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

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Abstract

The consequences of invasive species on ecosystem processes and ecological interactions remain poorly understood. Predator–prey interactions are fundamental in shaping species evolution and community structure and can be strongly modified by species introductions. To fully understand the ecological effects of invasive species on trophic linkages it is important to characterize novel interactions between native predators and exotic prey and to identify the impacts of invasive species on the performance of native predators. Although seaweed invasions are a growing global concern, our understanding of invasive algae—herbivore interactions is still very limited. We used a series of feeding experiments between a native herbivore and four invasive algae in the Mediterranean Sea to examine the potential of native sea urchins to consume invasive seaweeds and the impacts of invasive seaweed on herbivore performance. We found that three of the four invasive species examined are avoided by native herbivores, and that feeding behaviour in sea urchins is not driven by plant nutritional quality. On the other hand, Caulerpa racemosa is readily consumed by sea urchins, but may escape enemy control by reducing their performance. Recognizing the negative impacts of C. racemosa on herbivore performance has highlighted an enemy escape mechanism that contributes to explaining how this widespread invasive alga, which is preferred and consumed by herbivores, is not eradicated by grazing in the field. Furthermore, given the ecological and economic importance of sea urchins, negative impacts of invasive seaweeds on their performance could have dramatic effects on ecosystem function and services, and should be accounted for in sea urchin population management strategies.

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References

  • Ballesteros E (2006) Mediterranean coralligenous assemblages: a synthesis of present knowledge. Ocean Mar Biol Annu Rev 44:123–195

    Google Scholar 

  • 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

    Article  Google Scholar 

  • Bernays EA, Minkenberg OPJM (1997) Insect herbivores: different reasons for being a generalist. Ecology 78:1157–1169

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Borer ET, Halpern BS, Seabloom EW (2006) Assymetry in community regulation: effects of predators and productivity. Ecology 87:2813–2820

    Article  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Chapter  Google Scholar 

  • Boudouresque CF, Verlaque M (2002) Biological pollution in the Mediterranean Sea: invasive versus introduced macrophytes. Mar Poll Bull 44:32–38

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

  • 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

    Article  CAS  Google Scholar 

  • Cornell HV, Hawkins BA (2003) Herbivore responses to plant secondary compounds: a test of phytochemical coevolution theory. Am Nat 161:507–522

    Article  PubMed  Google Scholar 

  • Cruz-Rivera E, Hay ME (2000) Can quantity replace quality? Food choice, compensatory feeding, and fitness of marine mesograzers. Ecology 81:201–219

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Davis AR, Benkendorff K, Ward DW (2005) Responses of common SE Australian herbivores to three suspected invasive Caulerpa spp. Mar Biol 146:859–868

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Duffy JE, Paul VJ (1992) Prey nutritional quality and the effectiveness of chemical defenses against tropical reef fishes. Oecologia 90:333–339

    Article  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Ebert TA (1968) Growth rates of the sea urchin Strongylocentrotus purpuratus related to food availability and spine abrasion. Ecology 49:1075–1091

    Article  Google Scholar 

  • Ebert TA (1980) Relative growth of sea urchin jaws: an example of plastic resource allocation. Bull Mar Sci 30:467–474

    Google Scholar 

  • 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

    Article  Google Scholar 

  • Elton CS (1958) The ecology of invasions by animals and plants. Methuen & Co, London

    Google Scholar 

  • Fernandez C, Boudouresque C-F (1997) Phenotypic plasticity of Paracentrotus lividus (Echinodermata: Echinoidea) in a lagoonal environment. Mar Ecol Prog Ser 152:145–152

    Article  Google Scholar 

  • Fink P, Von Elert E (2006) Physiological responses to stoichoimetric constraints: nutrient limitation and compensatory feeding in a freshwater snail. Oikos 115:484–494

    Article  CAS  Google Scholar 

  • Gaines S, Lubchenco J (1982) A unified approach to marine plant -herbivore interactions II biogeography. Ann Rev Ecol Syst 13:111–138

    Article  Google Scholar 

  • Galil BS (2008) Alien species in the Mediterranean Sea—which, when, where, why? Hydrobiologia 606:105–116

    Article  Google Scholar 

  • George SB (1996) Echinoderm egg and larval quality as a function of adult nutritional state. Oceanol Acta 19:297–308

    Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Gross H, Goeger DE, Hills P et al (2006) Lophocladines, bioactive alkaloids from the red alga Lophocladia sp. J Nat Prod 69:640–644

    Article  PubMed  CAS  Google Scholar 

  • Keane RM, Crawley MJ (2002) Exotic plant invasions and the enemy release hypothesis. TREE 17:164–170

    Google Scholar 

  • Lawrence JM (2001) Edible sea urchins: biology and ecology. Elsevier Science BV, Amsterdam

    Google Scholar 

  • 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

    Article  Google Scholar 

  • Levitan DR (1988) Density-dependent size regulation and negative growth in the sea urchin Diadema antillarum Philippi. Oecologia 76:627–629

    Google Scholar 

  • 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

    Article  Google Scholar 

  • Lubchenco J, Gaines S (1981) A unified approach to marine plant-herbivore interactions I Populations and communities. Ann Rev Ecol Syst 12:405–437

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Mack RN, Simberloff D, Lonsdale WM et al (2000) Biotic invasions: causes, epidemiology, global consequences, and control. Ecol Appl 10:689–710

    Article  Google Scholar 

  • Mitchell CE, Agrawal AA, Bever JD et al (2006) Biotic interactions and plant invasions. Ecol Lett 9:726–740

    Article  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    PubMed  Google Scholar 

  • Occhipinti-Ambrogi A, Savini D (2003) Biological invasions as a component of global change in stressed ecosystems. Mar Poll Bull 46:542–551

    Article  CAS  Google Scholar 

  • 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

  • Paine RT (1992) Food-web analysis through field measurement of per capita interaction strength. Nature 355:73–75

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Parker JD, Hay ME (2005) Biotic resistance to plant invasions? Native herbivores prefer non-native plants. Ecol Lett 8:959–967

    Article  Google Scholar 

  • Parker JD, Burkepile DE, Hay ME (2006) Opposing effects of native and exotic herbivores on plant invasions. Science 311:1459–1461

    Article  PubMed  CAS  Google Scholar 

  • 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

    Google Scholar 

  • Paul VJ, Arthur KE, Ritson-Williams R et al (2007) Chemical defenses: from compounds to communities. Biol Bull 213:226–251

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Google Scholar 

  • Power ME (1992) Top-down and bottom-up forces in food webs: do plants have primacy? Ecology 73:733–746

    Article  Google Scholar 

  • 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

    Google Scholar 

  • Quinn GP, Keough MJ (2002) Experimental design and data analysis for biologists. Cambridge University Press, Cambridge

    Google Scholar 

  • Ricciardi A, Ward JM (2006) Comment on “Opposing effects of native and exotic herbivores on plant invasions”. Science 313:298

    Article  PubMed  CAS  Google Scholar 

  • 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

    Chapter  Google Scholar 

  • Romero J (2004) Posidònia: els prats del fons del mar, Col·lecció Norai. Publicacions de l’Ajuntament de Badalona, Badalona

    Google Scholar 

  • 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

    Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Schaffelke B, Smith JE, Hewitt CL (2006) Introduced macroalgae—a growing concern. J Appl Psycol 18:529–541

    Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Simpson SJ, Abisgold JD (1985) Compensation by locusts for changes in dietary nutrients: behavioural mechanisms. Phys Entom 10:443–452

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Tallamy DW, Ballard M, D’Amico V (2010) Can alien plants support generalist insect herbivores? Biol Inv 12:2285–2292

    Article  Google Scholar 

  • 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

    Chapter  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Vadas RL (1977) Preferential feeding: an optimization strategy in sea urchins. Ecol Mon 47:337–371

    Article  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Google Scholar 

  • Williams SL, Smith JE (2007) A global review of the distribution, taxonomy, and impacts of introduced seaweeds. Ann Rev Ecol Syst 38:327–359

    Article  Google Scholar 

  • Wright JT, Gribben PE (2008) Predicting the impact of an invasive seaweed on the fitness of native fauna. J Appl Ecol 45:1540–1549

    Article  Google Scholar 

  • Yoshida T, Jones LE, Ellner SP et al (2003) Rapid evolution drives ecological dynamics in a predator-prey system. Nature 424:303–306

    Article  PubMed  CAS  Google Scholar 

  • 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

    Google Scholar 

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Acknowledgments

The authors are indebted to R. Gradel and the “Palma Aquàrium” staff for providing facilities and invaluable assistance with the experiments. We would also like to thank E. Ballesteros, A. Ceballos, N. Comalada, E. Infantes, F.J. Medina, A. Sureda, and S. Deudero and her students for help in the field and the laboratory, as well as P. Fernandez from the “Serveis Científico Tècnics” University of Barcelona for assistance with C/N analyses. Financial support was provided by Grant CTM2005-01434/MAR from the Spanish Ministry of Science and Innovation. FT was funded by Juan de la Cierva Postdoctoral Fellowship.

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Tomas, F., Box, A. & Terrados, J. Effects of invasive seaweeds on feeding preference and performance of a keystone Mediterranean herbivore. Biol Invasions 13, 1559–1570 (2011). https://doi.org/10.1007/s10530-010-9913-6

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