecol Prog Ser 15:283–292

    Article  Google Scholar 

  • Kilian EF (1952) Waterflow and food intake in freshwater sponge Ephydatia fluviatilis. Wasserströmung und Nahrungsaufnahme beim Süßwasser schwämmen Ephydatia fluviatilis. Z Vergl Physiol 34:407–447

    Article  Google Scholar 

  • Kiorboe T, Mohlenberg F, Nohr O (1981) Effect of suspended bottom material on growth and energetics in Mytilus edulis. Mar Biol 61:283–288

    Article  Google Scholar 

  • Leung TLF, Bates AE (2013) More rapid and severe disease outbreaks for aquaculture at the tropics: implications for food security. J Appl Ecol 50:215–222

    Article  Google Scholar 

  • Licciano M, Stabili L, Giangrande A (2005) Clearance rates of Sabella spallanzanii and Branchiomma luctuosum (Annelida: Polychaeta) on a pure culture of Vibrio alginolyticus. Water Res 39(18):4375–4384

    Article  CAS  Google Scholar 

  • Licciano M, Stabili L, Giangrande A, Cavallo RA (2007a) Bacterial accumulation by Branchiomma luctuosum (Annelida: Polychaeta): a tool for biomonitoring marine systems and restoring polluted waters. Mar Environ Res 63:291–302

    Article  CAS  Google Scholar 

  • Licciano M, Terlizzi A, Giangrande A, Cavallo RA, Stabili L (2007b) Filter-feeder macroinvertebrates as key players in bacterioplankton biodiversity control: a case of study with Sabella spallanzanii (Polychaeta: Sabellidae). Mar Environ Res 64:504–513

    Article  CAS  Google Scholar 

  • Longo C, Corriero G, Licciano M, Stabili L (2010) Bacterial accumulation by the Demospongiae Hymeniacidon perlevis (Montagu): a tool for the bioremediation of polluted seawater. Mar Pollut Bull 60:1182–1187

    Article  CAS  Google Scholar 

  • Mohlenberg F, Riisgård HU (1978) Efficiency of particle retention in 13 species of suspension feeding bivalves. Ophelia 17:239–246

    Article  Google Scholar 

  • NSSP (National Shellfish Sanitation Program) (1999) Guide for the Control of Molluscan Shellfish, Model Ordinance. Chapter IV. U.S. Department of Health and Human Services, U.S. Food and Drug Administration, Centre for Food Safety and Applied Nutrition, Washington, D.C

    Google Scholar 

  • Ostroumov SA (2005) Some aspects of water filtering activity of filter-feeders. Hydrobiologia 542:275–286

    Article  CAS  Google Scholar 

  • Ostroumov SA, Widdows J (2006) Inhibition of mussel suspension feeding by surfactants of three classes. Hydrobiologia 556:381–386

    Article  CAS  Google Scholar 

  • Petersen JK, Riisgård HU (1992) Filtration capacity of the ascidian Ciona intestinalis and its grazing impact in a shallow fjord. Mar Ecol Prog Ser 88:9–17

    Article  Google Scholar 

  • Reilly A, Käferstein F (1997) Food safety hazards and the application of the principles of the hazard analysis and critical control point (HACCP) system for their control in aquaculture production. Aquac Res 28:735–752

    Article  Google Scholar 

  • Rigos G, Troisi G (2005) Antibacterial agents in Mediterranean finfish farming: a synopsis of drug pharmacokinetics in important euryhaline fish species and possible environmental implications. Rev Fish Biol Fisher 15(1–2):53–73

    Article  Google Scholar 

  • Riisgård HU (2001) On measurement of filtration rates in bivalves-the stony road to reliable data: review and interpretation. Mar Ecol Progr Ser 211:275–291

    Article  Google Scholar 

  • Simpson TL (1984) The Cell Biology of Sponges. Springer Verlag, New York

    Book  Google Scholar 

  • Stabili L, Acquaviva MI, Cavallo RA (2005) Mytilus galloprovincialis filter feeding on the bacterial community in a Mediterranean coastal area (Northern Ionian Sea, Italy). Water Res 39:469–477

    Article  CAS  Google Scholar 

  • Stabili L, Licciano M, Giangrande A, Fanelli G, Cavallo RA (2006a) Sabella spallanzanii filter-feeding on bacterial community: ecological implications and applications. Mar Environ Res 61:74–92

    Article  CAS  Google Scholar 

  • Stabili L, Licciano M, Giangrande A, Longo C, Mercurio M, Nonnis-Marzano C, Corriero G (2006b) Filtering activity of Spongia officinalis var. adriatica (Schmidt) (Porifera, Demospongiae) on bacterioplankton: implications for bioremediation of polluted seawater. Water Res 40:3083–3090

    Article  CAS  Google Scholar 

  • Stabili L, Licciano M, Longo C, Corriero G, Mercurio M (2008) Evaluation of microbiological accumulation capability of the commercial sponge Spongia officinalis var. adriatica (Schmidt) (Porifera, Demospongiae). Water Res 42:2499–2506

    Article  CAS  Google Scholar 

  • Stabili L, Schirosi R, Licciano M, Mola E, Giangrande A (2010) Bioremediation of bacteria in aquaculture waste using the polychaete Sabella spallanzanii. New Biotechnol 27:774–781

    Article  CAS  Google Scholar 

  • Stone AR (1970) Growth and reproduction of Hymeniacidon perleve (Montagu) (Porifera) in Langstone Harbour Hampshire. J Zool 161:443–459

    Article  Google Scholar 

  • Tyrrel SF (1999) The microbiological quality of water used for irrigation. Irrig News 27:39–42

    Google Scholar 

  • Umgiesser G, Scroccaro I, Alabiso G (2007) Mass exchange mechanisms in the Taranto Sea. Transit Waters Bull 2:59–71

    Google Scholar 

  • Underwood AJ (1997) Experiments in ecology: their logical design and interpretation using analysis of variance. Cambridge University Press, Cambridge

    Google Scholar 

  • World Health Organization (2003) The world health report 2003. Shaping the future. World Health Report, World Health Organization, Geneva, Switzerland

    Google Scholar 

  • Xue S, Zhang HT, Wu PC, Zhang W, Yuan Q (2004) Study on bioactivity of extracts from marine sponges in Chinese Sea. J Exp Mar Biol Ecol 298(1):71–78

    Article  Google Scholar 

  • Zhang C, Jia L, Wang SH, Qu J, Xu LL, Shi HH, Yan YC (2010) Biodegradation of beta-cypermethrin by two Serratia spp. with different cell surface hydrophobicity. Bioresource Technol 101:3423–342

    Article  CAS  Google Scholar 

  • Zheng L, Yan X, Han X, Chen H, Lin W, Lee FS, Wang X (2006) Identification of norharman as the cytotoxic compound produced by the sponge (Hymeniacidon perleve)-associated marine bacterium Pseudoalteromonas piscicida and its apoptotic effect on cancer cells. Biotechnol Appl Bioc 44(3):135–142

    Article  CAS  Google Scholar 

Download references

Acknowledgments

We are grateful to Dr. Giuseppe Portacci of the IAMC-CNR Taranto for his technical support provided during the sample collection. This study was carried out as part of the Italian RITMARE project funded by the Ministry of University and Research (MIUR).

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Correspondence to Loredana Stabili.

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Responsible editor: Robert Duran

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Longo, C., Cardone, F., Corriero, G. et al. The co-occurrence of the demosponge Hymeniacidon perlevis and the edible mussel Mytilus galloprovincialis as a new tool for bacterial load mitigation in aquaculture. Environ Sci Pollut Res 23, 3736–3746 (2016). https://doi.org/10.1007/s11356-015-5587-z

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