Biological Invasions

, Volume 11, Issue 6, pp 1463–1474 | Cite as

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

  • M. J. A. VermeijEmail author
  • T. B. Smith
  • M. L. Dailer
  • C. M. Smith
Original Paper


The effect of herbivory and nutrient enrichment on the growth of invasive and native macroalgal species was simultaneously studied in two biogeographic regions: the Caribbean and Hawaii. Herbivores suppressed growth of invasive algae in their native (Caribbean) and invaded range (Hawaii), but despite similar levels of herbivore biomass, the intensity of herbivory was lower in Hawaii. Algal species with a circumtropical distribution did not show a similar effect of herbivores on their growth. Nutrient enrichment did not enhance growth of any algal species in either region. The reduction in herbivore intensity experienced by invasive algae in Hawaii rather than an escape from (native) herbivores provided invasive macroalgae with “enemy release” sensu the Enemy Release Hypothesis (ERH). Since native, Hawaiian herbivores still feed and even prefer invasive algae over native species, invasion scenario’s that involve predation (e.g. the ERH) could be falsely dismissed when invasive species are only studied in their invasive range. We therefore argue that escape from herbivores (i.e. enemy release) can only effectively be determined with additional information on the intensity of predation experienced by an invasive species in its native range.


Herbivory Macroalgae Invasive species Enemy Release Hypothesis Resource Hypothesis Hawaii Caribbean Invasive algae Nutrient enrichment 



The Hawaii Department of Aquatic Resources (DAR) is thanked for their help with permitting procedures. The CARMABI foundation is thanked for logistical support on Curaçao. Stuart Sandin is thanked for constructive criticism on earlier versions of this MS. This research was supported by a grant to CMS, number NA03NOS4780020, from the Center for Sponsored Coastal Ocean Research, National Ocean Service, NOAA. This is ECOHAB publication 293.


  1. Blumenthal DM (2006) Interactions between resource availability and enemy release in plant invasion. Ecol Lett 9:887–895. doi: 10.1111/j.1461-0248.2006.00934.x PubMedCrossRefGoogle Scholar
  2. Burkepile DE, Hay ME (2006) Herbivore versus nutrient control of marine primary producers: context-dependent effects. Ecology 87:3128–3139. doi: 10.1890/0012-9658(2006)87[3128:HVNCOM]2.0.CO;2 PubMedCrossRefGoogle Scholar
  3. Callaway RM, Thelen G, Rodriguez A, Holben WE (2004) Release from inhibitory soil biota in Europe and positive plant-soil feedbacks in North America promote invasion. Nature 427:731–733. doi: 10.1038/nature02322 PubMedCrossRefGoogle Scholar
  4. Carlton JT (1989) Man’s role in changing the face of the ocean: biological invasions and implications for conservation of near-shore environments. Conserv Biol 3:265–273. doi: 10.1111/j.1523-1739.1989.tb00086.x CrossRefGoogle Scholar
  5. Carpenter RC (1986) Partitioning herbivory and its effects of coral reef algal communities. Ecol Monogr 56:345–364. doi: 10.2307/1942551 CrossRefGoogle Scholar
  6. Carreiro-Silva M, McClanahan TR, Kiene WE (2005) The role of inorganic nutrients and herbivory in controlling microbioerosion of carbonate substratum. Coral Reefs 24:214–221. doi: 10.1007/s00338-004-0445-3 CrossRefGoogle Scholar
  7. Colautti RI, Ricciardi A, Grigorovich IA, MacIsaac HJ (2004) Is invasion success explained by the enemy release hypothesis? Ecol Lett 7:721–733. doi: 10.1111/j.1461-0248.2004.00616.x CrossRefGoogle Scholar
  8. Coles SL, Eldredge LG (2002) Nonindigenous species introductions on coral reefs: a need for information. Pac Sci 56:191–209. doi: 10.1353/psc.2002.0010 CrossRefGoogle Scholar
  9. Conklin EJ (2007) Ph.D. Dissertation, University of Hawaii, Honolulu, HawaiiGoogle Scholar
  10. Daehler CC (2003) Performance comparisons of co-occurring native and alien invasive plants: implications for conservation and restoration. Annu Rev Ecol Syst 34:183–211. doi: 10.1146/annurev.ecolsys.34.011802.132403 CrossRefGoogle Scholar
  11. Davis MA, Grime JP, Thompson K (2000) Fluctuating resources in plant communities: a general theory of invasibility. J Ecol 88:528–534. doi: 10.1046/j.1365-2745.2000.00473.x CrossRefGoogle Scholar
  12. DeWalt SJ, Denslow JS, Ickes K (2004) Natural-enemy release facilitates habitat expansion of the invasive tropical shrub Clidemia hirta. Ecology 95:471–483. doi: 10.1890/02-0728 CrossRefGoogle Scholar
  13. Flagella MM, Verlaque M, Soria A, Buia MC (2007) Macroalgal survival in ballast water tanks. Mar Pollut Bull 54:1395–1401. doi: 10.1016/j.marpolbul.2007.05.015 PubMedCrossRefGoogle Scholar
  14. Harlin MM (1993) Changes in major plant groups following nutrient enrichment. In: McComb AJ (ed) Eutrophic shallow Estuaries and lagoons. CRC Press Inc., Boca Raton, pp 173–187Google Scholar
  15. Hay ME (1991) Marine-terrestrial contrasts in the ecology of plant chemical defenses against herbivores. Trends Ecol Evol 6:362–365. doi: 10.1016/0169-5347(91)90227-O CrossRefGoogle Scholar
  16. Hay ME, Steinberg PD (1992) The chemical ecology of plant-herbivore interactions in marine versus terrestrial communities. In: Rosenthal J, Berenbaum M (eds) Herbivores: their interaction with secondary metabolites, evolutionary and ecological processes. Academic Press, San Diego, pp 371–413Google Scholar
  17. Hedges LV, Gurevitch J, Curtis PS (1999) The meta-analysis of response ratios in experimental ecology. Ecology 80:1150–1156CrossRefGoogle Scholar
  18. Hierro JL, Maron JL, Callaway RM (2005) A biogeographical approach to plant invasions: the importance of studying exotics in their introduced and native range. J Ecol 93:5–15. doi: 10.1111/j.0022-0477.2004.00953.x CrossRefGoogle Scholar
  19. Hinz HL, Schwarzlaender M (2004) Comparing invasive plants from their native and exotic range: what can we learn for biological control? Weed Technol 18:1533–1541CrossRefGoogle Scholar
  20. Inderjit , Chapman D, Ranelletti M, Kaushik S (2006) Invasive marine algae: an ecological perspective. Bot Rev 72:153–178. doi: 10.1663/0006-8101(2006)72[153:IMAAEP]2.0.CO;2 CrossRefGoogle Scholar
  21. Jackson JBC, Kirby MX, Berger WH, Bjorndal KA, Botsford LW, Bourque BJ et al (2001) Historical overfishing and the recent collapse of coastal ecosystems. Science 293:629–637. doi: 10.1126/science.1059199 PubMedCrossRefGoogle Scholar
  22. 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 CrossRefGoogle Scholar
  23. Littler MM, Littler DS, Brooks BL, Lapointe BE (2006) Nutrient manipulation methods for coral reef studies: a critical review and experimental field data. J Exp Mar Biol Ecol 336:242–253. doi: 10.1016/j.jembe.2006.05.014 CrossRefGoogle Scholar
  24. Mineur F, Johnson MP, Maggs CA, Stegenga H (2007) Hull fouling on commercial ships as a vector of macroalgal introduction. Mar Biol (Berl) 151:1299–1307. doi: 10.1007/s00227-006-0567-y CrossRefGoogle Scholar
  25. Mooney HA, Hobbs RJ (2000) Invasive species in a changing world. Island Press, WashingtonGoogle Scholar
  26. Newman MJH, Paredes GA, Sala E, Jackson JBC (2006) Structure of Caribbean coral reef communities across a large gradient of fish biomass. Ecol Lett 9:1216–1227. doi: 10.1111/j.1461-0248.2006.00976.x PubMedCrossRefGoogle Scholar
  27. 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 CrossRefGoogle Scholar
  28. Parker JD, Burkepile DE, Hay ME (2006) Opposing effects of native and exotic herbivores on plant invasions. Science 311:1459–1461. doi: 10.1126/science.1121407 PubMedCrossRefGoogle Scholar
  29. Pimentel D, Zuniga R, Morrison D (2005) Update on the environmental and economic costs associated with alien invasive species in the U.S. Ecol Econ 52:273–288. doi: 10.1016/j.ecolecon.2004.07.013 Google Scholar
  30. Reinhart KO, Packer A, van der Putten WH, Clay K (2003) Plant-soil biota interactions and spatial distribution of black cherry in its native and invasive ranges. Ecol Lett 6:1046–1050. doi: 10.1046/j.1461-0248.2003.00539.x CrossRefGoogle Scholar
  31. Ricciardi A, Ward JM (2006) Comment on “Opposing effects of native and exotic herbivores on plant invasions”. Science 313:298. doi: 10.1126/science.1128946 PubMedCrossRefGoogle Scholar
  32. Russell DJ (1992) The ecological invasion of Hawaiian reefs by two marine red algae, Acanthophora spicifera (Vahl) Bøerg. and Hypnea musciformis (Wulfen) J.Ag., and their association with two native species, Laurencia nidifica and Hypnea cervicornis J Ag. ICES Mar Sci Symp 194:110–125Google Scholar
  33. Russell DJ, Balazs GH (2000) Identification manual for dietary vegetation of the Hawaiian green turtle, Chelonia mydas. NOAA TM-NMFS-SWFSC 294:1–49Google Scholar
  34. Sandin SA, Smith JE, DeMartini EE, Dinsdale EA, Donner SD, Friedlander AM et al (2008) Degradation of coral reef communities across a gradient of human disturbance. PLoS One 3:e1548. doi: 10.1371/journal.pone.0001548 PubMedCrossRefGoogle Scholar
  35. Sandin SA, Sampayo E, Vermeij MJA (in press) The distribution of reef fish on Curacao and Bonaire. Caribb J SciGoogle Scholar
  36. 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 CrossRefGoogle Scholar
  37. Smith JE, Hunter CL, Smith CM (2001) The effects of herbivory and nutrient enrichment on benthic community structure and development on a Hawaiian Reef. Coral Reefs 19:332–342Google Scholar
  38. Smith JE, Hunter CL, Smith CM (2002) Distribution and reproductive characteristics of nonindigenous and invasive marine algae in the Hawaiian Islands. Pac Sci 56:299–315. doi: 10.1353/psc.2002.0030 CrossRefGoogle Scholar
  39. Smith JE, Runcie JW, Smith CM (2005) Characterization of a large-scale ephemeral bloom of the green alga Cladophora sericea on the coral reefs of West Maui, Hawai’i. Mar Ecol Prog Ser 302:77–91. doi: 10.3354/meps302077 CrossRefGoogle Scholar
  40. Stimson J, Larned ST, Conklin E (2001) Effects of herbivory, nutrient levels, and introduced algae on the distribution and abundance of the invasive macroalgae Dictyosphaeria cavernosa in Kaneohe Bay, Hawaii. Coral Reefs 19:343–357Google Scholar
  41. Torchin ME, Lafferty KD, Dobson AP, McKenzie VJ, Kuris AM (2003) Introduced species and their missing parasites. Nature 421:628–630. doi: 10.1038/nature01346 PubMedCrossRefGoogle Scholar
  42. Vitousek PM, D’Antonio CM, Loope LL, Rejmánek M, Westbrooks R (1997) Introduced species and global change. N Z J Ecol 21:1–16Google Scholar
  43. Williams SL, Smith JE (2007) A global review of the distribution, taxonomy, and impacts of introduced seaweeds. Annu Rev Ecol Evol Syst 38:327–359. doi: 10.1146/annurev.ecolsys.38.091206.095543 CrossRefGoogle Scholar
  44. Wolfe LM (2002) Why alien invaders succeed: support for the escape-from-enemy hypothesis. Am Nat 160:705–711. doi: 10.1086/343872 PubMedCrossRefGoogle Scholar
  45. World Conservation Monitoring Centre (1992) Global biodiversity. Chapman & Hall, LondonGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2008

Authors and Affiliations

  • M. J. A. Vermeij
    • 1
    • 2
    Email author
  • T. B. Smith
    • 3
  • M. L. Dailer
    • 1
  • C. M. Smith
    • 1
  1. 1.Department of BotanyUniversity of Hawai’iHonoluluUSA
  2. 2.CARMABI FoundationWillemstadNetherlands Antilles
  3. 3.Center for Marine and Environmental StudiesUniversity of the Virgin IslandsSt. ThomasUSA

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