Benthic community responses to macroalgae invasions in seagrass beds: Diversity, isotopic niche and food web structure at community level

Estuarine, Coastal and Shelf Science

Volumn 142, Issue , 2014, Pages 12-22

  Deudero, S ^a   Box, A ^b   Vazquez Luis M ^a   Arroyo, N L ^c  

^a Centro Oceanográfico de Baleares   (Spain)

^b UNIVERSITAT DE LES ILLES BALEARS   (Spain)

^c Menntun Consultoría Científica SL ^*  (Spain)

Author keywords

Benthic; Caulerpa; Invasive; Stable isotopes

Indexed keywords

ADAPTATION; BENTHOS; BIOLOGICAL INVASION; COMMUNITY RESPONSE; FOOD WEB; HABITAT TYPE; INVASIVE SPECIES; MACROALGA; MEADOW; NATIVE SPECIES; NICHE; NITROGEN ISOTOPE; PHYSIOLOGICAL RESPONSE; SEAGRASS; SPECIES DIVERSITY; TAXONOMY; TROPHIC LEVEL;

EID: 84897086133     PISSN: 02727714     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ecss.2014.03.006     Document Type: Article

References (65)

1. Aizen M., Morales C.M., Morales J.M. Invasive mutualists erode native pollination webs. Public Libr. Sci. Biol. 2008, 6:396-403.
2. Anderson M.J. PERMDISP: a FORTRAN Computer Program for Permutational Analysis of Multivariate Dispersions (For Any Two-factor ANOVA Design) Using Permutation Tests 2004, 24. Department of Statistics, University of Auckland, New Zealand.
3. Bartomeus I., Vilà M., Santamaría L. Contrasting effects of invasive plants in plant-pollinator networks. Oecologia 2008, 155:761-770.
4. Behringer D.C., Butler M.J. Stable isotope analysis of production and trophic relationships in a tropical marine hard-bottom community. Oecologia 2006, 148:334-341.
5. Bevilacqua S., Fraschetti S., Terlizzi A., Boero F. The use of taxonomic distinctness in assessing patterns of biodiversity in modular organisms. Mar. Ecol. 2009, 3:151-163.
6. Bishop M.J., Coleman M.A., Kelaher B.P. Cross-habitat impacts of species decline: response of estuarine sediment communities to changing detrital resources. Oecologia 2010, 163:517-525.
7. Boudouresque C.F., Meinesz A., Riberta M.A., Ballesteros E. Spread of the green alga Caulerpa taxifolia (Caulerpales, Chlorophyta) in the Mediterranean: possible consequences of a major ecological event. Sci. Mar. 1995, 59:21-29.
8. Boudouresque C.F., Verlaque M. Biological pollution in the Mediterranean Sea: invasive versus introduced macrophytes. Mar. Pollut. Bull. 2002, 44(1):32-38.
9. Byrnes J.E., Reynolds P.L., Stachowicz J.J. Invasions and extinctions reshape coastal marine food webs. PLos One 2007, 3:e295.
10. Carabel S., Godínez-Domínguez E., Verísimo P., Fernández L., Freire J. An assessment of sample processing methods for stable isotope analyses of marine food webs. J.Exp. Mar. Biol. Ecol. 2006, 336:254-261.
11. Casu D., Ceccerelli G., Sechi N., Rumolo P., Sarà G. Caulerpa racemosa var. cylindracea as a potential source of organic matter for benthic consumers: evidences from a stable isotope analysis. Aquat. Ecol. 2009, 43(4):1023-1029.
12. Clarke K.R., Warwick R.M. Ataxonomic distinctness index and its statistcal properties. JAppl. Ecol. 1998, 35:523-531.
13. Clarke K.R., Warwick R.M. Afurther biodiversity index applicable to species lists: variation in taxonomic distinctness. Mar. Ecol. Prog. Ser. 2001, 216:265-278.
14. Clarke K.R., Warwick R.M. The taxonomic distinctness measure of biodiversity: weighting of step lengths between hierarchical levels. Mar. Ecol. Prog. Ser. 1999, 184:21-29.
15. Decottignies P., Beninger P.G., Rince Y., Riera P. Trophic interactions between two introduced suspension feeders, Crepidula fornicata and Crassostrea gigas, are influenced by seasonal effects and qualitative selection capacity. J.Exp. Mar. Biol. Ecol. 2007, 342(2):231-241.
16. Deudero S., Box A., Alos J., Arroyo N.L., Marba N. Functional changes due to invasive species: food web shifts at shallow Posidonia oceanica seagrass beds colonized by the alien macroalga Caulerpa racemosa. Estuar. Coast. Shelf Sci. 2011, 93(2):106-116.
17. Duffy J.E. Biodiversity loss, trophic skew and ecosystem functioning. Ecol. Lett. 2003, 6(8):680-687.
18. Elton C.S. The Ecology of Invasions by Animals and Plants 1958, 181. Methuen & Co., London.
19. Galil B.S. Loss or gain? Invasive aliens and biodiversity in the Mediterranean Sea. Mar. Pollut. Bull. 2007, 55:314-322.
20. Gambi M.C., Giangrande A., Martinelli M., Chessa L.A. Polychaetes of a Posidonia oceanica Bed off Sardinia (Italy) - spatio temporal distribution and feeding guild analysis. Sci. Mar. 1995, 59:129-141.
21. Gambi M.C., Lorenti M., Russo G.F., Scipione M.B., Zupo V. Depth and seasonal distribution of some groups of the Vagile fauna of the posidonia oceanica leaf stratum - structural and trophic analyses. Mar. Ecol. 1992, 13:17-39.
22. Glasby T.M. Caulerpa taxifolia in seagrass meadows: killer or opportunistic weed?. Biol. Invasions 2013, 15(5):1017-1035.
23. Heleno R.H., Ceia R.S., Ramos J.A., Memmott J. Effects of alien plants on insect abundance and biomass: a food-web approach. Conserv. Biol. 2009, 23:410-419.
24. Holmer M., Marbà N., Lamote M., Duarte C.M. Deterioration of sediment quality in seagrass meadows (Posidonia oceanica) invaded by macroalgae (Caulerpa sp.). Estuaries Coasts 2009, 32:456-466.
25. Ince R., Hyndes G.A., Lavery P.S., Vanderklift M.A. Marine macrophytes directly enhance abundances of sandy beach fauna through provision of food and habitat. Estuar. Coast. Shelf Sci. 2007, 74(1-2):77-86.
26. Kennedy H., Beggins J., Duarte C.M., Fourqurean J.W., Holmer M., Marbà N., Middelburg J.J. Seagrass sediments as a global carbon sink: Isotopic constraints. Glob. Biogeochem. Cycles 2010, 24(4). art. no. GB4026.
27. Klein J., Verlaque M. Temporal trends in invasion impacts in macrophyte assemblages of the Mediterranean Sea. Cah. Biol. Mar. 2012, 53(3):403-407.
28. Klein J., Verlaque M. The Caulerpa racemosa invasion: a critical review. Mar. Pollut. Bull. 2008, 56:205-225.
29. Lafaille P., Petillon J., Parlier E., Valery L., Ysnel F., Radureau A., Feunteun E., Lefeuvre J.C. Does the invasive plant Elymus athericus modify fish diet in tidal salt marshes?. Estuar. Coast. Shelf Sci. 2005, 65(4):739-746.
30. Layman C.A., Araújo M.S., Boucek R., Harrison E., Jud Z.R., Matich P., Hammerschlag-Peyer C.M., Rosenblatt A., Vaudo J., Yeager L.A., Post D.M., Bearhop S. Applying stable isotopes to examine food-web structure: an overview of analytical tools. Biol. Rev. 2012, 87(3):545-562.
31. Layman C.A., Quattrochi J.P., Peyer C.M., Allgeier J.E. Niche width collapse in a resilient top predator following ecosystem fragmentation. Ecol. Lett. 2007, 10:937-944.
32. Levin L.A., Neira C., Grosholz E.D. Invasive cordgrass modifies wetland trophic function. Ecology 2006, 87(2):419-432.
33. Lindeman R.L. The trophic-dynamic aspect of ecology. Ecology 1942, 23(4):399-417.
34. Longepierre S., Robert A., Levi F., Francour P. How an invasive alga species (Caulerpa taxifolia) induces changes in foraging strategies of the benthivorous fish Mullus surmuletus in coastal Mediterranean ecosystems. Biodivers. Conserv. 2005, 14:365-376.
35. Lorenti M., Gambi M.C., Guglielmo R., Patti F.P., Scipione M.B., Zupo V., Buia M.C. Soft-bottom macrofaunal assemblages in the Gulf of Salerno, Tyrrhenian Sea, Italy, an area affected by the invasion of the seaweed Caulerpa racemosa var. cylindracea. Mar. Ecol. Evol. Perspect. 2011, 32(3):320-334.
36. McCutchan J.H.J., Lewis W.M., Kendall C., McGrath C.C. Variation in trophic shift for stable isotope ratios of carbon, nitrogen, and sulfur. Oikos 2003, 102:378-390.
37. Montefalcone M., Albertelli G., Morri C., Bianchi C.N. Patterns of wide-scale substitution within meadows of the seagrass Posidonia oceanica in NW Mediterranean Sea: invaders are stronger than natives. Aquat. Conserv.-Marine Freshw. Ecosyst. 2010, 20(5):507-515.
38. Newsome S.D., Del Rio C.M., Bearhop S., Phillips D.L. Aniche for isotopic ecology. Front. Ecol. Environ. 2007, 5(8):429-436.
39. Ng J.S.S., Wai T.C., Williams G.A. The effects of acidification on the stable isotope signatures of marine algae and molluscs. Mar. Chem. 2007, 103(1-2):97-102.
40. Ólafsson E., Aarnio K., Bonsdorff E., Arroyo N.L. Fauna of the green alga Cladophora glomerata in the Baltic Sea: density, diversity and algal decomposition stage. Mar. Biol. 2013, 10.1007/s00227-013-2229-1.
41. Peterson B.J., Fry B. Stable isotopes in ecosystem studies. Ann. Rev. Ecol. Syst. 1987, 18:293-320.
42. Phillips D.L., Gregg J.W. Source partitioning using stable isotopes: coping with too many sources. Oecologia 2003, 136(2):261-269.
43. Piazzi L., Balata D. The spread of Caulerpa racemosa var. cylindracea in the Mediterranean Sea: an example of how biological invasions can influence beta diversity. Mar. Environ. Res. 2008, 65(1):50-61.
44. Piazzi L., Ceccherelli G., Cinelli F. Threats to macroalgal diversity: effects of the introduced green alga Caulerpa racemosa in the Mediterranean. Mar. Ecol. Prog. Ser. 2001, 210:149-159.
45. Poppe G.T., Goto Y. European Seashells 1991, vol I. (Wiesbaden, Germany).
46. Poppe G.T., Goto Y. European Seashells 1993, vol II. (Hackenheim, Germany).
47. Post D.M. Using stable isotopes to estimate trophic position: models, methods, and assumptions. Ecology 2002, 83:703-718.
48. Raffaelli D., var den Putten W.H., Persson L., Wardle D.A., Petchey O.L., Koricheva J., van der Heijden M., Mikola J., Kennedy T. Multi-trophic dynamics and ecosystems processess 2002, Oxford University Press. Biodiversity and Ecosystem Functioning. Synthesis and Perspectives, M. Loreau, S. Naeem, P. Inchausti (Eds.).
49. Salas F., Patrício J., Marcos C., Pardal M.A., Pérez-Ruzafa A., Marques J.C. Are taxonomic distincness measures compliant to other ecological indicators in assessing ecological status?. Mar. Pollut. Bull. 2006, 52:817-829.
50. San Martin G. Annelida Polychaeta II, Syllidae 2003, Vol, Madrid.
51. Sanchez-Moyano J.E., Estacio F.J., Garcia-Adiego E.M., Garcia-Gomez J.C. Effect of the vegetative cycle of Caulerpa prolifera on the spatio-temporal variation of invertebrate macrofauna. Aquat. Bot. 2004, 70:163-174.
52. Schlaepfer M.A., Sax D.F., Olden J.D. The potential conservation value of non-native species. Conserv. Biol. 2010, 25(3):428-437.
53. Skilleter G.A., Pryor A., Miller S., Cameron B. Detecting the effects of physical disturbance on benthic assemblages in a subtropical estuary: a beyond BACI approach. J.Exp. Mar. Biol. Ecol. 2006, 338(2):271-287.
54. Somerfield P.J., Clarke K.R. Taxonomic levesl in marine community studies. Mar. Ecol. Prog. Ser. 1995, 127:113-119.
55. Thomsen M.S. Experimental evidence for positive effects of invasive seaweed on native invertebrates via habitat-formation in a seagrass bed. Aquat. Invasions 2010, 5(4):341-346.
56. Varela-Álvarez E., Gómez Garreta A., Rull Lluch J., Salvador Soler N., Serrao E.A., et al. Mediterranean species of caulerpa are polyploid with smaller genomes in the invasive ones. PLoS ONE 2012, 7(10):e47728. 10.1371/journal.pone.0047728.
57. Vázquez -Luis M., Sánchez-Jerez P., Bayle-Sempere J. Does the invasion of Caulerpa racemosa var. cylindracea affect the feeding habits of amphipods (Crustacea: Amphipoda)?. J.Mar. Biol. Assoc. UK 2013, 93:87-94.
58. Vazquez-Luis M., Borg J.A., Sanchez-Jerez P., Bayle-Sempere J.T. Habitat colonisation by amphipods: comparison between native and alien algae. J.Exp. Mar. Biology Ecol. 2012, 432:162-170.
59. Viétez J.M., Alòs C., Parapar J., Besteiro C., Moreira J., Núñez J., Laborda A.J., San Martin G. Annelida Polychaeta I 2004, Vol, Madrid.
60. Vizzini S., Mazzola A. Stable isotopes and trophic positions of littoral fishes from a Mediterranean marine protected area. Environ. Biol. Fish. 2009, 84:13-25.
61. Vizzini S., Sarà G., Michener R.H. The role and contribution of the seagrass Posidonia oceanica (L.) Delille organic matter for secondary consumers as revealed by carbon and nitrogen stable isotope analysis. Acta Oecol. 2002, 23(4):277-285.
62. Wallentinus I., Nyberg C.D. "Introduced marine organisms as habitat modifiers. Mar. Pollut. Bull. 2007, 55(7-9):323-332.
63. Warwick R.M., Clarke K.R. New 'biodiversity' measures reveal a decrease in taxonomic distinctness with increasing stress. Mar. Ecol. Prog. Ser. 1995, 129:301-305.
64. Williams R.J., Berlow E.L., Dunne J.A., Barabási A.-L., Martinez N.D. Two degrees of separation in compelx food webs. PNAS 2002, 99(20):12913-12916.
65. Zariquiey R. Crustáceos Decápodos Ibéricos. Consejo Superior de Investigaciones Científicas 1968, vol 32. Patronato Juan de la Cierva, Barcelona.