Human stressors are driving coastal benthic long-lived sessile fan mussel pinna nobilis population structure more than environmental stressors

PLoS ONE

Volumn 10, Issue 7, 2015, Pages

  Deudero, Salud ^a   Vázquez Luis, Maite ^a   Álvarez, Elvira ^b  

^a Centro Oceanográfico de Baleares   (Spain)

^b Govern de les Illes Balears Direcció General de Medi Rural I Marí   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; BENTHOS; COASTAL WATERS; CONTROLLED STUDY; DIVING; ENVIRONMENTAL IMPACT; ENVIRONMENTAL PROTECTION; ENVIRONMENTAL STRESS; FISHING; GLOBAL CHANGE; MUSSEL; NONHUMAN; PINNA NOBILIS; POPULATION DENSITY; SEWAGE EFFLUENT; SPECIES DISTRIBUTION; SPECIES HABITAT; TSUNAMI; ANIMAL; BIVALVE; ECOSYSTEM; ENVIRONMENTAL EXPOSURE; HUMAN; HUMAN ACTIVITIES; MENTAL STRESS; PHYSIOLOGY;

ANIMALS; BIVALVIA; CONSERVATION OF NATURAL RESOURCES; ECOSYSTEM; ENVIRONMENTAL EXPOSURE; HUMAN ACTIVITIES; HUMANS; POPULATION DENSITY; STRESS, PSYCHOLOGICAL;

EID: 84941915349     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0134530     Document Type: Article

References (43)

1. Schultz PW, Huber M. Revision of the worldwide Recent Pinnidae and some remarks of fossil European Pinnidae. Acta Conch. 2013; 13: 1-164.
2. Lemer S, Buge B, Bemis A, Giribet G. First molecular phylogeny of the circumtropical bivalve family Pinnidae (Mollusca, Bivalvia): Evidence for high levels of cryptic species diversity. Molecular Phylogenetics and Evolution 2014; 75: 11-23. doi:10.1016/j.ympev.2014.02.008 PMID: 24569016.
3. WoRMS, World Register of Marine Species. 2014. Available: http://www.marinespecies.orgatVLIZ.
4. Zavodnik D, Hrs-Brenko M, Legac M. Synopsis on the fan shell Pinna nobilis L. in the eastern Adriatic Sea. In: Boudouresque C.F., Avon M., Gravez V., (eds) Les Espèces Marines à Protéger en Méditerranée. Gis Posidonie publ. Marseille. 1991; 169-178.
5. Butler AJ, Vicente N, De Gaulejac B. Ecology of the pteroid bivalves Pinna bicolor Gmelin and Pinna nobilis Linnaeus. Marine Life 1993; 3: 37-45.
6. Vicente N, Moreteau JC. Statut of Pinna nobilis L. en Méditerranée (Mollusque Eulamellibranche). In, Boudouresque C.F., Avon M., Garvez M., (Ed) Les Espèces Marines à Protèger en Méditerranée. GIS Posidonie Publ. 1991; 159-168.
7. Richardson CA, Peharda M, Kennedy H, Kennedy P, Onofri V. Age, growth rate and season of recruitment of Pinna nobilis (L) in the Croatian Adriatic determinated from Mg: Ca and Sr: Ca shell profiles. Journal of Experimental Marine Biology and Ecology. 2004; 299: 1-16.
8. SPA/BD Protocol. Annex II of SPA and Biodiversity Protocol. Barcelona Convention Protocol concerning Specially Protected Areas and Biological Diversity in the Mediterranean. 1995. Available: http://racspa.org/sites/default/files/annex/annex-2-en-2013.pdf.
9. EU Habitats Directive, 2007. Council Directive 92/43/EEC of 21 May 1992 on the conservation of natural habitats and of wild fauna and flora. Annex IV: Animal and plant species of community interest in need of strict protection. Available: http://ec.europa.eu/environment/nature/legislation/habitatsdirective/index-en.htm.
10. Katsanevakis S. Growth and mortality rates of the fan mussel Pinna nobilis in Lake Vouliagmeni (Korinthiakos Gulf, Greece): A generalized additive modelling approach. Marine Biology. 2007; 152: 1319- 1331.
11. Hendriks I, Tenan S, Tavecchia G, Marbà N, Jordà G, Deudero S, et al. Boat anchoring impacts coastal populations of the pen shell, the largest bivalve in the Mediterranean. Biological Conservation. 2013; 160: 105-113.
12. Prado P, Caiola N, Ibáñez C. Habitat use by a large population of Pinna nobilis in shallow waters. Scientia Marina. 2014; 78(4): 555-565.
13. Vázquez-Luis M, Borg JA, Morell C, Banach-Esteve G, Deudero S. Influence of boat anchoring on Pinna nobilis: A field experiment using mimic units. Marine and Freshwater Research. 2015. Available: doi:10.1071/MF14285.
14. Brown JH. On the relationship between abundance and distribution of species. The American Nauralist. 1984; 124 (2): 255-279.
15. Claudet J, Fraschetti F. Human-driven impacts on marine habitats: A regional meta-analysis in the Mediterranean Sea. Biological Conservation 1. 2010; 43(9): 2195-2206.
16. Katsanevakis S, Poursanidis D, Issaris Y, Panou A, Petza D, Vassilopoulou V, et al. "Protected" marine shelled molluscs: Thriving in Greek seafood restaurants. Mediterranean Marine Science. 2011; 12(2): 429-438.
17. García-March JR, Pérez-Rojas L, García-Carrascosa AM. Influence of hydrodynamic forces on population structure of Pinna nobilis L., 1758 (Mollusca: Bivalvia): The critical combination of drag force, water depth, shell size and orientation. Journal of Experimental Marine Biology and Ecology. 2007; 342: 202-212.
18. Hendriks IE, Cabanellas-Reboredo M, Bouma TJ, Deudero S, Duarte CM. Seagrass meadows modify drag forces on the Shell of the Fan Mussel Pinna nobilis. Estuaries and Coasts. 2011; 34: 60-67.
19. Coppa S, Andrea de Lucia G, Magni P, Domenici P, Antognarelli F, Satta A, Cucco A. The effect of hydrodynamics on shell orientation and population density of Pinna nobilis in the Gulf of Oristano (Sardinia, Italy). Journal of Sea Research. 2013; 76: 201-210.
20. Basso L, Vázquez-Luis M, García-March JR, Deudero S, Alvarez E, Vicente N, et al. The pen shell Pinna nobilis, state-of-the-art, research priorities and best practices. Advances in Marine Biology. 2015: in press.
21. Marbà N, Duarte CM, Díaz-Almela E, Terrados J, Álvarez E, Martínez R, et al. Direct evidence of imbalanced seagrass (Posidonia oceanica) shoot population dynamics along the Spanish Mediterranean. Estuaries 2005; 28: 53-62.
22. Procaccini G, Buia MC, Gambi MC, Perez M, Pergent G, Pergent-Martini C, Romero J. The seagrasses of the Western Mediterranean, In: World Atlas of Seagrasses, Green E.P.; Short F.T. 2003; 48-58. UNEP World Conservation Monitoring Centre, University of California Press, Berkeley, ISBN 0-520- 24047-2.
23. Deudero S, Vallespir J, Obrador M. Atlas de Biodiversidad Marina del Mar Balear. 2011. Available: http://www.ba.ieo.es.
24. Vázquez-Luis M, March D, Alvarez E, Alvarez-Berastegui D, Deudero S. Spatial distribution modelling of the endangered bivalve Pinna nobilis in a Marine Protected Area. Mediterranean Marine Science. 2014; 15/3: 626-634.
25. Historical Governamental dataset. WANA provide temporal series from numeric modeling. Puertos del Estado. Available: http://www.puertos.es/es-es/oceanografia/Paginas/portus.aspx.
26. Data obtained from local knowledge and Google Earth historical images.
27. Database sewage effluents Available: http://dgrechid.caib.es/www/ajuda-fondeig/visor/es.html.
28. Anderson MJ. PERMANOVA-2 factor: A FORTRAN computer program for permutational multivariate analysis of variance (for any two-factor ANOVA design) using permutation test. Department of Statistics, University of Auckland, Auckland. 2004.
29. Clarke KR, Gorley RN. PRIMER v6: user manual/tutorial. PRIMER-E, Plymouth. 2006.
30. Anderson MJ, Gorley RN, Clarke KR. PERMANOVA+ for PRIMER: guide to software and statistical methods. PRIMER-E, Plymouth. 2008.
31. Legendre P, Anderson MJ. Distance-based redundancy analysis: Testing multispecies responses in multifactorial ecological experiments. Ecological Monographs. 1999; 69: 1-24.
32. Claudet J, Osenberg CW, Benedetti-Cecchi L, Domenici P, García-Charton J-A, Pérez-Ruzafa Á, et al. Planes S. Marine reserves: Size and age do matter. Ecology Letters. 2008; 11(5): 481-489. doi:10.1111/j.1461-0248.2008.01166.xPMID: 18294212.
33. Fraschetti S, Guarnieri G, Bevilacqua S, Terlizzi A, Boero F. Protection Enhances Community and Habitat Stability: Evidence from a Mediterranean Marine Protected Area. PlosONE. 2013; 8(12): e81838.
34. Addis P, Secci M, Brundu G, Manunza A, Corrias S, Cau A. Density, size structure, shell orientation and epibiontic colonization of the fan mussel Pinna nobilis L. 1758 (Mollusca: Bivalvia) in three contrasting habitats in an estuarine area of Sardinia (W Mediterranean). Scientia Marina. 2009; 73(1): 143- 152.
35. Coppa S., Guala I., de Lucia G. A., Massaro G., & Bressan m. Of Oristano (Italy). Università degli studi della Tuscia di Viterbo, 2010; 90(5), 885-894.
36. Rabaoui L, Tlig-Zouari S, Katsanevakis S, Ben Hassine OK. Modelling population density of Pinna nobilis (Bivalvia) on the eastern and southertern coast of Tunisia. Journal of Molluscan Studies. 2010; 76: 340-347.
37. Waycott M, Duarte CM, Carruthers TJB, Orth RJ, Dennison WC, Olyarnik S, Calladine A, Fourqurean JW, Heck KL Jr, Hughes AR, Kendrick GA, Kenworthy WJ, Short FT, Williams SL. Accelerating loss of seagrasses across the globe threatens coastal ecosystems. PNAS, Proceedings of the National Academy of Sciences. 2009; 106(30): 12377-12381.
38. Boudouresque CF, Bernard G, Pergent G, Shili A, Verlaque M. Regression of Mediterranean seagrasses caused by natural processes and anthropogenic disturbances and stress: A critical review. Botanica Marina. 2009; 52(5): 395-418.
39. Cabanellas-Reboredo M, Deudero S, Alós J, Valencia JM, March D, Hendriks I, Alvarez E. Recruitment of Pinna nobilis (Mollusca: Bivalvia) on artificial structures. Marine Biodiversity Records. 2009; (2: ):126.
40. Alomar C, Vázquez-Luis M, Magraner K, Lozano L, Deudero S. Evaluating stable isotopic signals at bivalve Pinna nobilis under different human pressures. Journal of Experimental Marine Biology and Ecology. 2015; 467: 77-86.
41. Luna B, Valle C, Sanchez-Lizaso JL. Benthic impacts of recreational divers in a Mediterranean Marine Protected Area. ICES Journal of Marine Science. 2009; 66:517-523.
42. Milazzo M, Chemello R, Badalamenti F, Riggio RC, Riggio S. The impact of human recreational activities in marine protected areas: What lessons should be learnt in the Mediterranean sea? Marine Ecology. 2002; 23 (SUPPL. 1), 280-290.
43. Balaguer P, Diedrich A, Sardá R, Fuster M, Cañellas B, Tintoré J. Spatial analysis of recreational boating as a first key step for marine spatial planning in Mallorca (Balearic Islands, Spain).Ocean and Coastal Management. 2011; 54: 241-249.