The exploitation of limpets in a Mediterranean Marine Protected Area: assessing the effectiveness of protection in the intertidal zone


Published: Jan 17, 2018
Keywords:
Patella Mediterranean human harvesting intertidal accessibility marine protected area
STEFANO MARRA
STEFANIA COPPA
ANDREA CAMEDDA
GIORGIO MASSARO
GIUSEPPE A. de LUCIA
Abstract

Limpets are intertidal keystone grazers and their overexploitation could have significant consequences for intertidal communities. Limpets are harvested around the Sinis Peninsula (Sardinia, Italy) but harvesting is prohibited within the “Penisola del Sinis - Isola di Mal di Ventre” Marine Protected Area (MPA). This work assesses the effects of human harvesting on the population dynamics of three common Mediterranean species of Patella, namely, P. rustica, P. caerulea and P. ulyssiponensis, testing the effectiveness of the MPA and the role of site accessibility in limiting the intensity of such harvesting pressure. In the period between June 2015 and August 2016, limpet abundance and size were recorded on a monthly basis by means of photographic frames within linear transects at ten sites spread out along the coastline of the Sinis Peninsula to assess growth and temporal patterns. Limpets older than two years are extremely rare in the study area. Limpets are more abundant within the MPA in comparison with non-protected areas and within less accessible sites in comparison with areas where the intertidal zone is easily accessible from land. Despite this, overall human-induced mortality in the area is high, indeed the pool of limpets observed with a mean density of 104.3 ± 9.7 limpets/m2 during the first survey was reduced by 99.2%in less than one year. This work demonstrates that human harvesting strongly affects the population dynamics of Patella species in the area and that within the MPA this stressor is not efficiently reduced.

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Airoldi, L., Beck, M.W., 2007. Loss, status and trends for coastal marine habitats of Europe. Oceanography and Marine Biology. An Annual Review. 45, 345-405. DOI: 10.1201/9781420050943.ch7.
Anderson, M.J., Gorley, R.N., Clarke, K.R., 2008. PERMANOVA+ for PRIMER: Guide to Software and Statistical Methods. PRIMER-E: Plymouth, UK. 214 pp.
Belkhodja, H., Romdhane, M.S., 2012. Etude morphométrique du mollusque gastéropode” Patella caerulea Linnaeus”, 1758 des côtes nord de la Tunisie. Bulletin de l’Institut National des Sciences et Technologies de la Mer de Salammbô. 39, 15-23.
Boaventura, D., Alexander, M., Della Santina, P., Smith N.D., Ré, P. et al., 2002. The effects of grazing on the distribution and composition of low-shore algal communities on the central coast of Portugal and on the southern coast of Britain. Journal of Experimental Marine Biology and Ecology. 267, 185-206. DOI: 10.1016/S0022-0981(01)00372-0.
Borges, C.D.G., Hawkins, S.J., Doncaster, C.P., Crowe T.P., 2015. Effects of simulated human exploitation of a key grazer, Patella vulgata, on rocky shore assemblages. Marine Ecology Progress Series. 533, 163-176. DOI: 10.3354/meps11356.
Branch, G.M., 1974. The Ecology of Patella Linnaeus from the Cape peninsula, South Africa. III. Growth rates. Transactions of the Royal Society of South Africa. 41 (2), 161-193. DOI: 10.1080/00359197409520068.
Branch, G.M., Marsh, A.C., 1978. Tenacity and shell shape in six Patella species: adaptive features. Journal of Experimental Marine Biology and Ecology. 34 (2), 111-130. DOI:10.1016/0022-0981(78)90035-7.
Branch, G.M., 1981. The biology of limpets: physical factors, energy flow, and ecological interactions. Oceanography and Marine Biology. An Annual Review. 19, 235-380.
Branch, G.M., Odendaal, F., 2003. The effects of marine protected areas on the population dynamics of a South African limpet, Cymbula oculus, relative to the influence of wave action. Biological Conservation. 114 (2), 255-269. DOI:10.1016/S0006-3207(03)00045-4.
Brazão, S.A., Silva, A.C., Boaventura, D.M., 2009. Predation: a regulating force of intertidal assemblages on the central Portuguese coast? Journal of the Marine Biological Association of the UK. 89 (08), 1541-1548. DOI: 10.1017/S0025315409000757.
Bustamante, R., Branch, G., 1996. Large scale patterns and trophic structure of southern African rocky shores: the roles of geographic variation and wave exposure. Journal of Biogeography. 23 (3), 339-351. DOI: 10.1046/j.1365-2699.1996.00026.x.
Cannicci, S., Gomei, M., Dahdouh-Guebas, F., Rorandelli, R., Terlizzi, A., 2007. Influence of seasonal food abundance and quality on the feeding habits of an opportunistic feeder, the intertidal crab Pachygrapsus marmoratus. Marine Biology. 151, 1331-1342. DOI: 10.1007/s00227-006-0570-3.
Casola, E., Lariccia, M., Scardi, M., 2014. Areee Marine Protette e pesca professionale, Unimar: Roma. 199 pp.
Ceccherelli, G., Casu, D., Sechi, N., 2005. Spatial variation of intertidal assemblages at Tavolara-Capo Coda Cavallo MPA (NE Sardinia): geographical vs. protection effect. Marine Environmental Research. 59 (5), 533-546. DOI: 10.1016/j.marenvres.2004.09.002.
Ceccherelli, G., Pais, A., Pinna, S., Sechi, N., Chessa, L. A., 2011. Human impact on Paracentrotus lividus: the result of harvest restrictions and accessibility of locations. Marine Biology. 58, 845-852. DOI: 10.1007/s00227-010-1611-5.
Christiaens, J., 1973. Révision du genre Patella (Mollusca, Gastropoda). Bulletin du Muséum national d’histoire naturelle (Sér 3). 182, 1305-1392.
Coppa, S., de Lucia, G.A., Massaro, G., Camedda, A., Marra, S. et al., 2016. Is the establishment of MPAs enough to preserve endangered intertidal species? The case of Patella ferruginea in the Mal di Ventre Island (W Sardinia, Italy). Aquatic Conservation - Marine And Freshwater Ecosystem. 26, 623-638. DOI: 10.1002/aqc.2579.
Coppa, S., de Lucia, G. A., Massaro, G., Magni, P., 2012. Density and distribution of Patella ferruginea in a Marine Protected Area (western Sardinia, Italy): constraint analysis for population conservation. Mediterranean Marine Science. 13, 108-117. DOI: 10.12681/mms.27.
Crowe, T.P., Thompson, R.C., Bray, S., Hawkins, S.J., 2000. Impacts of anthropogenic stress on rocky intertidal communities. Journal of Aquatic Ecosystem Stress and Recovery. 7, 273-297. DOI: 10.1023/A:1009911928100.
De Santo, E. M., 2013. Missing marine protected area (MPA) targets: how the push for quantity over quality undermines sustainability and social justice. Journal of Environmental Management. 124, 137-146. DOI: 10.1016/j.jenvman. 2013.01.033
Denny, M.W., 2000. Limits to optimization: fluid dynamics, adhesive strength and the evolution of shape in limpet shells. Journal of Experimental Biology. 203, 2603-2622.
Denny, M.W. Blanchette, C.A., 2000. Hydrodynamics, shell shape, behaviour and survivorship in the owl limpet Lottia gigantea. Journal of Experimental Biology. 203, 2623-2639.
Diogo, H., Pereira, J.G., Schmiing, M., 2016. Catch me if you can: Non-compliance of limpet protection in the Azores. Marine Policy. 63, 92-99. DOI: 10.1016/j.ma pol.2015.10.007.
Ebenman, B., Jonsson, T., 2005. Using community viability analysis to identify fragile systems and keystone species. Trends in Ecology & Evolution. 20 (10), 568-575. DOI:10.1016/j.tree.2005.06.011.
Edgar, G.J., Stuart- Smith, R.D., Willis, T.J., Kininmonth, S., Baker, S.C. et al., 2014. Global conservation outcomes depend on marine protected areas with five key features. Nature. 506, 216-220. DOI: 10.1038/nature13022
Espinosa, F., Guerra- García, J.M., Fa, D., García- Gómez, J.C., 2006. Aspects of reproduction and their implications for the conservation of the endangered limpet, Patella ferruginea. Invertebrate Reproduction & Development. 49, 85-92. DOI: 10.1080/07924259.2006.9652197.
Espinosa, F., Gonzáles, A.R., Maestre, M.J., Fa, D., Guerra-García, J.M., 2008. Responses of the endangered limpet Patella ferruginea to reintroduction under different environmental conditions: survival, growth rates and life history. Italian Journal of Zoology. 75, 371-384. DOI:10.1080/11250000801887740.
Espinosa, F., Rivera- Ingraham, G.A., 2016. Biological conservation of giant limpets: the implications of large size Adv. Marine Biology. DOI: 10.1016/bs.amb.2016.10.002
Espinosa, F., Rivera- Ingraham, G.A., Fa, D., García-Gómez, J.C., 2009. Effect of human pressure on population size structures of the endangered ferruginean limpet: toward future management measures. Journal of Coastal Research. 25 (4), 857-863. DOI: 10.2112/08-1005.1.
Espinosa, F., Rivera-Ingraham, G.A., Maestre, M., González, A.R., Bazairi, H. et al., 2014. Updated global distribution of the threatened marine limpet Patella ferruginea (Gastropoda: Patellidae): an example of biodiversity loss in the Mediterranean. Oryx. 48 (02), 266-275. DOI:10.1017/S0030605312000580.
Fenberg, P.B., Caselle, J.E., Claudet, J., Clemence, M., Gaines, S.D. et al., 2012. The science of European marine reserves: Status, efficacy, and future needs. Marine Policy. 36, 1012-1021. DOI:10.1016/j.marpol.2012.02.021.
Fenberg, P.B., Roy, K., 2008. Ecological and evolutionary consequences of size-selective harvesting: how much do we know? Molecular Ecology. 17 (1), 209-220. DOI: 0.1111/j.1365-294X.2007.03522.x0.
Fenberg, P.B., Roy, K., 2012. Anthropogenic harvesting pressure and changes in life history: insights from a rocky intertidal limpet. American Naturalist. 180 (2), 200-210. DOI: 10.1086/666613.
Ferraz, R.R., Menezes, G.M., Santos, R.S., 2001. Limpet (Patella spp.) (Mollusca: Gastropoda) exploitation in the Azores, during the period 1993-1998. Arquipélago. Life and Marine Sciences. Suppl. 2 (Part B), 59-65.
Flores, A.A. V., Cruz, J., Paula, J., 2001. Intertidal distribution and species composition of brachyuran crabs at two rocky shores in Central Portugal. Hydrobiologia 449, 171-177. DOI: 10.1023/A:1017573927565.
Garcia, A., Smith, J.R., 2013. Factors influencing human visitation of southern California rocky intertidal ecosystems. Ocean & Coastal Management. 73, 44-53. DOI: 10.1016/j.ocecoaman.2012.12.006
García-Gómez, J.C., Guerra-García, J.M., Espinosa, F., Maestre, M.J., Rivera-Ingraham, G., et al., 2015. Artificial Marine
Micro-Reserves Networks (AMMRNs): an innovative approach to conserve marine littoral biodiversity and protect endangered species. Marine Ecology. 36 (3), 259-277. DOI: 10.1111/maec.12167.
Gayanilo, F.C., Sparre, P., Pauly, D., 2005. FAO-ICLARM Stock Assessment Tools II (FiSAT II). Revised version. User’s guide. 168 pp.
Guidetti, P., Milazzo, M., Bussotti, S., Molinari, A., Murenu, M. et al., 2008. Italian marine reserve effectiveness: does enforcement matter? Biological Conservation. 141, 699-709. DOI: 10.1016/j.biocon.2007.12.013.
Halpern, B.S, Frazier, M., Potapenko, J., Casey, K.S., Koenig, K. et al., 2015. Spatial and temporal changes in cumulative human impacts on the world’s ocean. Nature Communications. 14;6: 7615. DOI: 10.1038/ncomms8615.
Jenkins S.R., Coleman, R.A., Della Santina, P.S., Hawkins, J., Burrows, M.T. et al., 2005. Regional scale differences in the determinism of grazing effects in the rocky intertidal.
Marine Ecology Progress Series. 287, 77-86. DOI: 10.3354/meps287077.
Katsanevakis, S., Levin, N., Coll, M., Giakoumi, S., Shkedi, D. et al., 2015. Marine conservation challenges in an era of economic crisis and geopolitical instability: the case of the Mediterranean Sea. Marine Pollution. 51, 31-39. DOI: 10.1016/j.marpol.2014.07.013
Keough, M.J., Quinn, G.P., 2000. Legislative vs. practical protection of an intertidal shoreline in southeastern Australia. Ecological Applications. 10 (3), 871-881. DOI: 10.1890/1051-0761(2000)010[0871:LVPPOA]2.0.CO;2.
Khow, A.S., 2007. Growth determination of tropical limpet Cellana testudinaria (Linnaeus, 1758) living on the rocky shore of Ohoiwait, Southeast Moluccas, Indonesia. The Journal of Coastal Development. 10 (2), 89-103.
Kido, J.S., Murray, S.N., 2003. Variation in owl limpet Lottia gigantea population structures, growth rates, and gonadal production on southern California rocky shores. Marine Ecology Progress Series. 257, 111-124. DOI:10.3354/meps257111.
Lasiak, T., 1998. Multivariate comparisons on rocky intertidal macrofaunal assemblages from replicate exploited and non-exploited localities on the Transkei coast of South Africa. Marine Ecology Progress Series. 167, 15-23.
López, C., Poladura, A., Hernández, J.C., Martín, L., Concepción, L. et al., 2012. Contrasting effects of protection from harvesting in populations of two limpet species in a recently established marine protected area. Scientia Marina 76 (4), 799-807. DOI: 10.3989/scimar.03601.15C.
Marra, S., Camedda, A., de Lucia, G.A., Espinosa, F., Coppa, S., 2016. New records about status and distribution of the endangered limpet Patella ferruginea in Sardinia (Italy, W Mediterranean). Aquatic Conservation - Marine And Freshwater Ecosystem. 26 (3), 607-612. DOI: 10.1002/aqc.2615
Marsh, C.P., 1986. Impact of avian predators on high intertidal limpet populations. Journal of Experimental Marine Biology and Ecology. 104 (1-3), 185-201. DOI:10.1016/0022-0981(86)90104-8.
Martins, G.M., Jenkins, S.R., Hawkins, S.J., Neto, A.I., Thompson, R.C., 2008. Exploitation of rocky intertidal grazers: population status and potential impacts on community structure and functioning. Aquatic Biology. 3, 1-10. DOI: 10.3354/ab00072.
Martins, G.M., Jenkins, S.R., Hawkins, S.J., Neto, A.I., Medeiros, A.R. et al., 2011. Illegal harvesting affects the success of fishing closure areas. Journal of the Marine Biological Association of the UK. 91(04), 929-937. DOI: 10.1017/S0025315410001189.
Menge, B.A., 2000. Top-down and bottom-up community regulation in marine rocky intertidal habitats. Journal of Experimental Marine Biology and Ecology. 250, 257-289. DOI: 10.1016/S0022-0981(00)00200-8.
Millennium Ecosystem Assessment, 2005. Ecosystems and Human Well-being: Biodiversity Synthesis. World Resources Institute, Washington, DC. 85pp.
Moreno, C.A., 2001. Community patterns generated by human harvesting on Chilean shores: a review. Aquatic Conservation- Marine And Freshwater Ecosystem. 11, 19-30. DOI: 10.1002/aqc.430.
Navarro, P.G, Ramírez, R., Tuya, F., Fernandez-gil, C., Sanchez-jerez, P. et al., 2005. Hierarchical analysis of spatial distribution patterns of patellid limpets in the Canary islands. Journal of Molluscan. Studies. 71, 67-73. DOI: 10.1093/mollus/eyi009.
Oliva, D., Castilla, J.C., 1986. The Effect of Human Exclusion on the Population Structure of Key-Hole Limpets Fissurella crassa and F. limbata on the Coast of Central Chile. Marine Ecology. 7 (3), 201-217. DOI: 10.1111/j.1439-0485.1986.tb00158.x.
Palomares, M.L.D., Pauly, D. 2017. SeaLifeBase. http://www.sealifebase.org (Version 06/2017).
Paracuellos, M., Nevado, J.C., Moreno, D., Giménez, A., Alesina, J.J., 2003. Conservational status and demographic characteristics of Patella ferruginea Gmelin, 1791 (Mollusca, Gastropoda) on the Alborán Island (Western Mediterranean).
Animal Biodiversity and Conservation. 26 (2), 29-37. Plumeridge, A.A., Roberts, C.M., 2017. Conservation targets in marine protected area management suffer from shifting baseline syndrome: A case study on the Dogger Bank. Marine Pollution Bulletin. DOI: 10.1016/j.marpolbul. 2017.01.012
Pieraccini, M., Coppa, S., de Lucia, G.A., 2017. Beyond marine paper parks? Regulation theory to assess and address environmental non-compliance. Aquatic Conservation - Marine And Freshwater Ecosystem. 27 (1), 177-196. DOI: 10.1002/aqc.2632.
Prusina, I., Peharda, M., Ezgeta-Balić, D., Puljas, S., Glamuzina, B. et al., 2015. Life-history trait of the Mediterranean keystone species Patella rustica: growth and microbial bioerosion. Mediterranean Marine Science. 16: 393-401. DOI: http://dx.doi.org/10.12681/mms.1121.
Rife, A.N., Erisman, B., Sanchez, A., Aburto-Oropeza, O., 2013. When good intentions are not enough… Insights on networks of “paper park” marine protected areas. Conservation Letters. 6 (3), 200-212. DOI:10.1111/j.1755-263X.2012.00303.x
Rilov, G., Benayahu, Y., Gasith, A., 2004. Life on the edge: do biomechanical and behavioral adaptations to wave-exposure correlate with habitat partitioning in predatory whelks? Marine Ecology Progress Series. 282, 193-204. DOI:10.3354/meps282193.
Rilov, G., Gasith, A., Benayahu, Y., 2005. Effect of disturbance on foraging: whelk activity on wave-exposed rocky shores with minimal tidal range. Marine Biology. 147 (2), 421-428. DOI: 10.1007/s00227-005-1568-y.
Sagarin, R.D., Ambrose, R.F., Becker, B.J., Engle, J.M., Kido, J. et al., 2007. Ecological impacts on the limpet Lottia gigantea populations: human pressure over a broad scale on island and mainland intertidal zones. Marine Biology. 150, 399-413. DOI: 10.1007/s00227-006-0341-1.
Silva, A., Boaventura, D., Flores, A., Re, P., Hawkins, S.J., 2004. Rare predation by the intertidal crab Pachygrapsus marmoratus on the limpet Patella depressa. Journal of the Marine Biological Association of the UK. 84 (2), 367-370. DOI: 10.1017/S0025315404009294h.
Silva, A.C.F., Hawkins, S.J., Boaventura, D.M., Thompson, R.C., 2008. Predation by small mobile aquatic predators regulates populations of the intertidal limpet Patella vulgata (L.). Journal of Experimental Marine Biology and Ecology. 367, 259-265. DOI: 10.1016/j.jembe.2008.10.010.
Silva, A.C.F., Hawkins, S.J., Boaventura, D.M., Brewster, E., Thompson, R.C., 2010a. Use of the intertidal zone by mobile predators: influence of wave exposure, tidal phase and elevation on abundance and diet. Marine Ecology Progress Series. 406, 197-210. DOI:10.3354/meps08543.
Silva, A.C., Amador, A.C., Brazão, S., Faria, C., Boaventura, D., 2010b. Limpets as prey: Lipophrys pholis choice for size. Marine Ecology. 31 (4), 525-532. DOI: 10.1111/j.1439-0485.2010.00382.x
Sparre, P., Venema, S.C. 1998. Introduction to tropical fish stock assessment, Part 1. Manual. FAO Fisheries Technical Paper. No. 306.1, Rev. 2. Rome, FAO. 407 pp. Thompson, R.C., Crowe, T.P., Hawkins, S.J., 2002. Rocky intertidal communities: past environmental changes, present status and predictions for the next 25 years. Environmental Conservation. 29 (2), 168-191. DOI: http://dx.doi.org/10.1017/S0376892902000115.
Tlig-Zouari, S., Rabaoui, L., Fguiri, H., Diawara, M., Ben Hassine, O.K., 2010. Spatial diversity of rocky midlittoral macro-invertebrates associated with the endangered species Patella ferruginea (Mollusca: Gastropoda) of Tunisian coastline. Estuarine, Coastal and Shelf. S. 87 (2), 275-283. DOI: 10.1016/j.ecss.2009.12.007.
Weber, L.I., Hawkins, S.J., 2002. Evolution of the limpet Patella candei d’Orbigny (Mollusca, Patellidae) in Atlantic archipelagos: human intervention and natural processes. Biological Journal of the Linnean Society. 77, 341-353. DOI: 10.1046/j.1095-8312.2002.00102.x.
Worm, B., Barbier, E.B., Beaumont, N., Duffy, J. E., Folke, C. et al., 2006. Impacts of Biodiversity Loss on Ocean Ecosystem Services. Science. 314, 787-790. DOI: 10.1126/science.1132294.