Combined effects of fragmentation and herbivory on Posidonia oceanica seagrass ecosystems

Journal of Ecology

Volumn 101, Issue 4, 2013, Pages 1053-1061

  Gera, Alessandro ^a   Pagès, Jordi F ^a   Romero, Javier ^b   Alcoverro, Teresa ^a,c  

^a CENTRE D ESTUDIS AVANÇATS DE BLANES CEAB CSIC   (Spain)

^b UNIVERSITY OF BARCELONA   (Spain)

^c NATURE CONSERVATION FOUNDATION   (India)

Author keywords

Mediterranean; Paracentrotus lividus; Patch selection; Patch size; Plant responses; Plant herbivore interactions; Posidonia oceanica; Sarpa salpa; Seagrass

Indexed keywords

CANOPY ARCHITECTURE; DEFOLIATION; ECOSYSTEM FUNCTION; ECOSYSTEM MANAGEMENT; ENVIRONMENTAL STRESS; HABITAT FRAGMENTATION; HERBIVORY; LIGHT AVAILABILITY; NUTRIENT LIMITATION; PATCH SIZE; PLANT-HERBIVORE INTERACTION; PRIMARY PRODUCTION; SEAGRASS;

PARACENTROTUS LIVIDUS; POSIDONIA OCEANICA; SARPA SALPA;

EID: 84879606453     PISSN: 00220477     EISSN: 13652745     Source Type: Journal    
DOI: 10.1111/1365-2745.12109     Document Type: Article

References (84)

1. Alcoverro, T., Manzanera, M. & Romero, J. (2001) Annual metabolic carbon balance of the seagrass Posidonia oceanica: the importance of carbohydrate reserves. Marine Ecology Progress Series, 211, 105-116.
2. Alcoverro, T., Pagès, J., Gera, A., Farina, S., Roca, G., Pérez, M. & Romero, J. (2012) The effects of 26th December 2008 storm on Costa Brava Posidonia oceanica ecosystems. Assessment of the Ecological Impact of the Extreme Storm of Sant Esteve's Day (26 December 2008) on the Littoral Ecosystems of the North Mediterranean Spanish Coasts (eds M.A. Mateo & T. Garcia-Rubies ), pp. 147-156. Final Report (PIEC 200430E599). Centro de Estudios Avanzados de Blanes, Consejo Superior de Investigaciones Científicas, Blanes.
3. Arponen, H. & Boström, C. (2012) Responses of mobile epifauna to small-scale seagrass patchiness: is fragmentation important? Hydrobiologia, 680, 1-10.
4. Baguette, M. & Van Dyck, H. (2007) Landscape connectivity and animal behavior: functional grain as a key determinant for dispersal. Landscape Ecology, 22, 1117-1129.
5. Belisle, M. (2005) Measuring landscape connectivity: the challenge of behavioral landscape ecology. Ecology, 86, 1988-1995.
6. Bell, S.S., Robbins, B.D. & Jensen, S.L. (1999) Gap dynamics in a seagrass landscape. Ecosystems, 2, 493-504.
7. Borg, J.A., Attrill, M.J., Rowden, A.A., Schembri, P.J. & Jones, M.B. (2005) Architectural characteristics of two bed types of the seagrass Posidonia oceanica over different spatial scales. Estuarine Coastal and Shelf Science, 62, 667-678.
8. Borg, J.A., Rowden, A.A., Attrill, M.J., Schembri, P.J. & Jones, M.B. (2010) Spatial variation in the composition of motile macroinvertebrate assemblages associated with two bed types of the seagrass Posidonia oceanica. Marine Ecology Progress Series, 406, 91-104.
9. Boström, C., Jackson, E.L. & Simenstad, C.A. (2006) Seagrass landscapes and their effects on associated fauna: a review. Estuarine Coastal and Shelf Science, 68, 383-403.
10. Boström, C., Pittman, S., Simenstad, C. & Kneib, R. (2011) Seascape ecology of coastal biogenic habitats: Advances, gaps, and challenges. Marine Ecology Progress Series, 427, 191-217.
11. Boudouresque, C.F. & Meinesz, A. (1982) Découverte de l'herbier de Posidonies, p. 89. Parc National de Port-Cros et par le Parc Naturel Régional de la Corse, Marseille.
12. Boudouresque, C.F. & Verlaque, M. (2001) Ecology of Paracentrotus lividus. Edible Sea Urchins: Biology and Ecology (ed. J.M. Lawrence ), pp. 177-216. Elsevier, Amsterdam.
13. Brook, B.W., Sodhi, N.S. & Bradshaw, C.J.A. (2008) Synergies among extinction drivers under global change. Trends in Ecology & Evolution, 23, 453-460.
14. Burke, M.K., Dennison, W.C. & Moore, K.A. (1996) Non-structural carbohydrate reserves of eelgrass Zostera marina. Marine Ecology Progress Series, 137, 195-201.
15. Cebrián, J., Duarte, C., Marbá, N., Enríquez, S., Gallegos, M. & Olesen, B. (1996) Herbivory on Posidonia oceanica: magnitude and variability in the Spanish Mediterranean. Marine Ecology Progress Series, 130, 147-155.
16. Christianen, M.J.A., Govers, L.L., Bouma, T.J., Kiswara, W., Roelofs, J.G.M., Lamers, L.P.M. & van Katwijk, M.M. (2012) Marine megaherbivore grazing may increase seagrass tolerance to high nutrient loads. Journal of Ecology, 100, 546-560.
17. Crain, C.M., Kroeker, K. & Halpern, B.S. (2008) Interactive and cumulative effects of multiple human stressors in marine systems. Ecology Letters, 11, 1304-1315.
18. Darling, E.S. & Côté, I.M. (2008) Quantifying the evidence for ecological synergies. Ecology Letters, 11, 1278-1286.
19. Diaz-Almela, E., Marbà, N., Álvarez, E., Santiago, R., Martínez, R. & Duarte, C.M. (2008) Patch dynamics of the Mediterranean seagrass Posidonia oceanica: implications for recolonisation process. Aquatic Botany, 89, 397-403.
20. Didham, R.K., Tylianakis, J.M., Gemmell, N.J., Rand, T.A. & Ewers, R.M. (2007) Interactive effects of habitat modification and species invasion on native species decline. Trends in Ecology & Evolution, 22, 489-496.
21. Duarte, C.M. (1990) Seagrass nutrient content. Marine Ecology Progress Series, 67, 201-207.
22. Duarte, C.M. (2002) The future of seagrass meadows. Environmental Conservation, 29, 192-206.
23. Duarte, C.M. & Sand-Jensen, K. (1990) Seagrass colonization-biomass development and shoot demography in Cymodocea nodosa patches. Marine Ecology Progress Series, 67, 97-103.
24. Eggleston, D.B., Elis, W.E., Etherington, L.L., Dahlgren, C.P. & Posey, M.H. (1999) Organism responses to habitat fragmentation and diversity: habitat colonization by estuarine macrofauna. Journal of Experimental Marine Biology and Ecology, 236, 107-132.
25. Emlen, J.M. (1966) Natural selection and human behavior. Journal of Theoretical Biology, 12, 410-418.
26. Fáveri, S.B., Vasconcelos, H.L. & Dirzo, R. (2008) Effects of Amazonian forest fragmentation on the interaction between plants, insect herbivores, and their natural enemies. Journal of Tropical Ecology, 24, 57-64.
27. Folke, C., Carpenter, S., Walker, B., Scheffer, M., Elmqvist, T., Gunderson, L. & Holling, C.S. (2004) Regime shifts, resilience and biodiversity in ecosystem management. Annual Review of Ecology, Evolution and Systematics, 35, 557-581.
28. Frederiksen, M., Krause-Jensen, D., Holmer, M. & Laursen, J.S. (2004) Spatial and temporal variation in eelgrass (Zostera marina) landscapes: influence of physical setting. Aquatic Botany, 78, 147-165.
29. Frost, M.T., Rowden, A.A. & Attrill, M.J. (1999) Effect of habitat fragmentation on the macroinvertebrate infaunal communities associated with the seagrass Zostera marina L. Aquatic Conservation: Marine and Freshwater Ecosystems, 9, 255-263.
30. Graham, N.A.J., Chabanet, P., Evans, R.D., Jennings, S., Letourneur, Y., Aaron MacNeil, M., McClanahan, T.R., Öhman, M.C., Polunin, N.V.C. & Wilson, S.K. (2011) Extinction vulnerability of coral reef fishes. Ecology Letters, 14, 341-348.
31. Halpern, B.S., McLeod, K.L., Rosenberg, A.A. & Crowder, L.B. (2008) Managing for cumulative impacts in ecosystem-based management through ocean zoning. Ocean and Coastal Management, 51, 203-211.
32. Hambäck, P.A., Summerville, K.S., Steffan-Dewenter, I., Krauss, J., Englund, G. & Crist, T.O. (2007) Habitat specialization, body size, and family identity explain lepidopteran density-area relationships in a cross-continental comparison. Proceedings of the National Academy of Sciences of the United States of America, 104, 8368-8373.
33. Hamilton, J.G., Zangerl, A.R., DeLucia, E.H. & Berenbaum, M.R. (2001) The carbon-nutrient balance hypothesis: its rise and fall. Ecology Letters, 4, 86-95.
34. Haynes, K.J. & Crist, T.O. (2009) Insect herbivory in an experimental agroecosystem: the relative importance of habitat area, fragmentation, and the matrix. Oikos, 118, 1477-1486.
35. Heck, J.K.L. & Valentine, J.F. (2006) Plant-herbivore interactions in seagrass meadows. Journal of Experimental Marine Biology and Ecology, 330, 420-436.
36. Hemminga, M. & Duarte, C. (2000) Seagrass Ecology, 297 pp. Cambridge University Press, Cambridge.
37. Hemminga, M.A., Harrison, P.G. & Van Lent, F. (1991) The balance of nutrient losses and gains in seagrass meadows. Marine Ecology Progress Series, 71, 85-96.
38. Hirst, J.A. & Attrill, M.J. (2008) Small is beautiful: an inverted view of habitat fragmentation in seagrass beds. Estuarine Coastal and Shelf Science, 78, 811-818.
39. Hovel, K.A. & Lipcius, R.N. (2001) Habitat fragmentation in a seagrass landscape: patch size and complexity control blue crab survival. Ecology, 82, 1814-1829.
40. Hughes, T.P., Bellwood, D.R., Folke, C., Steneck, R.S. & Wilson, J. (2005) New paradigms for supporting the resilience of marine ecosystems. Trends in Ecology & Evolution, 20, 380-386.
41. Invers, O., Kraemer, G.P., Pérez, M. & Romero, J. (2004) Effects of nitrogen addition on nitrogen metabolism and carbon reserves in the temperate seagrass Posidonia oceanica. Journal of Experimental Marine Biology and Ecology, 303, 97-114.
42. Johnson, M.W. & Heck, K.L. (2006) Effects of habitat fragmentation per se on decapods and fishes inhabiting seagrass meadows in the northern Gulf of Mexico. Marine Ecology Progress Series, 306, 233-246.
43. Kéry, M., Matthies, D. & Fischer, M. (2001) The effect of plant population size on the interactions between the rare plant Gentiana cruciata and its specialized herbivore Maculinea rebeli. Journal of Ecology, 89, 418-427.
44. Kohn, D.D. & Walsh, D.M. (1994) Plant species richness-the effect of island size and habitat diversity. Journal of Ecology, 82, 367-377.
45. Kolb, A. (2008) Habitat fragmentation reduces plant fitness by disturbing pollination and modifying response to herbivory. Biological Conservation, 141, 2540-2549.
46. Kunin, W.E. (1997) Population size and density effects in pollination: pollinator foraging and plant reproductive success in experimental arrays of Brassica kaber. Journal of Ecology, 85, 225-234.
47. Lienert, J. (2004) Habitat fragmentation effects on fitness of plant populations - a review. Journal for Nature Conservation, 12, 53-72.
48. Lienert, J., Diemer, M. & Schmid, B. (2002) Effects of habitat fragmentation on population structure and fitness components of the wetland specialist Swertia perennis L. (Gentianaceae). Basic and Applied Ecology, 3, 101-114.
49. Lienert, J. & Fischer, M. (2003) Habitat fragmentation affects the common wetland specialist Primula farinosa in north-east Switzerland. Journal of Ecology, 91, 587-599.
50. MacArthur, R.H. & Pianka, E.R. (1966) On the optimal use of a patchy environment. Science, 186, 645-647.
51. Mills, V.S. & Berkenbusch, K. (2009) Seagrass (Zostera muelleri) patch size and spatial location influence infaunal macroinvertebrate assemblages. Estuarine Coastal and Shelf Science, 81, 123-129.
52. Pagès, J.F., Farina, S., Gera, A., Arthur, R., Romero, J. & Alcoverro, T. (2012) Indirect interactions in seagrasses: fish herbivores increase predation risk to sea urchins by modifying plant traits. Functional Ecology, 26, 1015-1023.
53. Planes, S., Raventos, N., Ferrari, B. & Alcoverro, T. (2011) Fish herbivory leads to shifts in seagrass Posidonia oceanica investments in sexual reproduction. Marine Ecology Progress Series, 431, 205-213.
54. Prado, P., Alcoverro, T. & Romero, J. (2010) Influence of nutrients in the feeding ecology of seagrass (Posidonia oceanica L.) consumers: a stable isotopes approach. Marine Biology, 157, 715-724.
55. Prado, P., Collier, C.J. & Lavery, P.S. (2008a) 13C and 15N translocation within and among shoots in two Posidonia species from Western Australia. Marine Ecology Progress Series, 361, 69-82.
56. Prado, P., Farina, S., Tomas, F., Romero, J. & Alcoverro, T. (2008b) Marine protection and meadow size alter fish herbivory in seagrass ecosystems. Marine Ecology Progress Series, 371, 11-21.
57. Prado, P., Tomas, F., Alcoverro, T. & Romero, J. (2007) Extensive direct measurements of Posidonia oceanica defoliation confirm the importance of herbivory in temperate seagrass meadows. Marine Ecology Progress Series, 340, 63-71.
58. R Development Core Team (2010) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. Available at: http://www.R-project.org.
59. Ramage, D.L. & Schiel, D.R. (1999) Patch dynamics and response to disturbance of the seagrass Zostera novazelandica on intertidal platforms in southern New Zealand. Marine Ecology Progress Series, 189, 275-288.
60. Raventos, N., Ferrari, B. & Planes, S. (2009) Differences in population parameters and behaviour of the herbivorous fish Sarpa salpa between protected and unprotected seagrass meadows in the north-western Mediterranean. Journal of the Marine Biological Association of the United Kingdom, 89, 1153-1159.
61. Reed, B.J. & Hovel, K.A. (2006) Seagrass habitat disturbance: how loss and fragmentation of eelgrass Zostera marina influences epifaunal abundance and diversity. Marine Ecology Progress Series, 326, 133-143.
62. Ruiz-Guerra, B., Guevara, R., Mariano, N.A. & Dirzo, R. (2010) Insect herbivory declines with forest fragmentation and covaries with plant regeneration mode: evidence from a Mexican tropical rain forest. Oikos, 119, 317-325.
63. Sala, O.E., Chapin, F.S., Armesto, J.J., Berlow, E., Bloomfield, J., Dirzo, R. et al. (2000) Global biodiversity scenarios for the year 2100. Science, 287, 1770-1774.
64. Short, F.T. & Duarte, C.M. (2001) Chapter 8 - Methods for the measurement of seagrass growth and production. Global Seagrass Research Methods (eds T.S. Frederick, A.S. Catherine & G.C. Robert ), pp. 155-182. Elsevier Science, Amsterdam.
65. Simonetti, J.A., Grez, A.A., Celis-Diez, J.L. & Bustamante, R.O. (2007) Herbivory and seedling performance in a fragmented temperate forest of Chile. Acta Oecologica, 32, 312-318.
66. Sleeman, J.C., Kendrick, G.A., Boggs, G.S. & Hegge, B.J. (2005) Measuring fragmentation of seagrass landscapes: which indices are most appropriate for detecting change? Marine and Freshwater Research, 56, 851-864.
67. Stoll, P., Dolt, C., Goverde, M. & Baur, B. (2006) Experimental habitat fragmentation and invertebrate grazing in a herbaceous grassland species. Basic and Applied Ecology, 7, 307-319.
68. Terborgh, J., Feeley, K., Silman, M., Nuñez, P. & Balukjian, B. (2006) Vegetation dynamics of predator-free land-bridge islands. Journal of Ecology, 94, 253-263.
69. Thrush, S.F., Halliday, J., Hewitt, J.E. & Lohrer, A.M. (2008) The effects of habitat loss, fragmentation, and community homogenization on resilience in estuaries. Ecological Applications, 18, 12-21.
70. Underwood, A.J. (1981) Techniques of analysis of variance in experimental marine biology and ecology. Oceanography and Marine Biology: An Annual Review, 19, 513-605.
71. Unsworth, R.K.F., Taylor, J.D., Powell, A., Bell, J.J. & Smith, D.J. (2007) The contribution of scarid herbivory to seagrass ecosystem dynamics in the Indo-Pacific. Estuarine Coastal and Shelf Science, 74, 53-62.
72. del-Val, E., Armesto, J., Barbosa, O. & Marquet, P. (2007) Effects of herbivory and patch size on tree seedling survivorship in a fog-dependent coastal rainforest in semiarid Chile. Oecologia, 153, 625-632.
73. Valentine, J.F. & Heck, K.L. Jr (1999) Seagrass herbivory: evidence for the continued grazing of marine grasses. Marine Ecology Progress Series, 176, 291-302.
74. Valentine, J.F. & Heck, K.L. Jr (2001) The role of leaf nitrogen content in determining turtlegrass (Thalassia testudinum) grazing by a generalized herbivore in the northeastern Gulf of Mexico. Journal of Experimental Marine Biology and Ecology, 258, 65-86.
75. Valentine, J.F., Heck, K.L., Busby, J. Jr & Webb, D. (1997) Experimental evidence that herbivory increases shoot density and productivity in a subtropical turtlegrass (Thalassia testudinum) meadow. Oecologia, 112, 193-200.
76. Vásquez, P.A., Grez, A.A., Bustamante, R.O. & Simonetti, J.A. (2007) Herbivory, foliar survival and shoot growth in fragmented populations of Aristotelia chilensis. Acta Oecologica, 31, 48-53.
77. Veblen, K.E. (2012) Savanna glade hotspots: plant community development and synergy with large herbivores. Journal of Arid Environments, 78, 119-127.
78. Veblen, K.E. & Young, T.P. (2010) Contrasting effects of cattle and wildlife on the vegetation development of a savanna landscape mosaic. Journal of Ecology, 98, 993-1001.
79. Vega Fernández, T., Milazzo, M., Badalamenti, F. & D'Anna, G. (2005) Comparison of the fish assemblages associated with Posidonia oceanica after the partial loss and consequent fragmentation of the meadow. Estuarine Coastal and Shelf Science, 65, 645-653.
80. Vergés, A., Pérez, M., Alcoverro, T. & Romero, J. (2008) Compensation and resistance to herbivory in seagrasses: induced responses to simulated consumption by fish. Oecologia, 155, 751-760.
81. Vidondo, B., Duarte, C.M., Middelboe, A.L., Stefansen, K., Lützen, T. & Nielsen, S.L. (1997) Dynamics of a landscape mosaic: size and age distributions, growth and demography of seagrass Cymodocea nodosa patches. Marine Ecology Progress Series, 158, 131-138.
82. Villafuerte, R., Litvaitis, J.A. & Smith, D.F. (1997) Physiological responses by lagomorphs to resource limitations imposed by habitat fragmentation: implications for condition-sensitive predation. Canadian Journal of Zoology, 75, 148-151.
83. White, K.S., Westera, M.B. & Kendrick, G.A. (2011) Spatial patterns in fish herbivory in a temperate Australian seagrass meadow. Estuarine Coastal and Shelf Science, 93, 366-374.
84. Zieman, J.C. (1974) Methods for the study of the growth and production of turtle grass, Thalassia testudinum König. Aquaculture, 4, 139-143.