Effects of invasive seaweeds on feeding preference and performance of a keystone Mediterranean herbivore

Biological Invasions

Volumn 13, Issue 7, 2011, Pages 1559-1570

  Tomas, Fiona ^a   Box, Antonio ^a   Terrados, Jorge ^a  

^a INSTITUTO MEDITERRÁNEO DE ESTUDIOS AVANZADOS   (Spain)

Author keywords

Biotic resistance; Caulerpa racemosa; Enemy release hypothesis; Plant herbivore interactions; Sea urchin; Seagrass

Indexed keywords

BIOTIC FACTOR; COMMUNITY STRUCTURE; ECHINODERM; ECOLOGICAL IMPACT; ECOSYSTEM FUNCTION; ECOSYSTEM SERVICE; ENEMY RELEASE HYPOTHESIS; EXPERIMENTAL STUDY; FOOD PREFERENCE; GRAZING; HERBIVORE; INVASIVE SPECIES; KEYSTONE SPECIES; NUTRITIVE VALUE; PLANT-HERBIVORE INTERACTION; PREDATOR-PREY INTERACTION; SEAWEED; SPECIES CONSERVATION; TROPHIC STRUCTURE;

MEDITERRANEAN SEA;

ALGAE; CAULERPA; CAULERPA RACEMOSA; ECHINOIDEA;

EID: 79957973024     PISSN: 13873547     EISSN: None     Source Type: Journal    
DOI: 10.1007/s10530-010-9913-6     Document Type: Article

References (93)

1. Ballesteros E (2006) Mediterranean coralligenous assemblages: a synthesis of present knowledge. Ocean Mar Biol Annu Rev 44: 123-195.
2. Ballesteros E, Cebrian E, Alcoverro T (2007) Mortality of shoots of Posidonia oceanica following meadow invasion by the red alga Lophocladia lallemandii. Bot Mar 50: 8-13.
3. Bernays EA, Minkenberg OPJM (1997) Insect herbivores: different reasons for being a generalist. Ecology 78: 1157-1169.
4. Berner D, Blanckenhorn WU, Körner C (2005) Grasshoppers cope with low host plant quality by compensatory feeding and food selection: N limitation challenged. Oikos 111: 525-533.
5. Borer ET, Halpern BS, Seabloom EW (2006) Assymetry in community regulation: effects of predators and productivity. Ecology 87: 2813-2820.
6. Boudoresque CF, Bernard G, Pergent G et al (2009) Regression of Mediterranean seagrasses caused by natural processes and anthropogenic disturbances and stress: a critical review. Bot Mar 52: 395-418.
7. Boudouresque C-F, Verlaque M (2001) Ecology of Paracentrotus lividus. In: Lawrence JM (ed) Edible sea urchins: biology and ecology. Elsevier Science BV, Amsterdam, pp 177-216.
8. Boudouresque CF, Verlaque M (2002) Biological pollution in the Mediterranean Sea: invasive versus introduced macrophytes. Mar Poll Bull 44: 32-38.
9. Boudouresque CF, Lemée R, Mari X et al (1996) The invasive alga Caulerpa taxifolia is not a suitable diet for the sea urchin Paracentrotus lividus. Aq Bot 53: 245-250.
10. Box A, Deudero S, Sureda A et al (2009) Diet and phyisiological responses of Spondylosoma cantharus (Linnaeus, 1758) to the Caulerpa racemosa var cylindracea invasion. J Exp Mar Biol Ecol 380: 11-19.
11. Box A, Sureda A, Tauler P et al (2010) Seasonality of caulerpenyne content in the native Caulerpa prolifera and the invasive C taxifolia and C racemosa var cylindracea in the western Mediterranean. Bot Mar 53(4): 367-375.
12. Bulleri F, Tamburello L, Benedetti Cecchi L (2009) Loss of consumers alters the effects of resident assemblages on the local spread of an introduced macroalga. Oikos 118: 269-279.
13. Cebrian E, Ballesteros E (2010) Invasion of Mediterranean benthic assemblages by red alga Lophocladia lallemandii (Montagne) F Schmitz: depth-related temporal variability in biomass and phenology. Aq Bot 92: 81-85.
14. Cebrian E, Ballesteros E, Linares C et al. (in press) Do native herbivores provide resistance to Mediterranean marine bioinvasions? A seaweed example. Biol Inv doi: 10. 1007/s10530-010-9898-1.
15. Cook EJ, Kelly MS (2007) Effect of variation in the protein value of the red macroalga Palmaria palmata on the feeding, growth and gonad composition of the sea urchins Psammechinus miliaris and Paracentrotus lividus (Echinodermata). Aquaculture 270: 207-217.
16. Cornell HV, Hawkins BA (2003) Herbivore responses to plant secondary compounds: a test of phytochemical coevolution theory. Am Nat 161: 507-522.
17. Cruz-Rivera E, Hay ME (2000) Can quantity replace quality? Food choice, compensatory feeding, and fitness of marine mesograzers. Ecology 81: 201-219.
18. Cruz-Rivera E, Hay ME (2001) Macroalgal traits and the feeding and fitness of an herbivorous amphipod: the roles of selectivity, mixing, and compensation. Mar Ecol Prog Ser 218: 249-266.
19. Davis AR, Benkendorff K, Ward DW (2005) Responses of common SE Australian herbivores to three suspected invasive Caulerpa spp. Mar Biol 146: 859-868.
20. Deudero S, Blanco A, Box A et al (2010) Interaction between the invasive macroalga Lophocladia lallemandii and the bryozoan Reteporella grimaldii at seagrass meadows: density and physiological responses. Biol Inv 12: 41-52.
21. Duffy JE, Hay ME (1990) Seaweed adaptations to herbivory-chemical, structural, and morphological defenses are often adjusted to spatial or temporal patterns of attack. Bioscience 40: 368-375.
22. Duffy JE, Paul VJ (1992) Prey nutritional quality and the effectiveness of chemical defenses against tropical reef fishes. Oecologia 90: 333-339.
23. Dumay O, Pergent G, Pergent-Martini C et al (2002) Variations in caulerpenyne contents in Caulerpa taxifolia and Caulerpa racemosa. J Chem Ecol 28: 343-352.
24. Ebert TA (1968) Growth rates of the sea urchin Strongylocentrotus purpuratus related to food availability and spine abrasion. Ecology 49: 1075-1091.
25. Ebert TA (1980) Relative growth of sea urchin jaws: an example of plastic resource allocation. Bull Mar Sci 30: 467-474.
26. Edwards PB, Ebert A (1991) Plastic responses to limited food availability and spine damage in the sea urchin Strongylocentrotus purpuratus (Stimpson). J Exp Mar Biol Ecol 145: 205-220.
27. Elton CS (1958) The ecology of invasions by animals and plants. Methuen & Co, London.
28. Fernandez C, Boudouresque C-F (1997) Phenotypic plasticity of Paracentrotus lividus (Echinodermata: Echinoidea) in a lagoonal environment. Mar Ecol Prog Ser 152: 145-152.
29. Fink P, Von Elert E (2006) Physiological responses to stoichoimetric constraints: nutrient limitation and compensatory feeding in a freshwater snail. Oikos 115: 484-494.
30. Gaines S, Lubchenco J (1982) A unified approach to marine plant -herbivore interactions II biogeography. Ann Rev Ecol Syst 13: 111-138.
31. Galil BS (2008) Alien species in the Mediterranean Sea-which, when, where, why? Hydrobiologia 606: 105-116.
32. George SB (1996) Echinoderm egg and larval quality as a function of adult nutritional state. Oceanol Acta 19: 297-308.
33. Goecker ME, Heck KL, Valentine JF (2005) Effects of nitrogen concentrations in turtlegrass Thalassia testudinum on consumption by the bucktooth parrotfish Sparisoma radians. Mar Ecol Prog Ser 286: 239-248.
34. Gollan JR, Wright JT (2006) Limited grazing pressure by native herbivores on the invasive seaweed Caulerpa taxifolia in a temperate Australian estuary. Mar Freshw Res 57: 685-694.
35. Gross H, Goeger DE, Hills P et al (2006) Lophocladines, bioactive alkaloids from the red alga Lophocladia sp. J Nat Prod 69: 640-644.
36. Keane RM, Crawley MJ (2002) Exotic plant invasions and the enemy release hypothesis. TREE 17: 164-170.
37. Lawrence JM (2001) Edible sea urchins: biology and ecology. Elsevier Science BV, Amsterdam.
38. Levine JM, Vila M, D'Antonio CM et al (2003) Mechanisms underlying the impacts of exotic plant invasions. Proc R Soc Lond Ser B Biol Sci 270: 775-781.
39. Levitan DR (1988) Density-dependent size regulation and negative growth in the sea urchin Diadema antillarum Philippi. Oecologia 76: 627-629.
40. Levitan DR (1991) Skeletal changes in the test and jaws of the sea urchin Diadema antillarum in response to food limitation. Mar Biol 111: 431-435.
41. Lubchenco J, Gaines S (1981) A unified approach to marine plant-herbivore interactions I Populations and communities. Ann Rev Ecol Syst 12: 405-437.
42. Lyons DA, Scheibling RE (2007) Differences in somatic and gonadic growth of sea urchins (Strongylocentrotus droebachiensis) fed kelp (Laminaria longicruris) or the invasive alga Codium fragile ssp tomentosoides are related to energy acquisition. Mar Biol 152: 285-295.
43. Mack RN, Simberloff D, Lonsdale WM et al (2000) Biotic invasions: causes, epidemiology, global consequences, and control. Ecol Appl 10: 689-710.
44. Mitchell CE, Agrawal AA, Bever JD et al (2006) Biotic interactions and plant invasions. Ecol Lett 9: 726-740.
45. Monteiro CA, Engelen AH, Santos ROP (2009) Macro- and mesoherbivores prefer native seaweeds over the invasive brown seaweed Sargassum muticum: a potential regulating role on invasions. Mar Biol 156: 2505-2515.
46. Moreau G, Quiring DT, Eveleigh ES et al (2003) Advantages of a mixed diet: feeding on several foliar age classes increases the performance of a specialist insect herbivore. Oecologia 135: 391-399.
47. Occhipinti-Ambrogi A, Savini D (2003) Biological invasions as a component of global change in stressed ecosystems. Mar Poll Bull 46: 542-551.
48. Occhipinti-Ambrogi A, Machini A, Cantone G et al. (2010) Alien species along the Italian coasts: an overview. Biol Inv doi: 10. 1007/s10530-010-9803-y.
49. Paine RT (1992) Food-web analysis through field measurement of per capita interaction strength. Nature 355: 73-75.
50. Panayotidis P, Žuljević A (2001) Sexual reproduction of the invasive green alga Caulerpa racemosa var occidentalis in the Mediterranean Sea. Oceanol Acta 24: 199-203.
51. Parker JD, Hay ME (2005) Biotic resistance to plant invasions? Native herbivores prefer non-native plants. Ecol Lett 8: 959-967.
52. Parker JD, Burkepile DE, Hay ME (2006) Opposing effects of native and exotic herbivores on plant invasions. Science 311: 1459-1461.
53. Paul VJ, Cruz-Rivera E, Thacker RW (2001) The chemical ecology of macroalgal-herbivore interactions: ecological and evolutionary perspectives. In: McClintock JB, Baker BJ (eds) Marine chemical ecology. CRC Press, Boca Raton, pp 227-266.
54. Paul VJ, Arthur KE, Ritson-Williams R et al (2007) Chemical defenses: from compounds to communities. Biol Bull 213: 226-251.
55. Pergent G, Romero J, Pergent-Martini C et al (1994) Primary production, stocks and fluxes in the Mediterranean seagrass Posidonia oceanica. Mar Ecol Prog Ser 106: 139-146.
56. Piazzi L, Balata D (2008) The spread of Caulerpa racemosa var cylindracea in the Mediterranean Sea: an example of how biological invasions can influence beta diversity. Mar Env Res 65: 50-61.
57. Piazzi L, Cinelli F (1999) Développement et dynamique saisonnière d'un peuplement méditerranéen de l'algue tropicale Caulerpa racemosa (Forsskal). J Agardh Crypt Alg 20: 295-300.
58. Piazzi L, Cinelli F (2001) Distribution and dominance of two introduced turf-forming macroalgae on the coast of Tuscany, Italy, Northwestern Mediterranean Sea in relation to different habitats and sedimentation. Bot Mar 44: 509-520.
59. Piazzi L, Meinesz A, Verlaque M et al (2005) Invasion of Caulerpa racemosa var cylindracea (Caulerpales, Chlorophyta) in the Mediterranean Sea: an assessment of the spread. Crypt Alg 26: 189-202.
60. Power ME (1992) Top-down and bottom-up forces in food webs: do plants have primacy? Ecology 73: 733-746.
61. Procaccini G, Buia MC, Gambi MC et al (2003) The seagrasses of the Western Mediterranean. In: Green EP, Short FT (eds) World Atlas of seagrasses University. California Press, Berkeley, pp 48-58.
62. Quinn GP, Keough MJ (2002) Experimental design and data analysis for biologists. Cambridge University Press, Cambridge.
63. Ricciardi A, Ward JM (2006) Comment on "Opposing effects of native and exotic herbivores on plant invasions". Science 313: 298.
64. Rilov G (2009) Predator-Prey interactions of marine invaders. In: Rilov G, Crooks JA (eds) Biological invasions in marine ecosystems Ecological, management, and geographic perspectives. Springer, Berlin, pp 261-286.
65. Romero J (2004) Posidònia: els prats del fons del mar, Col·lecció Norai. Publicacions de l'Ajuntament de Badalona, Badalona.
66. Ruitton S, Verlaque M, Aubin G et al (2006) Grazing on Caulerpa racemosa var cylindracea (Caulerpales, Chlorophyta) in the Mediterranean Sea by herbivorous fishes and sea urchins. Vie Milieu-Life Environ 56: 33-41.
67. Ruiz JM, Pérez M, Romero J et al (2009) The importance of herbivory in the decline of a seagrass (Posidonia oceanica) meadow near a fish farm: an experimental approach. Bot Mar 52: 449-458.
68. Sala E, Zabala M (1996) Fish predation and the structure of the sea urchin Paracentrotus lividus populations in the NW Mediterranean. Mar Ecol Prog Ser 140: 71-81.
69. Schaffelke B, Smith JE, Hewitt CL (2006) Introduced macroalgae-a growing concern. J Appl Psycol 18: 529-541.
70. Scheibling RE, Anthony SX (2001) Feeding, growth and reproduction of sea urchins (Strongylocentrotus droebachiensis) on single and mixed diets of kelp (Laminaria spp.) and the invasive alga Codium fragile ssp tomentosoides. Mar Biol 139: 139-146.
71. Scheibling RE, Gagnon P (2006) Competitive interactions between the invasive green alga Codium fragile ssp. tomentosoides and native canopy-forming seaweeds in Nova Scotia (Canada). Mar Ecol Prog Ser 325: 1-14.
72. Scheibling RE, Lyons DA, Sumi CBT (2008) Grazing of the invasive alga Codium fragile ssp tomentosoides by the common periwinkle Littorina littorea: effects of thallus size, age and condition. J Exp Mar Biol Ecol 355: 103-113.
73. Simpson SJ, Abisgold JD (1985) Compensation by locusts for changes in dietary nutrients: behavioural mechanisms. Phys Entom 10: 443-452.
74. Sjotun K, Eggereide SF, Hoisaeter T (2007) Grazer-controlled recruitment of the introduced Sargassum muticum (Phaeophycae, Fucales) in northern Europe. Mar Ecol Prog Ser 342: 127-138.
75. Sumi CBT, Scheibling RE (2005) Role of grazing by sea urchins Strongylocentrotus droebachiensis in regulating the invasive alga Codium fragile ssp tomentosoides in Nova Scotia. Mar Ecol Prog Ser 292: 203-212.
76. Tallamy DW, Ballard M, D'Amico V (2010) Can alien plants support generalist insect herbivores? Biol Inv 12: 2285-2292.
77. Targett NM, Arnold TM (2001) Effects of secondary metabolites on digestion in marine herbivores. In: McClintock JB, Baker BJ (eds) Marine chemical ecology. CRC Press, London, pp 391-411.
78. Thibaut T, Meinesz A, Amade P et al (2001) Elysia subornata (Mollusca) a potential control agent of the alga Caulerpa taxifolia (Chlorophyta) in the Mediterranean Sea. J Mar Biol Assoc UK 81: 497-504.
79. Thomsen M, Wernberg T, Tuya F et al (2009) Evidence for impacts of nonindigenous macroalgae: a meta-analysis of experimental field studies. J Psycol 45: 812-819.
80. Thornber CS, Kinlan BP, Graham MH et al (2004) Population ecology of the invasive kelp Undaria pinnatifida in California: environmental and biological controls on demography. Mar Ecol Prog Ser 268: 69-80.
81. Tomas F, Turon X, Romero J (2005a) Effects of herbivores on a Posidonia oceanica seagrass meadow: importance of epiphytes. Mar Ecol Prog Ser 287: 115-125.
82. Tomas F, Romero J, Turon X (2005b) Experimental evidence that intra-specific competition in seagrass meadows reduces reproductive potential in the sea urchin Paracentrotus lividus (Lamarck). Sci Mar 69: 475-484.
83. Tomas F, Alvarez-Cascos D, Turon X et al (2006) Differential element assimilation by sea urchins Paracentrotus lividus in seagrass beds: implications for trophic interactions. Mar Ecol Prog Ser 306: 125-131.
84. Trowbridge CD (1995) Establishment of the green alga Codium fragile ssp. tomentosoides on New Zealand rocky shores-current distribution and invertebrate grazers. J Ecol 83: 949-965.
85. Vadas RL (1977) Preferential feeding: an optimization strategy in sea urchins. Ecol Mon 47: 337-371.
86. Valentine JF, Heck KLJ (2001) The role of leaf nitrogen content in determining turtlegrass (Thalassia testudinum) grazing by a generalized herbivore in the northeastern Gulf of Mexico. J Exp Mar Biol Ecol 258: 65-86.
87. Vergés A, Becerro MA, Alcoverro T et al (2007a) Experimental evidence of chemical deterrence against multiple herbivores in the seagrass Posidonia oceanica. Mar Ecol Prog Ser 343: 107-114.
88. Vergés A, Becerro MA, Alcoverro T et al (2007b) Variation in multiple traits of vegetative and reproductive seagrass tissues influences plant-herbivore interactions. Oecologia 151: 675-686.
89. Vitousek PM, D'Antonio CM, Loope LL et al (1997) Introduced species: a significant component of human-caused global change. N Z J Ecol 21: 1-16.
90. Williams SL, Smith JE (2007) A global review of the distribution, taxonomy, and impacts of introduced seaweeds. Ann Rev Ecol Syst 38: 327-359.
91. Wright JT, Gribben PE (2008) Predicting the impact of an invasive seaweed on the fitness of native fauna. J Appl Ecol 45: 1540-1549.
92. Yoshida T, Jones LE, Ellner SP et al (2003) Rapid evolution drives ecological dynamics in a predator-prey system. Nature 424: 303-306.
93. Žuljević A, Nikolic V, Despalatovic M et al (2008) Experimental in situ feeding of the sea urchin Paracentrotus lividus with the invasive algae Caulerpa racemosa var cylindracea and Caulerpa taxifolia in the Adriatic Sea. Fresenius Environ Bull 17: 2098-2102.