Abstract
Several ecological models explain the success of introduced seaweeds by herbivore–prey interactions. The ‘enemy release hypothesis’ states that invaders benefit from a lack of natural enemies compared to the recipient community. The ‘novel weapons hypothesis,’ however, highlights the importance of chemical defense compounds of introduced species that are more effective in invaded regions than native counterparts. In order to explain the tremendous invasion success of the brown alga Sargassum muticum, we compared the palatability and nutritional value of S. muticum individuals from their native and invaded habitat (Japan and North Sea, respectively) with noninvasive congeneric species from Japan (S. fusiforme, S. horneri), and a native competitor from the North Sea (Fucus vesiculosus). Different feeding assays using artificial food with either freeze-dried algae or algal extracts and three dominant North Sea mesograzers were performed to detect feeding preferences. All herbivores preferred the local brown alga F. vesiculosus, followed by North Sea S. muticum, while Sargassum spp. from Japan were the least preferred. Since nutritional value did not correlate with feeding preference and algal extracts had the same effect as algal powder, we could demonstrate a deterrent activity of algal secondary metabolites. The preference of herbivores for the sympatric S. muticum population compared to the allopatric Japanese population could indicate a resource allocation from chemical defense to reproduction and growth. Due to the low palatability of Sargassum spp. from Japan, it might be reasonable to include additional Sargassum species in North Sea monitoring to prevent their establishment in European waters.
Similar content being viewed by others
References
Anderson LWJ (2007) Control of invasive seaweeds. Bot Mar 50:418–437. doi:10.1515/BOT.2007.045
Bazes A, Silkina A, Douzenel P et al (2009) Investigation of the antifouling constituents from the brown alga Sargassum muticum (Yendo) Fensholt. J Appl Phycol 21:395–403. doi:10.1007/s10811-008-9382-9
Blossey B, Notzold R (1995) Evolution of increased competitive ability in invasive nonindigenous plants—a hypothesis. J Ecol 83:887–889
Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254. doi:10.1016/0003-2697(76)90527-3
Cacabelos E, Olabarria C, Incera M, Troncoso JS (2010) Do grazers prefer invasive seaweeds? J Exp Mar Bio Ecol 393:182–187. doi:10.1016/j.jembe.2010.07.024
Callaway RM, Ridenour WM (2004) Novel weapons: invasive success and the evolution of increased competitive ability. Front Ecol Environ 2:436–443. doi:10.1890/1540-9295(2004)002[0436:NWISAT]2.0.CO;2
Cano L, Escarré J, Vrieling K, Sans FX (2009) Palatability to a generalist herbivore, defence and growth of invasive and native Senecio species: testing the evolution of increased competitive ability hypothesis. Oecologia 159:95–106. doi:10.1007/s00442-008-1182-z
Cappuccino N, Arnason JT (2006) Novel chemistry of invasive exotic plants. Biol Lett 2:189–193. doi:10.1098/rsbl.2005.0433
Cappuccino N, Carpenter D (2005) Invasive exotic plants suffer less herbivory than non-invasive exotic plants. Biol Lett 1:435–438. doi:10.1098/rsbl.2005.0341
Carlton JT (2009) Deep invasion ecology and the assembly of communities in historical time. Biol Invasions Mar Ecosyst 13–56. doi:10.1007/978-3-540-79236-9_2
Carpenter D, Cappuccino N (2005) Herbivory, time since introduction and the invasiveness of exotic plants. J Ecol 93:315–321. doi:10.1111/j.1365-2745.2005.00973.x
Cassano V, De-Paula JC, Fujii MT et al (2008) Sesquiterpenes from the introduced red seaweed Laurencia caduciramulosa (Rhodomelaceae, Ceramiales). Biochem Syst Ecol 36:223–226. doi:10.1016/j.bse.2007.07.005
Critchley AT (1983) Sargassum muticum—a taxonomic history including world-wide and western Pacific distributions. J Mar Biol Assoc United Kingdom 63:617–625
Cruz-Rivera E, Hay ME (2003) Prey nutritional quality interacts with chemical defenses to affect consumer feeding and fitness. Ecol Monogr 73:483–506. doi:10.1890/0012-9615(2003)073
Daehler CC (2003) Performance comparisons of co-occurring native and alien invasive plants: implications for conservation and restoration. Annu Rev Ecol Evol Syst 34:183–211. doi:10.1146/132403
Davidson AD, Campbell ML, Hewitt CL, Schaffelke B (2015) Assessing the impacts of nonindigenous marine macroalgae: an update of current knowledge. Bot Mar 58:55–79. doi:10.1515/bot-2014-0079
Deal MS, Hay ME, Wilson D, Fenical W (2003) Galactolipids rather than phlorotannins as herbivore deterrents in the brown seaweed Fucus vesiculosus. Oecologia 136:107–114. doi:10.1007/s00442-003-1242-3
Deysher L, Norton TA (1982) Dispersal and colonization in Sargassum muticum (Yendo) Fensholt. J Exp Mar Bio Ecol 56:179–195. doi:10.1016/0022-0981(81)90188-X
Dietz H, Edwards PJPJ (2006) Recognition that causal processes change during plant invasion helps explain conflicts in evidence. Ecology 87:1359–1367. doi:10.1890/0012-9658(2006)87[1359:RTCPCD]2.0.CO;2
Enge S, Nylund GM, Harder T, Pavia H (2012) An exotic chemical weapon explains low herbivore damage in an invasive alga. Ecology 93:2736–2745. doi:10.1890/12-0143.1
Engelen AH, Henriques N, Monteiro C, Santos R (2011) Mesograzers prefer mostly native seaweeds over the invasive brown seaweed Sargassum muticum. Hydrobiologia 669:157–165. doi:10.1007/s10750-011-0680-x
Engelen AH, Serebryakova A, Ang P, Britton-Simmons K, Mineur F, Pedersen MF, Arenas F et al (2015) Circumglobal invasion by the brown seaweed Sargassum muticum. Ocean Mar Biol Ann Rev 53:81–126
Forslund H, Wikström SA, Pavia H (2010) Higher resistance to herbivory in introduced compared to native populations of a seaweed. Oecologia 164:833–840. doi:10.1007/s00442-010-1767-1
Gao K, Hua W (1997) In Situ growth rates of Sargassum horneri (Fucales, Phaeophyta). Phycol. Res. 45:55–57
Halpern BS, Walbridge S, Selkoe KA et al (2008) A global map of human impact on marine ecosystems. Science 319(80):948–953. doi:10.1126/science.1149345
Hammann M, Wang G, Rickert E et al (2013) Invasion success of the seaweed Gracilaria vermiculophylla correlates with low palatibility. Mar Ecol Prog Ser 486:93–103. doi:10.3354/meps10361
Hammann M, Rempt M, Pohnert G, Wang G, Boo SM, Weinberger F (2016) Increased potential for wound activated production of Prostaglandin E2 and related toxic compounds in non-native populations of Gracilaria vermiculophylla. Harmful Algae 51:81–88. doi:10.1016/j.hal.2015.11.009
Hawkes CV (2007) Are invaders moving targets? The generality and persistence of advantages in size, reproduction, and enemy release in invasive plant species with time since introduction. Am Nat 170:832–843. doi:10.1086/522842
Hay ME, Kappel QE, Fenical W (1994) Synergisms in plant defenses against herbivores: Interactions of chemistry, calcification, and plant quality. Ecology 75:1714–1726
Hemmi A, Jormalainen V (2002) Nutrient enhancement increases performance of a marine herbivore via quality of its food alga. Ecology 83:1052–1064. doi:10.1890/0012-9658(2002)083[1052:NEIPOA]2.0.CO;2
Hemmi A, Jormalainen V (2004) Geographic covariation of chemical quality of the host alga Fucus vesiculosus with fitness of the herbivorous isopod Idotea baltica. Mar Biol 145:759–768. doi:10.1007/s00227-004-1360-4
Imrie DW, McCrohan CR, Hawkins SJ (1990) Feeding behaviour in Littorina littorea: a study of the effects of ingestive conditioning and previous dietary history on food preference and rates of consumption. Hydrobiologa 193:191–198
Jephson NA, Gray PWG (1977) Aspects of the ecology of Sargassum muticum (Yendo) Fensholt, in the Solent Region of the British Isles. 1. The growth cycle and epiphytes. In: Keegan BF, Boaden PJS, Ceidigh PO (eds) Biology of benthic organisms. 11th European symposium on marine biology. Pergamon Press, Oxford, pp 367–375
Johnsen KL, Halle LL, Karling ND (2013) Can grazer avoidance explain the invasiveness of the brown alga Sargassum muticum in Limfjorden, Denmark? Thesis, Roskilde Universitet, pp 12–17
Jormalainen V, Honkanen T, Heikkilä N (2001) Feeding preferences and performance of a marine isopod on seaweed hosts: cost of habitat specialization. Mar Ecol Prog Ser 220:219–230. doi:10.3354/meps220219
Josefsson M, Jansson K (2011) NOBANIS—invasive Alien Species fact sheet—Sargassum muticum. In: Online Database Eur. Netw. Invasive Alien Species—NOBANIS www.nobanis.org
Karlsson J, Loo LO (1999) On the distribution and continuous expansion of the Japanese seaweed—Sargassum muticum—in Sweden. Bot Mar 42:285–294. doi:10.1515/BOT.1999.032
Keane RM, Crawley MJ (2002) Exotic plant invasions and the enemy release hypothesis. Trends Ecol Evol 17:164–170. doi:10.1016/S0169-5347(02)02499-0
Kelly JR, Scheibling RE (2012) Fatty acids as dietary tracers in benthic food webs. Mar Ecol Prog Ser 446:1–22. doi:10.3354/meps09559
Kornmann P, Sahling PH (1994) Meeresalgen von Helgoland: Zweite Ergänzung. Helgoländer Meeresuntersuchungen 48:365–406. doi:10.1007/BF02366253
Le Cam S, Thiebaut CD, Bouchemousse S, Viard F (2015) Elucidating unresolved invasion history with genome-wide sequencing approach: the case of the global invader Sargassum muticum. Eur J Phycol 50:24–25. doi:10.1080/09670262.2015.1069489
Lind EM, Parker JD (2010) Novel weapons testing: are invasive plants more chemically defended than native plants? PLoS ONE. doi:10.1371/journal.pone.0010429
Marks LM, Salinas-Ruiz P, Reed DC et al (2015) Range expansion of a non-native, invasive macroalga Sargassum horneri (Turner) C. Agardh, 1820 in the eastern Pacific. BioInvasions Rec 4:243–248
Mattson WJJ (1980) Herbivory in relation to plant nitrogen content. Annu Rev Ecol Syst 11:119–161
Millennium Ecosystem Assessment (2005) Ecosystems and human well-being: synthesis. Island Press, Washington
Miller KA, Engle JM, Uwai S, Kawai H (2007) First report of the Asian seaweed Sargassum filicinum Harvey (Fucales) in California, USA. Biol Invasions 9:609–613. doi:10.1007/s10530-006-9060-2
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. doi:10.1007/s00227-009-1275-1
Morrison WE, Hay ME (2011) Herbivore preference for native vs. exotic plants: generalist herbivores from multiple continents prefer exotic plants that are evolutionarily naïve. PLoS ONE. doi:10.1371/journal.pone.0017227
Nejrup LB, Pedersen MF, Vinzent J (2012) Grazer avoidance may explain the invasiveness of the red alga Gracilaria vermiculophylla in Scandinavian waters. Mar Biol 159:1703–1712. doi:10.1007/s00227-012-1959-9
Nyberg CD, Wallentinus I (2005) Can species traits be used to predict marine macroalgal introductions? Biol Invasions 7:265–279. doi:10.1007/s10530-004-0738-z
Nylund GMN, Pereyra RT, Wood HL, Johannesson K (2012) Increased resistance towards generalist herbivory in the new range of a habitat-forming seaweed. Ecosphere 3:1–13. doi:10.1890/ES12-00203.1
Parker JD, Hay ME (2005) Biotic resistance to plant invasions? Native herbivores prefer non-native plants. Ecol Lett 8:959–967. doi:10.1111/j.1461-0248.2005.00799.x
Parker JD, Burkepile DE, Hay ME (2006) Opposing effects of native and exotic herbivores on plant invasions. Science 311(80):1459–1461
Pavia H, Åberg P (1996) Spatial variation in polyphenolic content of Ascophyllum nodosum (Fucales, Phaeophyta). Hydrobiologia 326:199–203
Pavia H, Toth GB, Åberg P (2002) Optimal defense theory: elasticity analysis as a tool to predict intraplant variation in defenses. Ecology 83:891–897. doi:10.2307/3071898
Pereira RC, da Gama BAP (2008) Macroalgal chemical defenses and their roles in structuring tropical marine communities. In: Amsler CD (ed) Algal chemical ecology. Springer, Berlin, Heidelberg, pp 25–49
Plouguerné E, Le Lann K, Connan S, Jechoux G, Deslandes E, Stiger-Pouvreau V (2006) Spatial and seasonal variation in density, reproductive status, length and phenolic content of the invasive brown macroalga Sargassum muticum (Yendo) Fensholt along the coast of Western Brittany (France). Aquat Bot 85:337–344
Plouguerné E, Hellio C, Deslandes E et al (2008) Anti-microfouling activities in extracts of two invasive algae: Grateloupia turuturu and Sargassum muticum. Bot Mar 51:202–208. doi:10.1515/BOT.2008.026
Plouguerné E, Ioannou E, Georgantea P et al (2010) Anti-microfouling activity of lipidic metabolites from the invasive brown alga Sargassum muticum (Yendo) Fensholt. Mar Biotechnol (NY) 12:52–61. doi:10.1007/s10126-009-9199-9
Polte P, Buschbaum C (2008) Native pipefish Entelurus aequoreus are promoted by the introduced seaweed Sargassum muticum in the northern Wadden Sea, North Sea. Aquat Biol 3:11–18. doi:10.3354/ab00071
Poore AGB, Campbell AH, Coleman RA et al (2012) Global patterns in the impact of marine herbivores on benthic primary producers. Ecol Lett 15:912–922. doi:10.1111/j.1461-0248.2012.01804.x
Rejmánek M, Richardson DM (1996) What attributes make some plant species more invasive? Ecology 77:1655–1661. doi:10.2307/2265768
Ribera M, Boudouresque C (1995) Introduced marine plants, with special reference to macroalgae: mechanisms and impact. Prog Phycol Res 11:187–268
Rohde S, Molis M, Wahl M (2004) Regulation of anti-herbivore defence by Fucus vesiculosus in response to various cues. J Ecol 92:1011–1018. doi:10.1111/j.0022-0477.2004.00936.x
Sabour B, Reani A, Magouri HEL, Haroun R (2013) Sargassum muticum (Yendo) Fensholt (Fucales, Phaeophyta) in Morocco, an invasive marine species new to the Atlantic coast of Africa. Aquat Invasions 8:97–102. doi:10.3391/ai.2013.8.1.11
Schaffelke B, Hewitt CL (2007) Impacts of introduced seaweeds. Bot Mar 50:397–417. doi:10.1515/9783110211344
Schaffelke B, Smith JE, Hewitt CL (2006) Introduced macroalgae—a growing concern. J Appl Phycol 18:529–541. doi:10.1007/s10811-006-9074-2
Schupp PJ, Paul VJ (1994) Calcium carbonate and secondary metabolites in tropical seaweeds: variable effects on herbivorous fishes. Ecology 75:1172–1185
Seabloom EW, Harpole WS, Reichman OJ, Tilman D (2003) Invasion, competitive dominance, and resource use by exotic and native California grassland species. Proc Natl Acad Sci USA 100:13384–13389. doi:10.1073/pnas.1835728100
Smith MD, Knapp AK (2001) Physiological and morphological traits of exotic, invasive exotic, and native plant species in tallgrass prairie. Int J Plant Sci 162:785–792. doi:10.1086/320774
Stæhr PA, Pedersen MF, Thomsen MS et al (2000) Invasion of Sargassum muticum in Limfjorden (Denmark) and its possible impact on the indigenous macroalgal community. Mar Ecol Prog Ser 207:79–88. doi:10.3354/meps207079
Tanniou A, Vandanjon L, Incera M et al (2014) Assessment of the spatial variability of phenolic contents and associated bioactivities in the invasive alga Sargassum muticum sampled along its European range from Norway to Portugal. J Appl Phycol 26:1–16. doi:10.1007/s10811-013-0198-x
Targett NM, Arnold TM (1998) Predicting the effects of brown algal phlorotannins on marine herbivores in tropical and temperate oceans. J Phycol 34:195–205. doi:10.1046/j.1529-8817.1998.340195.x
Thresher RE (1999) Key threats from marine bioinvasions: a review of current and future issues. In: Pederson J (ed) Marine bioinvasions: proceedings of the first national conference. Massachussetts Institute of Technology, Sea Grant College Program, Boston, pp 24–36
Toth GB, Karlsson M, Pavia H (2007) Mesoherbivores reduce net growth and induce chemical resistance in natural seaweed populations. Oecologia 152:245–255. doi:10.1007/s00442-006-0643-5
Trowbridge CD, Hirano YM, Hirano YJ (2009) Interaction webs of marine specialist herbivores on Japanese shores. J Mar Biol Assoc United Kingdom 89:277. doi:10.1017/S002531540900318X
van Alstyne KL (1995) Comparison of three methods for quantifying brown algal polyphenolic compounds. J Chem Ecol 21:45–58. doi:10.1007/BF02033661
van Kleunen M, Weber E, Fischer M (2010) A meta-analysis of trait differences between invasive and non-invasive plant species. Ecol Lett 13:235–245. doi:10.1111/j.1461-0248.2009.01418.x
Vas’kovskii VE, Isai SV (1972) Determination of the amount of mannitol in brown seaweeds. Chem Nat Compd 8:596–600. doi:10.1007/BF00564297
Vermeij MJA, Smith TB, Dailer ML, Smith CM (2009) Release from native herbivores facilitates the persistence of invasive marine algae: a biogeographical comparison of the relative contribution of nutrients and herbivory to invasion success. Biol Invasions 11:1463–1474. doi:10.1007/s10530-008-9354-7
Vitousek PM, Dantonio CM, Loope LL et al (1997) Introduced species: a significant component of human-caused global change. N Z J Ecol 21:1–16
Weinberger F, Buchholz B, Karez R, Wahl M (2008) The invasive red alga Gracilaria vermiculophylla in the Baltic Sea: adaptation to brackish water may compensate for light limitation. Aquat Biol 3:251–264. doi:10.3354/ab00083
Weinberger F, Rohde S, Oschmann Y et al (2011) Effects of limitation stress and of disruptive stress on induced antigrazing defense in the bladder wrack Fucus vesiculosus. Mar Ecol Prog Ser 427:83–94. doi:10.3354/meps09044
Wernberg T, Thomsen MS, Stæhr PA, Pedersen MF (2000) Comparative phenology of Sargassum muticum and Halidrys siliquosa (Phaeophyceae: Fucales) in Limfjorden, Denmark. Bot Mar 44:31–39. doi:10.1515/BOT.2001.005
Wikström SA, Steinarsdóttir MB, Kautsky L, Pavia H (2006) Increased chemical resistance explains low herbivore colonization of introduced seaweed. Oecologia 148:593–601
Yendo K (1907) The Fucaceae of Japan. J Coll Sci Tokyo Imp Univ 21(12):1–174
Zhang Q, Zhang J, Shen J et al (2006) A Simple 96-well microplate method for estimation of total polyphenol content in seaweeds. J Appl Phycol 18:445–450. doi:10.1007/s10811-006-9048-4
Zou D (2005) Effects of elevated atmospheric CO2 on growth, photosynthesis and nitrogen metabolism in the economic brown seaweed, Hizikia fusiforme (Sargassaceae, Phaeophyta). Aquaculture 250:726–735. doi:10.1016/j.aquaculture.2005.05.014
Acknowledgments
We would like to thank Fabian Heinke and Johanna Meinecke (ICBM, Germany) for algal nutrients extraction as well as two anonymous reviewers and Jutta Nietzer for valuable comments. NS was supported by the research-orientated teaching program at the University of Oldenburg.
Author information
Authors and Affiliations
Corresponding authors
Ethics declarations
Conflict of interest
The authors declare that they have no potential conflict of interest.
Ethical approval
All applicable international, national, and/or institutional guidelines for the collection, care and use of organisms were followed.
Additional information
Responsible Editor: F. Weinberger.
Reviewed by undisclosed experts.
This article is part of the Topical Collection on Invasive Species.
Rights and permissions
About this article
Cite this article
Schwartz, N., Rohde, S., Hiromori, S. et al. Understanding the invasion success of Sargassum muticum: herbivore preferences for native and invasive Sargassum spp. Mar Biol 163, 181 (2016). https://doi.org/10.1007/s00227-016-2953-4
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s00227-016-2953-4