Protection enhances community and habitat stability: Evidence from a Mediterranean marine protected area

PLoS ONE

Volumn 8, Issue 12, 2013, Pages

  Fraschetti, Simonetta ^a   Guarnieri, Giuseppe ^a   Bevilacqua, Stanislao ^a   Terlizzi, Antonio ^a   Boero, Ferdinando ^a,b  

^a UNIVERSITY OF SALENTO   (Italy)

^b CNR   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; ENVIRONMENTAL MANAGEMENT; ENVIRONMENTAL PROTECTION; INVERTEBRATE; LITTORAL; MACROALGA; MACROBENTHOS; MARINE ENVIRONMENT; MEDITERRANEAN SEA; MIDLITTORAL ROCK; NONHUMAN; ORGANISM COMMUNITY; POSIDONIA OCEANICA; SEAGRASS; SPECIES DISTRIBUTION; SPECIES HABITAT;

ANIMALS; CHLOROPHYTA; CONSERVATION OF NATURAL RESOURCES; ECOSYSTEM; ENVIRONMENTAL MONITORING; GEOLOGIC SEDIMENTS; HUMANS; INVERTEBRATES; ITALY; MARINE BIOLOGY; MODELS, STATISTICAL; POPULATION DYNAMICS; RHODOPHYTA; SPATIO-TEMPORAL ANALYSIS;

EID: 84892593256     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0081838     Document Type: Article

References (88)

1. Hooper DU, Adair EC, Cardinale BJ, Byrnes JEK, Hungate BA, et al. (2012) A global synthesis reveals biodiversity loss as a major driver of ecosystem change. Nature 486: 105-U129.
2. Cardinale BJ, Duffy JE, Gonzalez A, Hooper DU, Perrings C, et al. (2012) Biodiversity loss and its impact on humanity. Nature 486: 59-67.
3. Worm B, Barbier EB, Beaumont N, Duffy JE, Folke C, et al. (2006) Impacts of biodiversity loss on ocean ecosystem services. Science 314: 787-790.
4. Hooper DU, Chapin FS, Ewel JJ, Hector A, Inchausti P, et al. (2005) Effects of biodiversity on ecosystem functioning: A consensus of current knowledge. Ecol Monogr 75: 3-35.
5. Srivastava DS, Vellend M (2005) Biodiversity-ecosystem function research: Is it relevant to conservation? Annu Rev Ecol Evol Syst. 267-294.
6. Schwartz MW, Brigham CA, Hoeksema JD, Lyons KG, Mills MH, et al. (2000) Linking biodiversity to ecosystem function: implications for conservation ecology. Oecologia 122: 297-305.
7. Warwick RM, Clarke KR (1993) Increased variability as a symptom of stress in marine communities. J Exp Mar Biol Ecol 172: 215-226.
8. Hsieh CH, Reiss CS, Hunter JR, Beddington JR, May RM, et al. (2006) Fishing elevates variability in the abundance of exploited species. Nature 443: 859-862.
9. deYoung B, Barange M, Beaugrand G, Harris R, Perry RI, et al. (2008) Regime shifts in marine ecosystems: detection, prediction and management. Trends Ecol Evol 23: 402-409.
10. Hewitt JE, Thrush SF (2009) Do Species' abundances become more spatially variable with stress? Open Ecol J 2: 37-46.
11. Folke C, Carpenter S, Walker B, Scheffer M, Elmqvist T, et al. (2004) Regime shifts, resilience, and biodiversity in ecosystem management. Annu Rev Ecol Evol Syst 35: 557-581.
12. Scheffer M, Carpenter SR, Lenton TM, Bascompte J, Brock W, et al. (2012) Anticipating Critical Transitions. Science 338: 344-348.
13. Fraterrigo JM, Rusak JA (2008) Disturbance-driven changes in the variability of ecological patterns and processes. Ecol Lett 11: 756-770.
14. Hewitt J, Thrush S, Lohrer A, Townsend M (2010) A latent threat to biodiversity: consequences of small-scale heterogeneity loss. Biodivers Conserv 19: 1315-1323.
15. Carpenter SR, Cole JJ, Pace ML, Batt R, Brock WA, et al. (2011) Early Warnings of Regime Shifts: A Whole-Ecosystem Experiment. Science 332: 1079-1082.
16. Hughes TP, Baird AH, Bellwood DR, Card M, Connolly SR, et al. (2003) Climate change, human impacts, and the resilience of coral reefs. Science 301: 929-933.
17. Mumby PJ, Dahlgren CP, Harborne AR, Kappel CV, Micheli F, et al. (2006) Fishing, trophic cascades, and the process of grazing on coral reefs. Science 311: 98-101.
18. Hoey AS, Pratchett MS, Cvitanovic C (2011) High Macroalgal Cover and Low Coral Recruitment Undermines the Potential Resilience of the World's Southernmost Coral Reef Assemblages. Plos One 6.
19. Gorman D, Connell SD (2009) Recovering subtidal forests in human-dominated landscapes. J Appl Ecol 46: 1258-1265.
20. Petraitis PS, Methratta ET, Rhile EC, Vidargas NA, Dudgeon SR (2009) Experimental confirmation of multiple community states in a marine ecosystem. Oecologia 161: 139-148.
21. Perkol-Finkel S, Airoldi L (2010) Loss and Recovery Potential of Marine Habitats: An Experimental Study of Factors Maintaining Resilience in Subtidal Algal Forests at the Adriatic Sea. Plos One 5.
22. Sala E, Kizilkaya Z, Yildirim D, Ballesteros E (2011) Alien Marine Fishes Deplete Algal Biomass in the Eastern Mediterranean. Plos One 6.
23. Boero F, Bonsdorff E (2007) A conceptual framework for marine biodiversity and ecosystem functioning. Mar Ecol-Evol Persp 28: 134-145.
24. Fauchald P (2010) Predator-prey reversal: A possible mechanism for ecosystem hysteresis in the North Sea? Ecology 91: 2191-2197.
25. Bellwood DR, Hughes TP, Folke C, Nystrom M (2004) Confronting the coral reef crisis. Nature 429: 827-833.
26. Hughes TP, Bellwood DR, Folke C, Steneck RS, Wilson J (2005) New paradigms for supporting the resilience of marine ecosystems. Trends Ecol Evol 20: 380-386.
27. Allison GW, Lubchenco J, Carr MH (1998) Marine reserves are necessary but not sufficient for marine conservation. Ecol Appl 8: S79-S92.
28. Halpern BS, Lester SE, McLeod KL (2010) Placing marine protected areas onto the ecosystem-based management seascape. P Natl Acad Sci USA 107: 18312-18317.
29. Fraschetti S, Claudet J, Grorud-Colvert K (2011) Transitioning from single-sector management to ecosystem-based management: What can marine protected areas offer? In Claudet J (ed.) Marine Protected Areas - A multidisciplinary approach. Cambridge University Press. 11-34.
30. Linares C, Garrabou J, Hereu B, Diaz D, Marschal C, et al. (2012) Assessing the Effectiveness of Marine Reserves on Unsustainably Harvested Long-Lived Sessile Invertebrates. Conserv Biol 26: 88-96.
31. Goñi R, Quetglas A, Reñones O (2006) Spillover of spiny lobsters Palinurus elephas from a marine reserve to an adjoining fishery. Mar Ecol-Prog Ser 308: 207-219.
32. Guidetti P (2006) Potential of marine reserves to cause community-wide changes beyond their boundaries. Conserv Biol 21: 540-545.
33. Lester SE, Halpern BS, Grorud-Colvert K, Lubchenco J, Ruttenberg BI, et al. (2009) Biological effects within no-take marine reserves: a global synthesis. Mar Ecol-Prog Ser 384: 33-46.
34. Sala E, Ballesteros E, Dendrinos P, Di Franco A, Ferretti F, et al. (2012) The Structure of Mediterranean Rocky Reef Ecosystems across Environmental and Human Gradients, and Conservation Implications. Plos One 7.
35. Garcia-Charton JA, Perez-Ruzafa A, Marcos C, Claudet J, Badalamenti F, et al. (2008) Effectiveness of European Atlanto-Mediterranean MPAs: Do they accomplish the expected effects on populations, communities and ecosystems? J Nat Conserv 16: 193-221.
36. Pauly D, Christensen V, Guenette S, Pitcher TJ, Sumaila UR, et al. (2002) Towards sustainability in world fisheries. Nature 418: 689-695.
37. Francour P (1994) Pluriannual analysis of the reserve effect on ichthyofauna in the Scandola Natural Reserve (Corsica, Northwestern Mediterranean). Oceanol Acta 17: 309-317.
38. Hughes TP, Graham NAJ, Jackson JBC, Mumby PJ, Steneck RS (2010) Rising to the challenge of sustaining coral reef resilience. Trends Ecol Evol 25: 633-642.
39. Mumby PJ, Harborne AR (2010) Marine Reserves Enhance the Recovery of Corals on Caribbean Reefs. Plos One 5.
40. Micheli F, Saenz-Arroyo A, Greenley A, Vazquez L, Montes JAE, et al. (2012) Evidence That Marine Reserves Enhance Resilience to Climatic Impacts. Plos One 7.
41. Babcock RC, Shears NT, Alcala AC, Barrett NS, Edgar GJ, et al. (2010) Decadal trends in marine reserves reveal differential rates of change in direct and indirect effects. P Natl Acad Sci USA 107: 18256-18261.
42. Hereu B, Linares C, Sala E, Garrabou J, Garcia-Rubies A, et al. (2012) Multiple Processes Regulate Long-Term Population Dynamics of Sea Urchins on Mediterranean Rocky Reefs. Plos One 7.
43. Bevilacqua S, Terlizzi A, Fraschetti S, Russo GF, Boero F (2006) Mitigating human disturbance: can protection influence trajectories of recovery in benthic assemblages? J Anim Ecol 75: 908-920.
44. Navarrete SA, Gelcich S, Castilla JC (2010) Long-term monitoring of coastal ecosystems at Las Cruces, Chile: Defining baselines to build ecological literacy in a world of change. Rev Chil Hist Nat 83: 143-157.
45. Claudet J, Fraschetti S (2010) Human-driven impacts on marine habitats: A regional meta-analysis in the Mediterranean Sea. Biological Conservation 143: 2195-2206.
46. Guidetti P (2006) Marine reserves reestablish lost predatory interactions and cause community changes in rocky reefs. Ecol Appl 16: 963-976.
47. Boudouresque CF, Bernard G, Pergent G, Shili A, Verlaque M (2009) Regression of Mediterranean seagrasses caused by natural processes and anthropogenic disturbances and stress: a critical review. Bot Mar 52: 395-418.
48. Guidetti P, Milazzo M, Bussotti S, Molinari A, Murenu M, et al. (2008) Italian marine reserve effectiveness: Does enforcement matter? Biol Conserv 141: 699-709.
49. Claudet J, Guidetti P (2010) Improving assessments of marine protected areas. Aquat Conserv-Mar Freshw Ecosyst 20: 239-242.
50. Fraschetti S, Terlizzi A, Bussotti S, Guarnieri G, D'Ambrosio P, et al. (2005) Conservation of Mediterranean seascapes: analyses of existing protection schemes. Mar Environ Res 59: 309-332.
51. Dethier MN, Graham ES, Cohen S, Tear LM (1993) Visual versus randompoint percent cover estimations - Objective is not always better. Mar Ecol-Prog Ser 96: 93-100.
52. Steneck RS, Dethier MN (1994) A functional-group approach to the structure of algal-dominated communities. Oikos 69: 476-498.
53. Coleman RA, Underwood AJ, Benedetti-Cecchi L, Aberg P, Arenas F, et al. (2006) A continental scale evaluation of the role of limpet grazing on rocky shores. Oecologia 147: 556-564.
54. Pergent G, Pergent-Martini C, Boudouresque CF (1995) Utilisation de l'herbier à Posidonia oceanica comme indicateur biologique de la qualité du milieu littoral en Méditerranée: Etat des connaissances. Mésogée 54: 3-29.
55. Anderson MJ (2001) Permutation tests for univariate or multivariate analysis of variance and regression. Can J Fish Aquat Sci 58: 626-639.
56. Anderson MJ, Gorley RN, Clarke KR (2008) PERMANOVA+ for PRIMER: guide to software and statistical methods. PRIMER-E, Plymouth, UK: 214 p.
57. Anderson MJ, Willis TJ (2003) Canonical analysis of principal coordinates: A useful method of constrained ordination for ecology. Ecology 84: 511-525.
58. Anderson MJ, Robinson J (2003) Generalized discriminant analysis based on distances. Aust NZ J Stat 45: 301-318.
59. Gaston KJ, McArdle BH (1994) The temporal variability of animal abundances - measures, methods and patterns. Philos Trans R Soc Lond Ser B-Biol Sci 345: 335-358.
60. Fraschetti S, Terlizzi A, Bevilacqua S, Boero F (2006) The distribution of hydroids (Cnidaria, Hydrozoa) from micro- to macro-scale: Spatial patterns on habitat-forming algae. J Exp Mar Biol Ecol 339: 148-158.
61. Coll M, Piroddi C, Albouy C, Lasram FB, Cheung WWL, et al. (2012) The Mediterranean Sea under siege: spatial overlap between marine biodiversity, cumulative threats and marine reserves. Global Ecol Biogeogr 21: 465-480.
62. Polley HW, Wilsey BJ, Derner JD (2007) Dominant species constrain effects of species diversity on temporal variability in biomass production of tallgrass prairie. Oikos 116: 2044-2052.
63. Grman E, Lau JA, Schoolmaster DR, Gross KL (2010) Mechanisms contributing to stability in ecosystem function depend on the environmental context. Ecol Lett 13: 1400-1410.
64. Bulleri F, Alestra T, Ceccherelli G, Tamburello L, Pinna S, et al. (2011) Determinants of Caulerpa racemosa distribution in the north-western Mediterranean. Mar Ecol-Prog Ser 431: 55-67.
65. Valdivia N, Gollety C, Migne A, Davoult D, Molis M (2012) Stressed but Stable: Canopy Loss Decreased Species Synchrony and Metabolic Variability in an Intertidal Hard-Bottom Community. Plos One 7.
66. Milazzo M, Chemello R, Badalamenti F, Camarda R, Riggio S (2002) The Impact of Human Recreational Activities in Marine Protected Areas: What Lessons Should Be Learnt in the Mediterranean Sea? Mar Ecol 23: 280-290.
67. Hughes TP, Bellwood DR, Folke CS, McCook LJ, Pandolfi JM (2007) No-take areas, herbivory and coral reef resilience. Trends Ecol Evol 22: 1-3.
68. Bevilacqua S, Plicanti A, Sandulli R, Terlizzi A (2012) Measuring more of beta-diversity: Quantifying patterns of variation in assemblage heterogeneity. An insight from marine benthic assemblages. Ecol Indic 18: 140-148.
69. Fraschetti S, Bevilacqua S, Guarnieri G, Terlizzi A (2012) Idiosyncratic effects of protection in a remote marine reserve. Mar Ecol-Prog Ser 466: 21-U41.
70. Guarnieri G, Terlizzi A, Bevilacqua S, Fraschetti S (2012) Increasing heterogeneity of sensitive assemblages as a consequence of human impact in submarine caves. Mar Biol 159: 1155-1164.
71. O'Sullivan D, Emmerson M (2011) Marine reserve designation, trophic cascades and altered community dynamics. Mar Ecol-Prog Ser 440: 115-U128.
72. Ceccherelli G, Casu D, Pala D, Pinna S, Sechi N (2006) Evaluating the effects of protection on two benthic habitats at Tavolara-Punta Coda Cavallo MPA (North-East Sardinia, Italy). Mar Environ Res 61: 171-185.
73. Bertocci I, Dominguez R, Freitas C, Sousa-Pinto I (2012) Patterns of variation of intertidal species of commercial interest in the Parque Litoral Norte (north Portugal) MPA: Comparison with three reference shores. Mar Environ Res 77: 60-70.
74. Shears NT, Kushner DJ, Katz SL, Gaines SD (2012) Reconciling conflict between the direct and indirect effects of marine reserve protection. Environ Conserv 39: 225-236.
75. Guarnieri G, Terlizzi A, Bevilacqua S, Fraschetti S (2009) Local vs regional effects of substratum on early colonization stages of sessile assemblages. Biofouling 25: 593-604.
76. Badalamenti F, Carlo G, D'Anna G, Gristina M, Toccaceli M (2006) Effects of dredging activities on population dynamics of Posidonia oceanica (L.) Delile in the Mediterranean sea: The case study of Capo Feto (SW Sicily, Italy). Hydrobiologia 555: 253-261.
77. Gonzalez-Correa JM, Torquemada YF, Lizaso JLS (2008) Long-term effect of beach replenishment on natural recovery of shallow Posidonia oceanica meadows. Estuar Coast Shelf S 76: 834-844.
78. Montefalcone M, Albertelli G, Morri C, Parravicini V, Bianchi CN (2009) Legal protection is not enough: Posidonia oceanica meadows in marine protected areas are not healthier than those in unprotected areas of the northwest Mediterranean Sea. Mar Pollut Bull 58: 515-519.
79. Montefalcone M, Albertelli G, Morri C, Bianchi CN (2007) Urban seagrass: Status of Posidonia oceanica facing the Genoa city waterfront (Italy) and implications for management. Mar Pollut Bull 54: 206-213.
80. Dominguez M, Celdran D, Munoz-Vera A, Infantes E, Martinez-Banos P, et al. (2012) Experimental Evaluation of the Restoration Capacity of a Fish-Farm Impacted Area with Posidonia oceanica (L.) Delile Seedlings. Restor Ecol 20: 180-187.
81. Hereu B, Mangialajo L, Ballesteros E, Thibaut T (2008) On the occurrence, structure and distribution of deep-water Cystoseira (Phaeophyceae) populations in the Port-Cros National Park (north-western Mediterranean). Eur J Phycol 43: 263-273.
82. Hereu B, Zabala M, Sala E (2008) Multiple controls of community structure and dynamics in a sublittoral marine environment. Ecology 89: 3423-3435.
83. Sales M, Cebrian E, Tomas F, Ballesteros E (2011) Pollution impacts and recovery potential in three species of the genus Cystoseira (Fucales, Heterokontophyta). Estuar Coast Shelf S 92: 347-357.
84. Bellan G, Bourcier M, Salen-Picard C, Arnoux A, Casserley S (1999) Benthic ecosystem changes associated with wastewater treatment at Marseille: Implications for the protection and restoration of the Mediterranean coastal shelf ecosystems. Water Environ Res 71: 483-493.
85. Aguado-Gimenez F, Piedecausa MA, Gutierrez JM, Garcia-Charton JA, Belmonte A, et al. (2012) Benthic recovery after fish farming cessation: A ''beyond-BACI'' approach. Mar Pollut Bull 64: 729-738.
86. Bustamante M, Bevilacqua S, Tajadura J, Terlizzi A, Saiz-Salinas JI (2012) Detecting human mitigation intervention: Effects of sewage treatment upgrade on rocky macrofaunal assemblages. Mar Environ Res 80: 27-37.
87. Boero F (1994) Fluctuations and variations in coastal marine environments. Mar Ecol 15: 3-25.
88. Halpern BS, White C, Lester SE, Costello C, Gaines SD (2011) Using portfolio theory to assess tradeoffs between return from natural capital and social equity across space. Biol Conserv 144: 1499-1507.